Prevention of Salmonella Enteritidis in Shell Eggs During Production, Storage, and Transportation

DEPARTMENT OF HEALTH AND HUMAN SERVICES

Food and Drug Administration

21 CFR Parts 16 and 118

[Docket No. FDA-2000-N-0190] (Formerly Docket No. 2000N-0504)

RIN 0910-AC14

Prevention of Salmonella Enteritidis in Shell Eggs During Production, Storage, and Transportation

AGENCY:

Food and Drug Administration, HHS.

ACTION:

Final rule.

SUMMARY:

The Food and Drug Administration (FDA) is issuing a final rule that requires shell egg producers to implement measures to prevent

Salmonella

Enteritidis (SE) from contaminating eggs on the farm and from further growth during storage and transportation, and requires these producers to maintain records concerning their compliance with the rule and to register with FDA. FDA is taking this action because SE is among the leading bacterial causes of foodborne illness in the United States, and shell eggs are a primary source of human SE infections. The final rule will reduce SE-associated illnesses and deaths by reducing the risk that shell eggs are contaminated with SE.

DATES:

This final rule is effective September 8, 2009. The Director of the Office of the Federal Register approves the incorporation by reference in accordance with 5 U.S.C. 552(a) and 1 CFR part 51 of certain publications in new 21 CFR 118.8 as of September 8, 2009.

Please see

section II.C of this document for the compliance dates of this final rule. Submit comments on information collection issues under the Paperwork Reduction Act of 1995 by August 10, 2009 (

see

the “Paperwork Reduction Act of 1995” section of this document).

FOR FURTHER INFORMATION CONTACT:

John Sheehan, Center for Food Safety and Applied Nutrition (HFS-315), Food and Drug Administration, 5100 Paint Branch Pkwy., College Park, MD 20740, 301-436-1488.

SUPPLEMENTARY INFORMATION:

Table of Contents

I. Background

A. FDA's Proposed Rule

B. What Are

Salmonella

and SE Infection?

C. What Is the Connection Between

Salmonella

and Shell Eggs?

D. The U.S. Egg Industry

E. Current On-Farm Practices

F. Voluntary EQAPs

G. The Food Code

H. Rationale for the Final Rule

II. Highlights of the Final Rule and Summary of Significant Differences Between the Proposed and Final Rules

A. Highlights of the Final Rule

B. Significant Differences Between the Proposed and Final Rules

C. Compliance Dates

III. Comments on the Proposed Rule

A. General Comments

B. Comments on “Persons Covered by the Requirements in This Part” (Proposed and Final § 118.1)

C. Comments on “Definitions” (Proposed and Final § 118.3)

D. Comments on “

Salmonella

Enteritidis (SE) Prevention Measures” (Proposed and Final § 118.4)

E. Comments on “Environmental Testing for

Salmonella

Enteritidis (SE)” (Proposed and Final § 118.5)

F. Comments on “Egg Testing for

Salmonella

Enteritidis (SE)” (Proposed and Final § 118.6)

G. Comments on “Sampling Methodology for

Salmonella

Enteritidis (SE)” (Proposed and Final § 118.7)

H. Comments on “Testing Methodology for

Salmonella

Enteritidis (SE)” (Proposed and Final § 118.8)

I. Comments on “Administration of the

Salmonella

Enteritidis (SE) Prevention Plan” (Proposed and Final § 118.9)

J. Comments on “Recordkeeping Requirements for the

Salmonella

Enteritidis (SE) Prevention Plan” (Proposed and Final § 118.10)

K. Comments on “Registration Requirements for Shell Egg Producers Covered by the Requirements of This Part” (Final § 118.11)

L. Comments on “Enforcement and Compliance” (Proposed and Final § 118.12)

M. Comments on Request for Comments as to Whether FDA Should Mandate Special Requirements for Certain Food Establishments That Serve Highly Susceptible Populations

