Salmonella Enteritidis in Eggs

DEPARTMENT OF AGRICULTURE

Food Safety and Inspection Service

7 CFR Part 59

[Docket No. 96-035A]

RIN 0583-AB

DEPARTMENT OF HEALTH AND HUMAN SERVICES

Food and Drug Administration

21 CFR Part 100

[Docket No. 97N-0322]

RIN 0583-AC52

Salmonella Enteritidis in Eggs

AGENCIES: Food Safety and Inspection Service, USDA; Food and Drug

Administration, HHS.

ACTION: Advance notice of proposed rulemaking; request for comments.

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SUMMARY: Eggs contaminated with Salmonella Enteritidis (SE) are

associated with significant numbers of human illnesses and continue to

be a public health concern. SE infected flocks have become prevalent

throughout the country, and large numbers of illnesses have been

attributed to consumption of mishandled SE-contaminated eggs. As a

result, there have been requests for Federal action to improve egg

safety. The Food Safety and Inspection Service (FSIS) and the Food and

Drug Administration (FDA) share Federal regulatory responsibility for

egg safety. However, regulation of shell eggs is primarily the

responsibility of FDA. Through joint issuance of this notice, FSIS and

FDA are seeking to identify farm-to-table actions that will decrease

the food safety risks associated with shell eggs. The agencies want to

explore all reasonable alternatives and gather data on the public

benefits and the public costs of various regulatory approaches before

proposing a farm-to-table food safety system for shell eggs. Interested

persons are requested to comment on the alternatives discussed in this

advance notice of proposed rulemaking (ANPR), suggest other possible

approaches, and provide information that will help the agencies weigh

the merits of all alternatives. In addition to the actions contemplated

in this ANPR, both agencies are planning to take actions that address

adoption of refrigeration and labeling requirements that are designed

to reduce the risk of foodborne illness.

DATES: Comments must be received on or before August 17, 1998.

ADDRESSES: Send an original and two copies of comments to: FSIS Docket

Clerk, Docket No. 96-035A, Room 102 Cotton Annex Building, 300 12th St,

SW., Washington, DC 20250-3700. Reference material cited in this

document and any comments received will be available for public

inspection in the FSIS Docket Room from 8:30 a.m. to 1:00 p.m. and 2:00

p.m. to 4:30 p.m., Monday through Friday.

FOR FURTHER INFORMATION CONTACT: Mr. Ralph Stafko, Food Safety and

Inspection Service, USDA, Washington, DC, 20250, (202) 720-7774, or Dr.

Marilyn Balmer, Center for Food Safety and Applied Nutrition, Food and

Drug Administration, HHS, Washington, DC 20204, (202) 205-4400.

SUPPLEMENTARY INFORMATION:

Table of Contents

Background

1. Egg production and marketing.

2. Salmonella and the salmonellosis epidemic.

3. Salmonella in eggs; the risk.

--Contamination through the shell; current cleaning practices

--Transovarian contamination of eggs with SE

4. Mitigating the risk; current efforts.

--Production: preventing introduction of SE into laying flocks

and from hens to eggs.

--Processing and distribution: preventing growth of SE in eggs.

--Rewashing/repackaging: preventing growth of SE in eggs.

--Preparation and consumption: preventing ingestion of SE from

eggs.

5. Current regulation of shell eggs.

6. Need for additional information and analysis.

Information Requested

Background

This section provides information on the egg industry, data that

associate eggs with an epidemic of cases of human salmonellosis caused

by Salmonella Enteritidis, and past efforts and current plans to

alleviate this public health problem.

1. Egg Production and Marketing

Eggs are a nutrient-dense food that play an important part in most

Americans' diets, either alone or as a constituent of another food. On

a per capita basis, Americans consume about 234 eggs a year. The

National Agriculture Statistics Service (NASS) of the Department of

Agriculture (USDA) estimates the total value of the table eggs (eggs

produced for human consumption, not hatching) produced in the U.S. in

1995 at $3.96 billion.

The egg industry is fairly stable in terms of overall production.

U.S. production has increased only slightly in absolute terms in recent

years, from about 60 billion eggs in 1984 to about 63 billion in 1995.

About 70 percent are sold as whole ``shell'' eggs. The remaining 30

percent are processed into liquid, frozen or dried pasteurized egg

products, the majority of which are destined for institutional use or

further processing into other foods such as cake mixes, pasta, ice

cream, mayonnaise, and bakery goods.

International trade is a small but growing part of the U.S. egg

market. The U.S. does not import a significant quantity of shell eggs

and imports only 0.2 percent of processed egg products. Exports now

amount to more than 2 percent of the total U.S. production. In 1996,

exports of eggs and egg products reached a market value of nearly $20

million.

There are essentially three kinds of flocks associated with egg

production: breeder flocks, multiplier flocks, and laying flocks

(including both immature pullets and mature laying hens). There are

roughly 300,000 breeding hens (grandparents), 3 million multipliers

(parents), and 300 million laying hens. NASS estimates the value of the

laying flocks alone to be close to $1 billion.

Geographically, commercial egg production in the western United

States is concentrated in California, and in the east it is centered in

Ohio, Indiana, and Pennsylvania. According to NASS, which surveys the

number of egg laying flocks of 30,000 or more hens, California and Ohio

each have about 25 million layers, and Indiana and Pennsylvania each

have about 20 million. Other states in which major producers are

located

[[Page 27503]]

include Iowa, Texas, Minnesota, and Georgia. Twenty-one other states

are reported as having fewer than 10 million, but more than 2 million,

layers in production.

Egg production is being concentrated in fewer, larger firms.

Federal Regulations require commercial flocks of more than 3,000 hens

to be registered with USDA. USDA's Agricultural Marketing Service (AMS)

currently has 757 such egg producers registered. The United Egg

Producers (UEP), a cooperative that provides a variety of services to

member egg producers, reports that the number of major producers (those

with flocks of 75,000 or more, which produce about 94 percent of

America's table eggs) declined in just 3 years from 380 producers in

1994 to 329 producers in 1996.

Modern egg production facilities are increasingly large, ``in-

line'' facilities. They integrate laying, packing, and even processing

of egg products at one location. Freshly laid eggs go directly into a

processing system where they are cleaned, sorted, and packed for

distribution.

A significant portion of production, however, is still ``off-

line.'' Off-line operations are those that are not integrated with

laying facilities, but rather have eggs shipped from laying facilities

at other locations. The fresh eggs are collected and shipped from the

laying facilities periodically, usually once a day but sometimes less

often. These eggs are frequently placed in coolers at the laying

facility before shipment to a facility where they are processed and

packed.

Most packers either own or have contractual relationships with

their suppliers. Their laying hens are bred and cared for to ensure the

largest possible numbers of consistent quality eggs, and are housed

together in large hen houses.

Although shell egg cleaning and packing is configured differently

in different plants, after collection the eggs generally are (1)

washed, (2) rinsed and sanitized, (3) dried, (4) candled, sorted, and

graded, (5) packed in cartons and crates onto shipping pallets, and (6)

placed in a cooler pending shipment. Eggs that are found to be cracked

or otherwise unsuitable for sale as whole shell eggs are by law

``restricted.'' USDA allows a certain percentage of some classes of

restricted eggs to be moved in commerce. If restricted eggs sent to a

federally inspected facility (often referred to as a ``breaker plant'')

are determined acceptable, they are broken, inspected for

wholesomeness, pooled, and then processed into a pasteurized liquid,

frozen, or dried egg product.

After packing, shell eggs usually are loaded into refrigerated

transports for shipment to market. Some producers use their own trucks,

while others contract with trucking firms to deliver eggs to their

customers. Some are delivered directly to retail outlets, and others

are delivered to warehouses and other intermediate distribution points

before going to the retail store or food service facility where they

reach the consumer.

2. Salmonella and the Salmonellosis Epidemic

Salmonella is a gram-negative, motile, rod-shaped bacteria that can

grow under both aerobic and anaerobic conditions. Salmonella has

evolved into a successful human pathogen because of its survival

characteristics and virulence. The organisms are ubiquitous, and are

commonly found in the digestive tracts of animals, especially birds and

reptiles. Human illnesses are usually associated with ingestion of food

or drink contaminated with Salmonella, but infection may also be

acquired from an infected person by the fecal-oral route through poor

personal hygiene, or from pets.

More than 2,300 different serotypes have been identified and are

associated with a variety of animal reservoirs, geographic locations,

and frequencies. However, microbiologists are finding that atypical

biotypes have emerged that are difficult to identify and detect by

conventional means, placing more value on new molecular methods and

other technologies for identifying them.\1\

Epidemiologically, salmonellae can be grouped as follows:

1. Those that infect mainly humans. These include human pathogens

such as S. Typhi and S. Paratyphi (A and C) which cause typhoid

(enteric) and paratyphoid fevers, respectively, the most severe of the

Salmonella diseaseS. S. Typhi may be found in blood, as well as in

stool and urine before enteric fever develops. Typhoid fever has a high

mortality rate; the paratyphoid syndrome is generally milder. These

diseases are spread through food and water contaminated by feces and

urine of patients and carriers.\2\

2. Those that infect mainly animals. These include animal pathogens

such as S. Gallinarum (poultry), S. Dublin (cattle), S. Abortus-ovis

(sheep), and S. Choleraesuis (swine). Some of the organisms in this

group are also human pathogens and can be contracted through foods.

In general, salmonellae are quite resilient and able to adapt to

extremes in environmental conditions. They are resistant to freezing

and drying. They are able to grow within a wide temperature range; from

extremes as low as 2-4 deg.C (36-39 deg.F), and as high as 54 deg.C

(129 deg.F). They have been reported to grow within a pH range of 4.5

to 9.5. Salmonellae do not grow in foods with a water activity of 0.93

or less, and are inhibited by the presence of salt at levels between 3

and 4 percent. Preconditioning to thermal and acid stress has been

shown to allow strains to adapt to greater extremes.\3\ These

properties make many food products more likely to support the growth of

these organisms, such as many refrigerated products, fermented foods,

and cheeses.

The human infectious dose is highly variable, depending largely on

the strain, the food, and the susceptibility of the human host. Recent

evidence suggests that as few as one to ten Salmonella cells can cause

infection in humans. Human diarrheagenic response and enterocolitis

result from the migration of the pathogen from the mouth at ingestion

to the intestinal tract and mesenteric lymph nodes, and the coinciding

production of bacterial enterotoxin. Salmonella also produce a

cytotoxin that inhibits protein synthesis and causes lysis of host

cells, helping the organisms to spread to other tissues.\4\

The Centers for Disease Control and Prevention (CDC), which has

classified salmonellosis as a reportable disease since 1943, has found

it to be one of the most commonly reported bacterial infections of any

kind in the United States. Human salmonellosis is the second most

prevalent foodborne disease in the U.S. after illnesses from

Campylobacter (a generally milder illness associated with raw and

undercooked poultry, raw milk, and untreated water as well as improper

handling and preparation of food). In 1996, 39,027 confirmed cases of

human salmonellosis were reported to CDC by State and local departments

of health. Although this number of cases is below the peak year of

1985, when 57,896 cases were reported, the number of cases is

significant. From 1985 through 1996, there have been 508,673 reported

cases of salmonellosis.\5\

Salmonella usually cause an intestinal infection accompanied by

diarrhea, fever, and abdominal cramps starting 6 to 72 hours after

consuming a contaminated food or drink. The illness is usually 4 to 7

days in duration, and most people recover without antibiotic treatment.

About 2 percent of affected persons may later develop recurring joint

pains and arthritis.\6\ In

[[Page 27504]]

the very young, the elderly, and persons with compromised immune

systems, the infection can spread to the bloodstream, and then to other

areas of the body such as the bone marrow or the meningeal linings of

the brain, leading to a severe and occasionally fatal illness unless

treated promptly with antibiotics.\7\

Because many cases are not reported, these cases may represent only

a small fraction of the actual number of illnesses that occur. Not all

infected persons develop symptoms severe enough that they seek medical

attention, and physicians may not have patients' stool analyzed. It is

estimated that there are an additional 20 to 100 cases of salmonellosis

for every reported case, or some 800,000 to 4 million actual cases each

year in the U.S.\8\

The cost to Americans is considerable. The patient-related costs of

salmonellosis from medical expenses and loss of income were estimated

in 1988 to be about $1,560 per reported case and about $250 for each

unreported case.\9\ By applying the cost per reported case to the

41,222 cases and probable illnesses reported in 1995, the cost of

salmonellosis in 1995 can be estimated to be between $350 million and

$1.5 billion.

CDC's surveillance data on isolates reported by State and

territorial epidemiologists list close to 600 different serotypes that

have caused human illness in the U.S. Based primarily on outbreak data,

where Federal, State, and local epidemiologists have sought to identify

the source of infection, some serotypes are linked to particular food

vehicles. The three illness-causing serotypes most frequently

reported--S.Typhimurium, S. Heidelberg, and S. Enteritidis--are most

often traced to poultry or eggs when a food vehicle is found.

Salmonella Enteritidis emerged in epidemic proportions in the

United States about a decade ago in the northeast. Over the last 20

years, SE-associated illnesses have increased greatly in number. The

proportion of reported Salmonella isolates that were SE increased from

5 percent in 1976 to 26 percent in 1994.\10\ SE was the most frequently

reported Salmonella serotype in 1994, 1995, and 1996.

CDC surveillance data show that the rates of isolation of SE

increased in the U.S. during 1976-1994 from 0.5 to 3.9 per 100,000

population, and that illnesses are occurring throughout the U.S. While

the trends for the years 1990-1994 show a decrease in the SE isolation

rate in the northeast from 8.9 to 7.0 per 100,000 population, the rate

increased approximately threefold for the Pacific region, particularly

for southern California, which had rates as high as 14 per 100,000.\11\

From 1985 through 1996, there have been 660 SE outbreaks reported

to CDC. Associated with these outbreaks, there have been 77 reported

deaths, 2,508 reported hospitalizations, and 25,935 reported cases of

illness. The peak year for outbreaks was 1989 with 77 reported. Deaths

have occurred in all years. In 1995 and 1996, there were 57 and 51

reported outbreaks respectively with 8 deaths in 1995 and 2 deaths in

1996. The majority of the outbreaks occur in the commercial venue with

the implicated food containing undercooked eggs.

There is evidence that this increase in SE infections is global.