IV. Legal Authority

V. Analysis of Economic Impacts—Final Regulatory Impact Analysis

A. Introduction

B. Need for Regulation

C. Comments on the Preliminary Regulatory Impact Analysis in the Proposed Rule and Responses

D. Economic Analysis of Potential Mitigations: Overview

E. Summary of Costs and Benefits of Regulatory Options and the Rule

F. Benefits and Costs of Potential SE Prevention Measures: Detailed Analysis

G. Summary of Benefits and Costs of the Final Rule

VI. Final Regulatory Flexibility Analysis

A. Introduction

B. Economic Effects on Small Entities

C. Regulatory Options

D. Description of Recordkeeping and Recording Requirements

E. Summary

VII. Unfunded Mandates

VIII. Small Business Regulatory Enforcement Fairness Act

IX. Paperwork Reduction Act of 1995

X. Analysis of Environmental Impact

XI. Federalism

XII. References

I. Background

A. FDA's Proposed Rule

On September 22, 2004, FDA proposed a rule to prevent SE contamination in shell eggs during production (the proposed rule) (69 FR 56824). The proposed rule set out several measures to be taken by egg producers to prevent the contamination of shell eggs with SE during egg production, such as implementation of biosecurity and pest control programs, environmental and egg testing requirements, and requirements concerning refrigerated storage of eggs at the farm and diversion from the table egg market of eggs from flocks in which SE has been detected (69 FR 56824).

In addition, in the proposed rule we solicited comments on whether we should include additional requirements in the final rule, particularly in two areas. First, we asked whether we should expand the proposed recordkeeping requirements to include a written SE prevention plan and records documenting compliance with the SE prevention measures (69 FR 56824 at 56825 and 56841 through 56842). Second, we asked whether the safe egg handling and preparation practices in FDA's Food Code (

see http://www.cfsan.fda.gov/~dms/fc05-toc.html

(accessed December 14, 2006)) should be federally mandated for establishments that specifically serve a highly susceptible population (such as nursing homes, hospitals, and daycare centers) (69 FR 56824 at 56825 and 56849 through 56852).

The proposed rule had a 90-day comment period, which ended on December 21, 2004. To discuss the proposed rule and solicit comments from interested stakeholders, FDA held three public meetings in 2004. Based on comments received in response to the proposed rule, FDA reopened the comment period on May 10, 2005, for the limited purpose of receiving comments and other information regarding industry practices and programs that prevent SE-monitored chicks from becoming infected by SE during the period of pullet rearing until placement into laying hen houses (70 FR 24490). The term “pullet” refers to a chicken less than 20 weeks of age. On May 24, 2005, FDA received a request for an extension of the reopened comment period from two of the major trade associations representing egg producers and others affected by this

rule. We agreed to extend the reopened comment period until July 25, 2005.

B. What Are Salmonella and SE Infection?

As we described in greater detail in the proposed rule (69 FR 56824 at 56825 through 56827),

Salmonella

microorganisms are ubiquitous and are commonly found in the digestive tracts of animals, especially birds and reptiles. Human illnesses are usually associated with ingesting food or drink contaminated with

Salmonella,

although infection also may be transmitted person-to-person through the fecal-oral route where personal hygiene is poor or by the animal-to-man route (Ref. 1-2).

All people are at risk for salmonellosis, although the severity of the infection is influenced by a person's age and immune status.

Salmonella

infections are characterized by diarrhea, fever, abdominal cramps, headache, nausea, and vomiting. Symptoms usually begin within 6 to 72 hours after consuming a contaminated food or liquid and last for 4 to 7 days. Most healthy people recover without antibiotic treatment; however, the diarrhea can be severe, and the person may be ill enough to require hospitalization. In some patients, the infection can spread into the bloodstream, then to other areas of the body, such as the bone marrow or the meningeal linings of the brain. This infection can lead to a severe and fatal illness (Ref. 2). These complications associated with an infection are more likely to occur in children, the elderly, and persons with a weakened immune system.

In addition, about 2 percent of those who recover from salmonellosis may later develop recurring joint pain and reactive arthritis (Ref. 3, 4).

Salmonellosis is a serious health concern. It is a notifiable disease, i.e., physicians and health laboratories are required to report cases (single occurrences of illness) to local health departments in accordance with procedures established by each State. These cases are then reported to State health departments, and the

Salmonella

isolates are referred to State Public Health laboratories for serotyping (a method of distinguishing related organisms by their antigens). Each case and each serotyped isolate is reported to the U.S. Centers for Disease Control and Prevention (CDC). These reports are made only for diagnosed cases of

Salmonella

infection.

A case of illness is confirmed as salmonellosis only if an isolate is confirmed by a laboratory as being

Salmonella.

Although all cases may not be confirmed, all confirmed cases are associated with isolates of

Salmonella.

Reported cases are likely to represent only a small portion of the actual number of illnesses that occur because of the following reasons: (1) Ill individuals do not always seek care by medical professionals, especially if the symptoms are not severe; (2) medical professionals may not establish the cause of the illness but may simply treat the symptoms; and (3) medical professionals do not always report

Salmonella

cases to public health officials. CDC estimates that there are 38 cases of salmonellosis for every reported culture-confirmed case (Ref. 5). The overall burden of salmonellosis in 2001 was estimated to be 1,203,650 cases, including 14,000 hospitalizations, and 494 deaths (Refs. 6 and 7). Updated

Salmonella

surveillance data for 2004 indicate that the burden of salmonellosis in 2004 was somewhat higher, estimated to be 1,376,514 cases, including 14,264 hospitalizations, and 427 deaths (Refs. 5 and 8).

CDC surveillance data list close to 600 different

Salmonella

serotypes that have caused illness in the United States. Since 1995,

Salmonella enterica

serotype Enteritidis (SE) has been the second most frequently reported cause of

Salmonella

infection (Ref. 9). CDC reported that in 2008 SE was the leading reported cause of

Salmonella

infections, accounting for 20.1% of all of the

Salmonella

isolates that were serotyped (Ref. 10). The rate of SE isolates reported to CDC increased from 0.6 per 100,000 population in 1976 to 3.6 per 100,000 population in 1996 (Ref. 11-12). In 2001 the isolation rate for SE was 2.0 per 100,000 population, and the annual contribution of SE (corrected for underreporting) to salmonellosis was estimated to be 193,463 illnesses, including 2,004 hospitalizations and 60 deaths (Refs. 5 and 8). Estimated incidence of

Salmonella

infection in 2008 did not change significantly compared with estimates for the preceding 3 years, and in particular the apparent increase in

Salmonella

infections was not significant. However, the incidence of SE did increase by 19% (CI = 3%-39%) (Ref. 10). These data confirm the continued significance of SE as a cause of human infection in the United States.

In 1985, States reported to CDC 26 SE-related outbreaks (i.e., occurrences of 2 or more cases of a disease related to a common source); by 1990 the number of SE-related outbreaks reported to CDC had increased to 85. The number of outbreaks began declining in the 1990s; in 1995 there were 56 confirmed outbreaks of SE infection, in 2000 there were 50, and in 2002 there were 32 (Ref. 13). The number of outbreaks has remained roughly constant since 2002; in 2004 there were 28, in 2005 there were 35, and in 2006 there were 26 SE outbreaks in the United States (Ref. 13). Although these data indicate that there has been a decrease in reported outbreaks (and associated illness) linked to SE infection since the mid-1990s, the incidence of SE infection in the United States remains much higher than in the 1970s (Ref. 14), and the decrease in reported outbreaks of SE illness since 1999 has appeared to slow or stop compared to decreases seen in the mid-1990s (Ref. 15). CDC recently reported that, of the four pathogens with HP2010 targets,

Salmonella,

with 16.2 cases per 100,000 in 2008, is the farthest from its 2010 target (6.8) (Ref. 10). If current trends continue, we will fall short of the public health and foodborne illness gains required to meet the Healthy People 2010 goal of a 50 percent reduction from the 1997 baseline in both the number of SE foodborne outbreaks and the rate of isolation in the population of foodborne

Salmonella

infections (Ref. 16).

C.

What Is the Connection Between Salmonella and Shell Eggs?