World Health Organization data show increases in SE on several

continents, including North America, South America, Europe, and perhaps

Africa.\12\ The trend towards centralized large-scale food processing

with wide distribution means that when contamination occurs, it can

affect large numbers of people over a large area. Although most eggs

are consumed individually, large numbers are sometimes pooled during

the production or preparation of some foods. This increases the

likelihood of SE being in the raw product. This potential was

illustrated by a major 1994 SE outbreak attributed to ice cream. FDA

reported the most likely cause was contamination of the pasteurized ice

cream mix by hauling it in a tanker improperly cleaned after carrying a

load of unpasteurized liquid eggs. The ice cream mix was not heat

treated after receipt from the contaminated tanker, and the ice cream

was distributed widely.\13\

In 1995 surveys, SE phage-type 13A was found to be the predominant

phage-type in egg laying flocks in the United States, followed by

phage-type 8 and, increasingly, phage-type 4. This represents a

significant change since 1991, when phage-type 8 was predominant and

phage-type 4 was undetected in laying flocks.\14\

3. Salmonella in Eggs; the Risk

a. Contamination Through the Shell; Current Egg Cleaning Practices

Eggs have long been valued for their natural protective packaging.

Having evolved to protect the developing embryonic bird inside, the egg

provides an inhospitable environment for Salmonella as well as other

bacterial contaminants. A fresh egg is fairly resistant to invasive

bacteria, a fact relied upon in many countries where shell eggs are not

refrigerated. The egg's defenses are both mechanical and chemical.

Mechanically, there are essentially four layers of protection

preventing bacteria from reaching the nutrient rich yolk: (1) the

shell, (2) the two membranes (inner and outer) between the shell and

the albumen, (3) the albumen (eggwhite), and (4) the vitelline (yolk)

membrane which holds the yolk.

When laid, the egg shell is covered on the outside by the cuticle,

a substance similar in composition to the shell membranes. When the

cuticle dries, it seals the pores and hinders initial bacterial

penetration. However, the cuticle usually is removed along with debris

on the surface of the shell during the cleaning process. Some

processors add a thin coating of edible oil or wax to eggs after they

are washed and dried to close the shell pores in a manner similar to

the cuticle.

The shell, although porous and easily penetrated by bacteria,

protects the outer membrane from physical abuse. The dry and much less

porous outer shell membrane is much more difficult for bacteria to

penetrate. The inner shell membrane and the yolk membrane also present

barriers. Perhaps the most substantial line of defense against bacteria

is provided by the egg albumen.

In fresh eggs, the albumen has a high viscosity, which both anchors

the yolk protectively in the center of the shell and prevents movement

of bacteria toward the yolk. (Eggs are stored with the blunt end up to

help keep the yolk, which has a lower specific gravity, from drifting

toward the inner membrane.) In addition, the albumen has chemical

properties that inhibit bacterial growth.

Originally, the potential for Salmonella to contaminate shell eggs

was primarily a matter of the organisms passing through the shell into

the egg's contents because of, mostly, environmental conditions. With

salmonellae other than SE, this still is the most likely means of

potential contamination of intact shell eggs.\15\

It has long been known that the laying environment can contribute

to egg shell contamination. The surface of the egg can become

contaminated with virtually any microorganism that is excreted by the

birds. Many serotypes of Salmonella as well as other bacteria have been

isolated from laying flocks. Contact with feces, nesting material,

dust, feedstuffs, shipping and storage containers, human beings, and

other creatures all contribute to the likelihood of shell

contamination. Penetration into the egg contents by both salmonella and

spoilage bacteria increases with duration of contact with contaminated

material, especially during storage at

[[Page 27505]]

high temperatures and high relative humidities. Therefore, eggs should

be collected as frequently as possible, and kept as clean and cool as

possible (short of freezing, which can damage the shell).

Other sources of shell contamination are always present in the

production environment. Producers should clean and sanitize equipment

and facilities as necessary to prevent egg contamination, and not rely

simply on egg washing to remove contaminants after the fact. One recent

study found high levels of Salmonella isolates from egg belts, egg

collectors, and ventilation fans (64-100 percent of samples on

different farms) as compared to isolates from egg shells before

collection (8 percent overall).

Cleaning the exteriors of shell eggs to remove fecal material and

other debris reduces the risk that pathogenic bacteria will have an

opportunity to penetrate the egg shell. The cleaning process provides

consumers with clean egg surfaces not likely to promote contamination

of the egg by penetration of bacteria through the intact shell or by

cross contamination upon cracking open the egg for use.

Most modern egg washing machines are spray-washers. The typical

continuous egg washer consists of three stages: a wash chamber where

the eggs are washed with warm water and detergent using moving brushes

or high pressure jets, a rinse chamber which usually includes a

sanitizing agent, and a drying chamber.

If not done properly, washing can contribute to microbial

contamination of the egg's contents and may contribute to increased

spoilage rates. Organisms have the potential to concentrate in the

recirculating wash water, and the liquid can be aspirated into the egg

through the shell under certain conditions. In particular, when wash

water outside the egg shell is colder than the eggs' contents, as the

eggs' contents cool it creates low pressure on the inside of the egg

shell that draws liquid outside the shell into the egg through the

shell's pores. This observation led to the USDA egg grading requirement

that wash water be at least 20 deg. F warmer than the eggs being

washed. Typically, U.S. processors use a hot wash water (110-120 deg.

F) to ensure temperatures hostile to most organisms that may collect in

the wash water as well as to ensure that the 20 deg. F egg-wash water

temperature difference is maintained even when cleaning quite warm

eggs, which are common in in-line facilities. However, the use of hot

water damages or removes the cuticle, which if left intact, helps

prevent bacterial contamination.

After washing, the eggs should be quickly and completely dried to

reduce the risk that any bacteria remaining on the surface of the eggs

are aspirated into the eggs as they cool to ambient temperature. They

must be handled carefully thereafter to avoid recontamination.

b. Transovarian Contamination of Egg Contents With SE

The increase in SE outbreaks associated with shell eggs in the

1970's and 1980's raised suspicions of transovarian contamination.\16\

This mode of contamination was confirmed by an experiment in which

laying hens were infected with SE and found to produce eggs

contaminated with the same strain of SE.\17\ The site of infection is

usually the albumen near the yolk membrane.

Based on USDA data, it can be estimated that such transovarian SE

contamination occurs in about 1 out of every 10,000 eggs produced in

the U.S. This prevalence is based on a model applying data on the

frequency of SE positive eggs from infected flocks to an estimation of

the number of infected flocks in the U.S. The frequency of infected

eggs in an infected flock can be determined from USDA tests of eggs

produced by SE-positive flocks. The number of positive flocks is based

on USDA's nationwide survey in 1995 of SE in spent hens at slaughter

and unpasteurized liquid eggs at breaker plants. Application of the

model resulted in a distribution of prevalences ranging from 0.2 to 2.1

positive eggs per 10,000 with a mean of 0.9 positive eggs per

10,000.\18\ The problem is nationwide, although there are some regional

differences.\19\

Although a prevalence of 1 in 10,000 seems low, it is significant

in terms of exposure. That frequency amounts to about 4.5 million SE-

contaminated eggs annually in the U.S., exposing a large number of

people to SE.

Salmonellosis outbreaks commonly occur when mishandling permits the

SE organisms to multiply and inadequate cooking or mishandling during

preparation or service results in live pathogens being ingested with

the food. However, the dose required to make a person ill may vary with

the individual. The biggest factor in determining whether illness

occurs, and how severe it may be, appears to be the age and health of

the person ingesting the organisms.