CDC established an epidemiological and laboratory association between eggs and

Salmonella

outbreaks in the mid-1980s (

see

69 FR 56824 at 56826 through 56827). Shell eggs are the predominant source of SE-related cases of salmonellosis in the United States where a food vehicle is identified (a food vehicle is identified in approximately half of the outbreaks of illness associated with SE). Between 1985 and 2002, a total of 53 percent of all SE illnesses identified through CDC outbreak surveillance are attributable to eggs. Where a vehicle of transmission was identified, 81 percent of outbreaks and 79 percent of illnesses identified through outbreaks were attributed to eggs (Ref. 17). These data are in accord with a published analysis by CDC researchers reporting that between 1990 and 2001, 78 percent of vehicle-confirmed SE outbreaks were associated with eggs, primarily raw or undercooked (Ref. 15). Over that decade, 14,319 illnesses were attributed to SE associated with shell eggs (Ref. 15). Most of these attributed illnesses occurred before 1995 (10,406 illnesses), but 3,913 occurred during 1996 through 2001. We believe egg quality assurance programs (EQAPs), consumer and retailer education, and Federal regulations requiring egg refrigeration have contributed to the decrease in SE

illness since the mid-1990s, but that further reductions in SE illness and foodborne salmonellosis cannot be accomplished without additional Federal measures to address SE contamination of shell eggs.

The surface of an egg can become contaminated with any microorganism that might be excreted by a laying hen or through contact with contaminated nesting materials, dust, feedstuff, shipping and storage containers, human beings, and other animals. The likelihood of trans-shell penetration increases with the length of time that the eggs are in contact with contaminating materials. This mechanism of contamination was previously considered the source of all SE contamination of eggs.

However, while environmental contamination is still a route for

Salmonella

contamination, SE experts now believe that the predominant route through which eggs become contaminated with SE is the transovarian route. Although the mechanism is still not well understood, SE will infect the ovaries and oviducts of some egg-laying hens, permitting transovarian contamination of the interior of the egg while the egg is still inside the hen (Refs. 18 and 19). The site of contamination is usually the albumen (the egg white).

Researchers believe that only a small number of hens in an infected flock shed SE at any given time and that an infected hen may lay many uncontaminated eggs (Ref. 20). In a farm-to-table risk assessment of SE in eggs which was conducted by FDA and the U.S. Department of Agriculture's (USDA's) Food Safety and Inspection Service (FSIS) (“the 1998 joint SE risk assessment”) (Ref. 21), we estimated that of the 47 billion shell eggs consumed annually as table eggs (eggs consumed as shell eggs, as opposed to eggs that are used to make egg products), 2.3 million are SE-positive, exposing a large number of people to the risk of illness (Ref. 21). FDA and FSIS updated this risk assessment in 2005 and derived this same estimate (Ref. 22). This figure is based on data compiled from 1991 to 1995 (Ref. 23).

D. The U.S. Egg Industry

On a per capita basis, Americans consume about 234 eggs per year (Ref. 24). U.S. production is relatively stable and has increased only slightly over time. For example, it was at about 60 billion eggs in 1984 and at 67.3 billion eggs in 1998 (Ref. 25). Generally, about 70 percent of the edible shell eggs produced are sold as table eggs, while the remainder are processed into liquid, frozen, or dried pasteurized egg products. The majority of egg products are destined for institutional use or further processing into foods such as cake mixes, pasta, ice cream, mayonnaise, and bakery goods.

Geographically, commercial egg production in the western United States is concentrated in California, and in the eastern United States is centered in Ohio, Indiana, Iowa, and Pennsylvania. Other States in which major producers are located include Texas, Minnesota, and Georgia. Over 4,000 farm sites have 3,000 or more egg-laying hens, representing 99 percent of all domestic egg-laying hens and accounting for 99 percent of total egg production. There are an additional 65,000 farms with fewer than 3,000 egg-laying hens, accounting for the balance of eggs produced (Ref. 26).

E. Current On-Farm Practices

In the proposed rule we described in detail current farm practices to address the risk of SE contamination (69 FR 56824 at 56830 through 56831). Most of the information we provided came from a 1999 study (the Layers 99 study) (Refs. 27, 28, and 29) by USDA's Animal and Plant Health Inspection Service (APHIS) National Animal Health Monitoring System (NAHMS), as well as information on voluntary EQAPs, which are discussed more fully in section I.G of this document.