4. Mitigating the Risk; Current Efforts

Mitigation of risks associated with SE in eggs requires analysis of

everything in the food production-distribution-consumption continuum

from the farm to table that might affect the likelihood that consumers

will become ill from SE in eggs.

a. Production: Preventing Introduction of SE Into Laying Flocks and

From Hens to Eggs

The Federal government has devoted significant efforts to

investigating and controlling SE in laying hens. Between 1990 and 1995,

USDA's Animal Plant Health Inspection Service (APHIS) conducted an SE

control program (9 CFR Parts 71 and 82; 56 FR 3730; January 30, 1991).

Under that program, APHIS restricted the movement of eggs from flocks

that tested positive for SE. In cooperation with FDA, CDC, and State

authorities, eggs implicated in SE outbreaks were traced back to their

farms of origin. If initial tests of manure and egg transport machinery

indicated the presence of SE, the flock became a ``test flock.'' Blood

and internal organ testing was done on the test flocks, and if any were

found positive, the flock was designated ``infected.'' The eggs from

test and infected flocks could not be sold as table eggs but could be

sent to processors for pasteurization, hard boiling, or export. A

flock's status as a ``test'' or ``infected'' flock was not lifted until

extensive testing, including additional tests of internal organs of

birds, detected no SE. Establishments had to clean and disinfect the

hen houses before installing replacement flocks.

In 1995, shortly after transfer of the program from APHIS to FSIS,

funding for the entire program was removed from the USDA's 1996

appropriations. FDA, which had worked closely with APHIS on its

tracebacks, assumed responsibility for all aspects of investigating

outbreaks, tracing back egg-associated SE illnesses to particular

producers/flocks, diverting eggs, collecting flock data to help track

the spread of SE, encouraging better quality control measures by

producers, and adoption by States of egg quality assurance programs.

State and county health departments usually perform the epidemiological

investigations of outbreaks.

The APHIS-sponsored National Poultry Improvement Plan (NPIP), a

cooperative Federal-State program, provides assistance to breeders and

hatchers on keeping birds free of egg-transmitted diseases. In 1989, an

SE control program was developed to reduce the prevalence of SE

organisms in hatching eggs and chicks. Participants in the program

follow sanitation and other control procedures at breeder farms and

hatcheries. Forty-

[[Page 27506]]

six SE-positive isolates have been found since its inception, with a

decline evident in recent years. Only two were found in 1995, and one

in 1996.\20\

A third APHIS program resulted in a variety of voluntary flock

control programs that appear to have had some effect in reducing the

numbers of infected flocks. In 1992, in the wake of APHIS tracebacks

implicating flocks in Pennsylvania, APHIS cooperated with industry

representatives, State government officials, and academic experts to

develop a program to reduce the prevalence of SE in laying hens. In the

Salmonella Enteritidis Pilot Program (SEPP), flock owners purchased

chicks from hatcheries participating in the NPIP program, imposed

strict rodent control measures, cleaned and disinfected hen houses

between flocks, controlled feed, and implemented other biosecurity

measures. The program relied on APHIS testing of environmental samples

to determine positive flocks, and egg testing by commercial

laboratories when environmental samples were positive.

In recent years, several other voluntary programs for controlling

SE in shell eggs have been developed. California's Egg Quality

Assurance Plan calls for producers and processors to apply current good

manufacturing practices and to implement risk reduction measures for

all hazards throughout the production and processing environments. The

New England Risk Reduction Program for SE in eggs is being adopted by

producers in Maine and other northeast States. United Egg Producers has

developed a ``Five Star'' program for its members, which requires

participants to ensure (1) poultry house cleaning and disinfecting, (2)

rodent and pest elimination, (3) proper egg washing, (4) biosecurity

measures, and (5) egg refrigeration during transport and storage. UEP

has recently added testing provisions for verification. The U. S.

Animal Health Association, a professional association of veterinarians,

developed ``Recommended Best Management Practices for a SE Reduction

Program for Egg Producers,'' guidelines intended for use by producers

without a State or industry program. Other States are working on egg

quality programs, and an increasing proportion of producers seem to be

adopting SE-control programs.

Much remains unknown about how SE infects flocks, and how the

organism contaminates eggs. USDA scientists believe that among birds in

an SE-infected flock, only a small number are shedding SE organisms at

any given time, and that an infected bird might easily lay many normal,

uncontaminated eggs, only occasionally laying an egg contaminated with

SE. There is speculation that the likelihood of infection or the laying

of contaminated eggs also may be related to factors other than

environmental conditions, such as the genetics of the birds, the age of

the birds, the site of infection in the hen, and whether the birds have

been stressed (e.g., because of molting).\21\ At this time, it may not

be possible to design an SE control program that will remove all

possibility of egg-laying chickens producing SE contaminated eggs. The

agencies seek comments on this issue.

b. Processing and Distribution: Preventing Growth of SE in Eggs

In addition to the presence of SE in shell eggs, many other factors

may influence the number and severity of salmonellosis cases. Key

factors are pathogenicity and virulence of the organism, the dose

level, and the numbers and susceptibility of the people exposed. In

general, the greater the dose, the greater the chance that the person

ingesting it will become ill.

The likelihood of SE multiplying depends primarily on the variables

of time and temperature, although other factors such as the site of the

egg contamination and the presence in the albumen of free iron also

appear to play a role.\22\ The site of contamination normally is the

albumen. Over time, beginning after the egg is laid, the albumen

proteins break down, ultimately rendering the albumen watery and less

viscous and reducing the mechanical as well as the chemical defenses

against bacterial motility and growth. At the same time, the yolk

membrane degrades and becomes more porous. This degradation of the

albumen and yolk membrane permits bacteria to reach the nutrient-rich

yolk and multiply. The rate at which this degradation takes place

relates to the temperature of the egg, with degradation delayed at cold

temperatures and occurring more rapidly at warm temperatures.\23\

Studies of the growth of SE adjacent to the yolk indicate that

there are three distinct phases in the growth curve of SE in eggs. The

first phase takes place in the first 24 hours after lay, when the pH of

the albumen rises from about 7 to about 9 and, it is suggested, the

bacterium have enough iron reserves of their own to support about four

generations. Studies suggest the numbers of salmonellae can increase

about 10-fold during that initial phase, before entering a lag phase

during which numbers remain fairly constant. The length of that lag

phase is largely temperature-dependent, and its end, the beginning of

the third phase, is signaled by penetration of the yolk membrane by the

bacteria and resumption of rapid growth.\24\

Failure to cool eggs clearly contributes to SE multiplication. One

study found that SE in eggs artificially inoculated in the albumen and

stored at 20 deg.C (68 deg.F) grew rapidly after they had been stored

for approximately 3 weeks, but that rapid growth occurred within 7 to

10 days when storage temperatures fluctuated between 18 deg.C (64

deg.F) and 30 deg.C(86 deg.F).\25\ A different study of eggs with SE

inoculated under the shell membrane found that after only 48 hours at

26 deg.C (78.8 deg.F) yolks contained high levels of SE.\26\ Although

there is consensus on the advisability of keeping eggs cool to prevent

SE growth, there is debate on precisely what temperature is required.

Because the studies referenced above rely on inoculated eggs, they may

not accurately represent naturally occurring strains or the numbers of

organisms that occur and grow in eggs under similar conditions. The

conclusions suggest that internal egg temperatures of 7 deg.C (approx.

45 deg.F) or lower are unlikely to promote SE growth should SE be

present in the egg.

Although the studies suggest that there is a delay of at least

several days before the egg's natural defenses start breaking down,

they also suggest that the rate at which degradation occurs is

temperature related, and that eggs should be chilled as soon as

possible.\27\ The sooner an egg is chilled, the longer its defenses

will be retained and the less likely that any SE present will have an

opportunity to replicate.

The time it takes for an egg's contents to reach a temperature of

45 deg.F is affected by many things, including the temperature of the

egg when received at the packing plant, heat added during processing,

temperature when packed, insulation effect of the packaging, how packed

eggs are stacked in coolers during storage and transportation, and the

ambient air temperature and air circulation provided at all points

after packing.

Egg processing procedures in the U.S. typically result in eggs

being warmed. Warming begins as the eggs are loaded onto the conveyance

system, and increases as they are washed; surface temperatures of eggs

immediately after washing will approach that of the wash water, which

is normally about 43-40 deg.C or 110-120 deg.F.\28\ As noted, hot

wash water temperatures are intended to provide adequate cleaning of

the shell surface and an adequate temperature differential between the

wash water and

[[Page 27507]]

the egg. USDA studies have shown that water temperatures colder than

the internal egg temperatures cause the eggs' contents to cool leading

to a pressure gradient that pulls in water and any bacteria in the

water through the shell.\29\

After the eggs emerge from the wash and are dried with forced

ambient air, internal temperature at the time they are packed is often

in the 70-80 deg.F range. After packing, most processors hold eggs in

coolers at an ambient air temperature of 45-55 deg.F, and transport

eggs at an ambient air temperature of 60 deg.F or less. However, the

ambient air temperature does not correlate to egg temperature. The

temperature of the eggs' contents at the time they are transported from

the packer will range between 50 deg.F and 80 deg.F, depending on the

starting temperature, the packaging, how the crates are packed and

stacked, and the length of time they are in the cooler before shipping.

The rate at which eggs chill after leaving the processor is

similarly dependent on the initial temperature, packaging, loading

configurations, and the capability of the refrigeration equipment.

Transporters contend that their refrigeration units are designed to

maintain--not reduce--temperatures, and that they cannot be relied upon

to reduce the temperatures of products being transported. Further, the

driver of a truck making multiple deliveries must open the truck door

frequently, and if the outside temperature is warm, it would be

virtually impossible to maintain the ambient air temperature uniformly

throughout the load. Similarly, most retail stores' display cases have

been designed to keep products cool, not to cool down products. Eggs

received by retail stores are frequently at temperatures well above 45

deg.F.

Ideally, reliance on the use of ambient air temperature of 45

deg.F during distribution and retail as a reasonable measure of whether

the eggs are being maintained under appropriate conditions would

necessitate the eggs being chilled to an internal temperature of 45

deg.F before they are shipped. Significantly, there are a number of

actions processors may take to reduce the temperature at which eggs are

packed, and to cool them before shipment, including lowering the wash

temperatures and pre-pack chilling of eggs. Recent research has shown

that new technologies are available to processors to rapidly cool shell

eggs. One study found that carbon dioxide, as a cryogenic gas, can be

used instead of air chilling to rapidly chill eggs and results in no

increase in cracked shells.

c. Rewashing/Repackaging: Preventing Growth of SE in Eggs

It appears that eggs are occasionally removed from retail

establishments when they are within a few days of the expiration or

sell-by date stamped on the carton and returned to the processing

plant. These eggs are co-mingled with eggs that are being cleaned for

the first time, go through the hot water/sanitizing process again, and

are graded. The rewashed eggs are then packed into cartons and are

redistributed for sale. These eggs receive a new expiration or sell-by

date.

On April 17, 1998, USDA announced that as of April 27, 1998,

repackaging of eggs packed under its voluntary grading program will be

prohibited while the Department reviews its policies on egg repackaging

and engages in any necessary rulemaking. The prohibition on repackaging

affects eggs packed in cartons that bear the USDA grade shield. About

one-third of all shell eggs sold to consumers are graded by USDA.

In the wake of the USDA action, FDA is considering appropriate

measures to take to address this issue. FDA requests comments on how

widespread this practice is and on whether any aspect of rewashing/

repackaging of eggs significantly increases the risk that consumers

will contract SE-related illness from these eggs. FDA notes, for

example, that repackaged eggs are subjected to warming during

rewashing. Inasmuch as an egg's natural barriers to the multiplication

of SE may be compromised at temperatures above 45 deg.F (see

discussion in section 4b), does the warming of shell eggs during rewash

significantly increase the risk that SE (if present) will multiply in

rewashed/repackaged eggs during distribution or while held for sale,

service, or preparation? Does it significantly increase the risk of

illness for the consumer if the egg is not thoroughly cooked before

consumption?

Are there important aspects, for example, safety risks or

otherwise, of rewashed/repackaged eggs that would raise the question

whether rewashed/repackaged eggs should be labeled in the same manner

as other shell eggs? Are rewashed/repackaged eggs different enough from

other shell eggs such that label statements in addition to

``expiration'' or ``sell-by'' dates would be necessary to adequately

describe the product? If, for some segments of the U.S. population, the

standard egg labeling practices are not appropriate for rewashed/

repackaged eggs, how should these eggs be labeled to enable consumers

to understand the nature of this product and to communicate other

important information to the purchaser?

The issue of rewashing and repackaging of eggs also calls attention

to current practices regarding the expiration dating of eggs in

establishments that function primarily under State regulatory

oversight. While a few States have regulations governing expiration

dating of eggs, most do not and egg packers determine what expiration

dating practices they will employ. Processors that do not use USDA's

grading service, and that are not covered by State requirements,

typically choose to place a 30- or 45-day expiration date on egg

cartons. Some processors do not provide any expiration date. Section

403(a) of the Federal Food, Drug, and Cosmetic Act (FFDCA) states that

a food is misbranded if its labeling is false or misleading in any

particular. FDA requests comments on the latter two practices described

above could violate 403(a) or other provisions of the Act. It also

seeks comments on whether the variety of expiration dating practices

for eggs could be misleading to consumers given their expectations when

they purchase eggs. FDA will evaluate comments received regarding

expiration dating and will consider providing guidance to the States on

appropriate controls. FDA also requests comments on whether any such

guidance should address appropriate practices for use of eggs that are

not sold by the expiration date.

d. Preparation and Consumption: Preventing Ingestion of SE from Eggs

Another risk factor is exposure--the number of people who ingest SE

organisms from SE-contaminated eggs. Pathogens like SE usually become a

public health problem as a consequence of changes in the agent itself,

the host, or the environment. Examples of such changes include the

types of food people eat, the sources of those foods, and the possible

decline in public awareness of safe food preparation. Antibiotic-

resistant strains of pathogens are emerging, and people are exposed to

new pathogens originating in other regions and other parts of the

world. People today have increased life expectancies, and there are

increasing numbers of immuno-compromised persons, increasing the

population susceptible to severe illness after infection with foodborne

pathogens.\30\

Finally, preparation and consumption patterns can greatly influence

the likelihood of foodborne illness from eggs. However, SE outbreaks of

foodborne illness from eggs continue to be associated with the use of

recipes

[[Page 27508]]

calling for uncooked eggs or with undercooking of eggs. Low numbers of

SE organisms in prepared foods can increase if the foods are held at

room temperature or are cross contaminated with other foods. The risk

is further amplified in commercial or institutional food service

settings where larger quantities of food are served to larger groups of

persons over extended periods of time.

As the proportion of food that is eaten outside homes in the U.S.

increases, outbreaks associated with these foods increase in

importance. They accounted for more than 90 percent of reported

foodborne disease outbreaks in the 1990s.

5. Current Regulation of Shell Eggs

Federal authority to regulate eggs for safety is shared by FDA and

USDA. FDA has jurisdiction over the safety of foods generally,

including shell eggs, under the FFDCA (21 U.S.C. 301, et seq.). FDA

also has authority to prevent the spread of communicable diseases under

the Public Health Service Act (PHSA)(42 U.S.C. 201, et seq.). This

authority would include the authority to regulate foods when the foods

may act as a vector of disease, as is the case with eggs and SE. USDA

has primary responsibility for implementing the Egg Products Inspection

Act (EPIA)(21 U.S.C. 1031, et seq.), although FDA shares authority

under the statute (see, for example, 21 U.S.C. 1034). USDA's Food

Safety and Inspection Service and Agricultural Marketing Service share

responsibilities under the EPIA. FSIS has primary responsibility for

the inspection of processed egg products to prevent the distribution

into commerce of adulterated or misbranded egg products (7 CFR 2.53),

while AMS conducts a surveillance program to ensure proper disposition

of restricted shell eggs.

Under Federal regulations, all major commercial egg producers--the

757 producers who have more than 3,000 laying hens and collectively are

responsible for close to 94 percent of the nation's eggs--are required

to register with AMS. They are subject to periodic on-site visits by

AMS to ensure that eggs packed for commercial sale have no more than

the percentage of restricted eggs allowed for the grade of eggs being

packed, that they are properly labeled, and that proper disposition is

made of inedible and restricted eggs. Exempted from this oversight are

approximately 80,000 small egg producers.

States may have their own laws governing eggs, as long as they are

consistent with Federal laws (e.g., 21 U.S.C. 1052(b)(2)). Generally,

State laws and regulations specifically govern egg grading and labeling

in each of the States. These laws influence how eggs are packed and

shipped for sale and then handled by retail stores, restaurants, and

other food service establishments in those jurisdictions.

FDA and FSIS work with the States to encourage uniformity among the

State laws affecting food safety in retail and food service

establishments. The principal mechanism for this is the Food Code, a

model code published by FDA intended for adoption by State and local

authorities for governing retail food and food service establishments.

The provisions of the Food Code are modified periodically with input

from a broad spectrum of organizations--industry, academia, consumers

and government agencies at the Federal, State, and local levels. In

addition, training programs on the Food Code recommendations have been

conducted yearly with State agencies.

The Food Code states that ``potentially hazardous foods,''

including shell eggs, should be received and maintained at a

temperature of 41 deg.F or less, or, if permitted by other law to be

received at more than 41 deg.F, be reduced to that temperature within

4 hours. Because eggs are often received at temperatures well above 41

deg.F, the 1997 edition of the Food Code contains an exception for

shell eggs, requiring only that they be placed upon receipt in

refrigerated equipment that is capable of maintaining food at 41

deg.F.

The Food Code specifies that shell eggs, when prepared for service,

are to be cooked to specified temperatures for a specified time. If the

egg is not served immediately, hot and cold hold temperatures are

specified. The Food Code further specifies that pasteurized eggs be

substituted in delicatessen and menu items that typically contain raw

eggs unless the consumer is informed of the increased risk. Pasteurized

egg substitution is specified for eggs that are held before service of

vulnerable individuals.

In recent years, many States have enacted laws requiring specified

ambient air temperatures for shell egg storage and handling. While many

States specify 45 deg.F or less for that purpose, others retain the 60

deg.F temperature requirement traditionally required under the USDA

grading standards, and some have no requirement. A number of States

have stated that they are waiting for USDA implementation of the EPIA

shell egg refrigeration requirements before instituting any State law

governing shell egg refrigeration.

The egg industry clearly has an interest in finding a way to

constructively address the public concern about SE in eggs, and many in

the industry have communicated their desire to work with the government

toward an effective regulatory solution.

In November 1996, Rose Acre Farms, Inc., submitted a detailed

petition (Docket No. 96P-0418) to the Federal agencies that have played

a role in the regulation of shell eggs--FDA, FSIS, APHIS, and AMS--

requesting that in regulating the presence of pathogens in shell eggs,

the agencies ``adopt a comprehensive, coordinated regulatory program to

replace the patchwork of approaches they currently take.'' The

petitioner acknowledged the need to reduce the prevalence of SE in

shell eggs, but advocated a broad-based regulatory program that goes

beyond the traceback-and-sanction approach that, the petitioner

contended, is both inadequate to protect consumers and unfairly burdens

producers. The petitioner called for a collaborative process in

developing incentives to encourage improved handling of eggs throughout

the farm-to-table cycle and other modifications to promote greater

levels of food safety.

In May of 1997, the Center for Science in the Public Interest

submitted a petition (Docket No. 97P-0197) requesting that FDA issue

regulations requiring that shell egg cartons bear a label cautioning

consumers that eggs may contain harmful bacteria and that they should

not eat raw or undercooked eggs. The petitioner further requested that

all egg producers be required to implement on-farm HACCP programs to

minimize the risk that their eggs will be contaminated with SE.

FDA and FSIS are responding to these petitions by initiating such a

comprehensive, coordinated process with this ANPR.

Finally, USDA and FDA intend to encourage and assist in additional

research on how hens become infected with SE, the factors that relate

to infected hens' production of SE-contaminated eggs, better ways to

identify specific strains of SE, the virulence and other

characteristics of emerging SE strains, the extent of the potential

public health risk from SE, and identification of effective controls

and intervention strategies.

Because of the number of outbreaks of foodborne illness caused by

Salmonella Enteritidis that are associated with the consumption of

shell eggs, FDA and FSIS have tentatively determined that there are

actions that can be taken even at this time to reduce the risk of

foodborne illness from shell eggs while

[[Page 27509]]

additional measures are being considered pursuant to this ANPR. FSIS

intends to act to amend its regulations to require that shell eggs

packed for consumer use be stored and transported under refrigeration

at an ambient temperature not to exceed 45 deg.F, and that these

packed shell eggs be labeled to indicate that refrigeration is

required. FDA intends to act to publish shortly a proposal to (1)

require that retail food stores and food service establishments hold

shell eggs under refrigeration and (2) require safe handling statements

on the labeling of shell eggs that have not been treated to destroy

Salmonella microorganisms that may be present.

6. Need for Additional Information and Analysis.

In 1991, the EPIA was amended in the wake of publicity about

foodborne disease outbreaks attributed to Salmonella in shell eggs. The

amendment requires, essentially, that shell eggs packed for consumers

be stored and transported under refrigeration at an ambient air

temperature not to exceed 45 deg.F. (21 U.S.C. Secs. 1034, 1037).

Congress also provided that these provisions would be effective only

after promulgation of implementing regulations by USDA.

After reviewing the issue in 1996, FSIS concluded and informed

Congress that a regulation establishing an ambient air temperature at

which eggs must be held and transported would not address the

underlying food safety problems, and that the problem could be dealt

with effectively only in the context of a broader process examining a

variety of issues in addition to ambient air temperatures. As part of

the 1998 Appropriations for Agriculture, Rural Development, Food and

Drug Administration, and Related Agencies (P.L. 105-86), however,

Congress provided that $5 million of FSIS' annual appropriation will be

available for obligation only after the Agency promulgates a final rule

to implement the refrigeration and labeling requirements included in

the 1991 EPIA amendments.

FSIS and FDA are now looking at how best to address the food safety

concerns associated with shell eggs in the context of their mutual,

HACCP-based, farm-to-table food safety strategy. FSIS and FDA believe

that comprehensive shell egg regulations must address the public health

risks identified; that such regulations must be fully considered in an

open, public process; and that each regulation adopted must have been

considered in light of available alternatives and be consistent with

other laws and regulations.

FSIS and FDA, in furtherance of their commitment to develop a

comprehensive strategy for shell eggs, have undertaken the following

actions:

(1) Time-temperature Conference. A 3-day technical conference on

November 18-20, 1996, provided a forum for information on temperature

control interventions and verification techniques in the transportation

and storage of meat, poultry, seafood, and eggs and egg products. The

egg session included many informative technical presentations and

policy discussions on the issue of implementing the EPIA's 45 deg.F

ambient temperature requirement. The opportunity to submit written

comments to supplement the record was provided.

(2) Transportation ANPR. In a related activity, FSIS and FDA

published a joint ANPR (61 FR 58780) soliciting information on issues

related to ensuring the safety of potentially hazardous foods during

transportation. The agencies posed a range of regulatory and non-

regulatory options, and solicited information to help them assess the

risks and decide what approaches are best suited to addressing those

risks. The comment period on this ANPR closed on February 20, 1997.

Fifty-two comments have been received.

(3) Risk Assessment. The agencies are conducting a quantitative

risk assessment for shell eggs. The project is being conducted by a

multidisciplinary team of scientists from USDA, FDA, and academia.

Begun in December, 1996, it is intended to (a) provide a more

definitive understanding of the risks of egg-associated foodborne

disease; (b) assist in evaluating risks and ways in which the risks

might be reduced; and (c) verify data needs and prioritize data

collection efforts. A draft report on risks of SE in eggs and egg

products is on the FSIS Homepage and was presented at a technical

meeting in September 1997. The draft report of the risk assessment team

will be available for public comment and subject to modification based

on that input before being made final. Interested persons are

encouraged to provide any data or information relevant to the risk

assessment for use in the analysis.

(4) Research. The Agencies are undertaking efforts to initiate:

--a nationwide surveillance program for SE and SE phage-type 4 to

track the spread among layer flocks.

--research (in conjunction with USDA's Agricultural Research

Service) on the molecular and virulence comparison of U.S. SE phage-

type 4 with isolates from other parts of the world (human and poultry).

(5) Dialogue. FDA and FSIS intend to engage affected industry,

Federal and State regulatory agencies, and business organizations in an

open, on-going dialogue regarding steps they might take voluntarily to

address the SE problem and ways in which the Federal agencies might

help such efforts.

(6) Forthcoming FDA/FSIS Actions. As stated above, because there

are actions that can be taken at this time to reduce the risk of

foodborne illness from shell eggs, FDA intends to publish shortly a

proposal to (1) require that retail food stores and food service

establishments hold shell eggs under refrigeration and (2) require safe

handling statements on the labeling of shell eggs that have not been

treated to destroy Salmonella microorganisms that might be present. In

that proposal, FDA will solicit comments and information concerning

these two matters. FDA requests that comments or information submitted

in response to this ANPR also be submitted in response to FDA's

proposed rule if such comments or information are relevant to the

issues raised therein. In addition, as stated above, FSIS intends to

act to amend its regulations to require that shell eggs packed for

consumer use be stored and transported at an ambient temperature that

does not exceed 45 deg.F.

Information Requested

FDA and FSIS have available a wide range of mechanisms for

administering the laws for which they are responsible. The agencies are

interested in the public's views on what regulations may be required to

reduce the public health risk of SE in shell eggs, including any

performance standards that might be developed.

One approach might be a process-oriented rule similar to the

agencies' HACCP regulations for meat, poultry, and seafood. Regulations

may be proposed to mandate HACCP-like process controls to reduce the

microbiological and other food safety hazards in shell egg production,

processing and handling. Such an approach requires each business to

develop controls that are best suited to its particular processes and

products. The agencies are interested in comments on whether HACCP-like

controls could be effective against SE in eggs, in how many producers

are presently using HACCP-like controls, and in the overall costs of

these controls. The agencies are interested in how such a program would

affect small entities.

The agencies may achieve public health objectives by providing

guidance to interested parties as a companion to or in lieu of

regulations. The agencies

[[Page 27510]]

provide a variety of technical information and guidance materials to

industries that must comply with Federal laws, to State and local

officials, and to consumers. These materials range from general advice

to fairly detailed examples or ``models'' of ways in which a plant may

ensure compliance with a particular statutory or regulatory provision.

Such guidance may be particularly useful for smaller plants with

limited resources.

A third general approach would be a Federal-State cooperative

program under which overall regulatory oversight is left primarily to

State agencies using mutually agreed-upon standards and procedures and

Federal assistance. The agencies frequently work cooperatively with

State and local government authorities. FDA currently participates in a

formal Federal-State cooperative program for the interstate shipment of

two commodities, Grade A milk and shellfish.

The agencies believe that a comprehensive, effective program for

the control of SE in shell eggs is likely to require some combination

of these three general approaches. The following sets out questions the

answers to which, the agencies believe, will help them to shape a

program that will be useful in reducing risk at each stage in the shell

egg farm-to-table continuum.

Production

Should the patchwork of voluntary quality assurance (QA) programs

be made consistent with a single, national standard for flock-based

quality assurance programs, and be applicable to all producers? Does

there need to be more uniformity among the QA programs to assure

consumers that producers in all States are uniformly doing all they can

to reduce the frequency of SE-contaminated eggs, and to provide ``a

level playing field'' among competing producers in the various States?

Should the agencies establish minimum QA requirements for all

commercial shell egg producers? This might be accomplished through

rulemaking or some form of cooperative program with the States. Should

the microbiological testing under such a program be done by a third

party (someone other than the producer) to ensure test uniformity and

the integrity of the program? Should the agencies require the

submission of testing data so that they can identify ways to improve

the program, including possible justification for regional variations,

verify the overall effectiveness of the program, track the prevalence

of emerging strains of SE and, as necessary, identify the need for

additional testing programs or other interventions required to protect

human or animal health? Should a QA program be voluntary?

Processing

In-shell pasteurization of shell eggs is a relatively new

technological development by which harmful bacteria are destroyed

without significantly altering the nature of the egg. Were this

technology viable for broad scale adoption by producers, it could

conceivably significantly reduce the risk of foodborne illness through

the destruction of any SE in the egg at the time of processing. The

agencies seek comments and information that would address the current

viability of in-shell pasteurization for eggs. What factors will

determine whether and when in-shell pasteurization of eggs could be

applied to the whole industry? Comments should address technological

and cost factors.

FSIS and FDA believe that there are many interventions that might

be applied during processing that would reduce the risk to consumers

from SE in shell eggs. The agencies could continue to defer to States,

or processors could be required to use only shell eggs from production

facilities adhering to a QA program meeting national standards. This

would enable each processor to identify and control all hazards,

including SE, that might be introduced into the product during

processing. The systems would address those factors known to influence

SE growth in shell eggs during processing (principally the age and

temperature of the eggs), precluding the necessity of developing

detailed prescriptive regulations attempting to specify how such

control should be achieved. The agencies would like comments on how

such processing requirements might best be structured.

Another alternative might be a sliding scale approach similar to

that under consideration by the European Union. Under this approach, a

specific egg temperature is not required, but a ``sell by'' date is

mandatory, which would vary depending on the temperatures at which eggs

are maintained. Assuming packed eggs are transported and stored at an

ambient air temperature of 45 deg.F, the primary determinant of the

temperature of eggs in commercial channels will be the temperature of

the eggs when they are shipped from the packer. To provide an incentive

for processors to chill eggs before shipping, yet retain flexibility to

accommodate reasonable alternatives to an absolute temperature

requirement, a regulation might prescribe a range of ``sell-by'' dates

based on the egg temperature achieved by the packer. However, such an

approach might be difficult to verify and enforce. The agencies would

like comments on the feasibility and advisability of this kind of

approach.

Retail

FDA intends shortly to propose regulations to require that food

retail and food service establishment hold eggs under refrigeration. As

explained elsewhere in this document, FDA believes that these actions

are measures that can be taken at this time to reduce the risk of

foodborne illness from shell eggs. Pursuant to this ANPR, both agencies

will consider other matters that affect eggs at retail as part of the

comprehensive farm-to-table solution that the agencies ultimately put

in place.

The agencies are interested in whether retail stores should require

their suppliers to use temperature recording devices, or affix

temperature indicating devices on the egg cases or cartons, to help

ensure that the eggs have not been subject to temperature abuse during

transportation. Could any requirement for delivery at 45 deg.F be

enforced effectively as a matter of contract between the processors

(vendors) and the retail stores (purchasers)? Should the agencies

consider regulations to effect these changes?

Restaurants and Food Service Operations

Restaurants, food service operators, and many retail stores that

prepare food for immediate consumption are regulated primarily by State

and local governments. Should the agencies take a more direct role, or

should they continue to rely on the Food Code to provide guidance on

the maintenance and preparation of eggs and encourage State and local

authorities to adopt and enforce those standards?

The agencies believe that much of what must be done to reduce the

risk of foodborne disease transmission in restaurants and other food

service facilities involves education and training. Food service

managers play an increasingly important role in food safety, and they

must place a high priority on employee hygiene and proper food handling

techniques. Thus, the Federal agencies are currently exploring with

industry representatives (the major associations representing retail

stores and restaurants as well as major food producer groups),

representatives of State and local regulatory agencies, and consumer

groups the possibility of a partnership

[[Page 27511]]

that would build on current programs to develop a comprehensive,

national food safety education and training campaign directed at people

who work in restaurants and other food service facilities, people who

work in retail stores, and at consumers. This campaign would include

lesson plans and materials for classroom training that could be used in

public school curricula as well as in food service settings.

Household Consumers

A primary tool for reducing the risk of foodborne disease among

consumers is education. To ensure that consumers are fully and

adequately informed of the significant risks associated with SE in eggs

and how to best avoid these risks, FDA shortly will be proposing

certain labeling requirements for eggs. The agencies also plan to

intensify their consumer education efforts in the coming months and to

institute permanent food safety education programs that will help

consumers protect themselves from all food safety hazards.

Thus, by this notice, FDA and FSIS are requesting comments and

information on a variety of issues concerning ways to reduce the risk

to the public health from SE in shell eggs. These issues need to be

addressed comprehensively by the agencies. FSIS and FDA welcome

discussion and comments on the issues in this notice and other issues

related to the subject. The agencies are particularly interested in

comments about alternatives that would minimize the impact on small

entities.

Done in Washington, DC, on May 11, 1998.

Thomas J. Billy,

Administrator, FSIS.

William B. Schultz,

Deputy Commissioner for Policy, FDA.

References

1. D'Aoust, J. 1997, Salmonella Species. pp. 129-158. In, Doyle, M.,

Beuchat, L. and Montville, L. (eds.), Food Microbiology Fundamentals

and Frontiers, ASM Press, Washington, D.C.; Jay, J. 1996. Chapter

23. Foodborne Gastroenteritis caused by Salmonella and Shigella. pp.

507-526, In Modern Food Microbiology, Fifth ed., Chapman & Hall, New

York.

2. Berenson, A. (ed). 1995. Typhoid Fever, pp. 502-507. In, Control

of Communicable Diseases Manual, Sixteenth ed., American Public

Health Assn., Washington, D.C.

3. id. n. 1.

4. id.

5. CDC. Laboratory Confirmed Salmonella, Surveillance Annual

Summary, 1993-1995 and 1996.

6. Swerdlow, D. et al. Reactive arthropathy following a multistate

outbreak of Salmonella typhimurium infections. Abstract 916. 30th

Interscience Conference on Antimicrobial Agents and Chemotherapy.

7. CDC. Memo to the Record dtd 2/8/96 from Chief, Foodborne Diseases

Epidemiology Section, NCID.

8. Chalker, R. And Blaser, M. 1988. A Review of Human Salmonellosis:

III. Magnitude of Salmonella Infections in the United States. Rev

Inf Dis. 10:111-123

9. id. n. 8.

10. CDC. 1996. Outbreaks of Salmonella Serotype Enteriditis

Infection Associated with Consumption of Raw Shell Eggs--United

States, 1994-1995. MMWR 45:737-742.

11. Letter dtd April 16, 1997, from J. Stratton, Calif. Dept. of

Health Services to T. Billy, FSIS.

12. Altekruse S., et al, 1993. A Comparison of Salmonella

Enteritidis Phage Types from Egg-associated Outbreaks and Implicated

Flocks. Epidemiol. Infect. 110-17-22.

13. Hennessy T., et al. A National Outbreak of Salmonella

Enteriditis Infections from Ice Cream. N E J Med. 1996. 334:1281-

1286.

14. Khan M. And Nguyen A. 1995. A Salmonella-Specific DNA Probe and

Its Use in Southern Hybridration for Differentiation of Salmonella

Enteriditis. Avian Diseases. 39:368-374.

15. Buchanan, R., et al. 1997. Egg and Egg Products. In,

Microorganisms in Foods; No. 6, Microbiology of Commodities.

International Commission on Microbiological Specifications for Foods

(eds.); Chapman Hall, London, UK. (In press)

16. id n. 11; Tauxe, R. 1966. An Update on Salmonella. Health and

Environment Digest. 10:1-4; Mishu B., et al. 1994. Outbreaks of

Salmonella Enteriditis Infections in the United States, 1985-1991. J

Infect Dis 169: 547-552.

17. St. Louis, M. et al. 1988. The Emergence of Grade A Eggs as a

Major Source of Salmonella Enteriditis Infections, New Implications

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24. Humphrey, T. and Whitehead, A. 1993. Egg age and the growth of

Salmonella Enteritidis PT4 in egg contents. Epidemiol. Inf. 111:209-

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40.

25. id, (Humphrey, T.).

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Enteritidis in Grade A Eggs During Prolonged Storage. Poultry Sec.

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27. Kim, C., et al. 1989. Effect of Time and Temperature Growth of

Salmonella Enteritidis in Experimentally Inoculated Eggs. Avian

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Influence of Storage Temperature. Vet. Rec. 1236:292

29. Anderson, K.E., 1993. Refrigeration and Removal of Heat from

Eggs. Misset-World Poultry 9:11

30. Saeed, A.M., and Koons, C.W. 1993. Growth and Heat Resistance of

Salmonella Enteritidis in Refrigerated and Abused Eggs. Jrnl. Food

Prot. 57:592-595.

31. M. Taylor to J. Skeen, MC, dtd Sept. 5, 1996.

[FR Doc. 98-13056 Filed 5-14-98; 10:28 am]

BILLING CODE 3410-DM-P