The Layers 99 study was designed to include information from States that account for at least 70 percent of the animal and farm population in the United States (Refs. 27, 28, and 29). Each operation participating in the study had more than 30,000 laying hens. The study found that egg laying operations varied considerably in size and style of poultry house; approximately 34 percent of the houses had fewer than 50,000 layers, 29 percent had 50,000 to 99,999 layers, 20 percent had 100,000 to 199,999 layers, and 17 percent had 200,000 or more layers. One-third of farm sites surveyed had only one layer house, while 16.5 percent had six or more layer houses. The study also found wide variability within the poultry houses with respect to style of housing and number and level of cages, although less than one percent were cage-free. Manure handling varied with house style and also varied regionally.

The study found that, when a poultry house is repopulated with new laying hens (also known as “layers”), most of the new layers come from a pullet raising facility. Less than 10 percent of layer farms raised pullets at the layer farm site, although some layer farms had their own pullet-raising facilities at other locations. Most (95 percent) of pullets in pullet-raising facilities came as chicks from National Poultry Improvement Plan (NPIP) monitored breeder flocks. USDA's NPIP is a cooperative Federal-State-industry mechanism intended to prevent and control egg-transmitted, hatchery-disseminated poultry diseases. NPIP has monitoring programs for many avian diseases and pathogens, including SE. Chicks are SE-monitored if they are hatched from eggs from flocks that are certified through NPIP as “U.S. S. Enteritidis Clean” breeder flocks (9 CFR 145.23(d)).

Many pullet-raising facilities in the Layers 99 study had their own programs for SE monitoring. In the West region, 83 percent of farms obtained layers from SE-monitored pullet facilities, and 70 percent of layers on all farms came from SE-monitored pullet facilities. Pullet facilities used one or more of the following methods to monitor SE: (1) Dead chick/chick paper testing, (2) environmental culture, (3) bird culture, and (4) serology. Some pullet facilities used competitive exclusion products and/or vaccines to protect pullets against SE.

The study found that in 1997, the average flock was placed for its first production cycle at 17.5 weeks of age. Flocks in their first production cycle reached peak production around 29 weeks of age. At peak production, the average maximum number of eggs produced was 90 eggs per 100 hens per day. Induced molting was used on many farms (83 percent of farm sites). In the West and Southeast regions, 95 percent or more of farms molted birds, while in the Central region just over half (57 percent) of the farms molted birds. On average, molted flocks ended production at 111 weeks of age, while non-molted flocks ended production at 74 weeks of age.

Approximately two-thirds of farms had biosecurity measures that did not allow visitors without a business reason to enter poultry houses. Sixty-two percent of farms that allowed visitors allowed business visitors provided they had not been on another poultry farm that day. Of the farms that allowed visitors in the layer house, most farms (76 percent) required that visitors wear clean boots. The majority of farms prohibited employees from being around other poultry and from owning their own birds.

With respect to pest control, the Layers 99 study estimated that rodents and flies had access to feed in feed troughs on nearly all farms. Fly control was practiced on 90 percent of all farms; baiting was the most common form of

fly control (72 percent of farms). Essentially all farms used some type of rodent control. Chemicals and baits were used for rodent control by 93 percent of farms. Professional exterminators were used on less than 15 percent of farms that used rodent control. Producers rated almost 30 percent of farms as having a moderate or severe problem with mice and almost 9 percent as having a moderate or severe problem with rats.

The Layers 99 study found essentially all farms emptied feeders, 91 percent emptied feed hoppers, 81 percent flushed water lines, 79 percent dry cleaned cages, walls, and ceilings, and 71 percent cleaned fans and ventilation systems. Approximately one-third of farm sites never cleaned or disinfected egg belts/elevators between flocks. Down time between flocks varied regionally; most farms had a down time of more than 11 days, although some were down for less than 4 days.

The Layers 99 study showed that, in 1997, 58 percent of farms tested for SE. The number of farms testing for SE varied by region. The number and regional distribution of farms doing testing for SE is very similar to the number and distribution of farms participating in an EQAP.

F. Voluntary EQAPs

The Layers 99 study found that 51 percent of all farm sites participated in an EQAP sponsored by a State or commodity group (e.g., United Egg Producers). The

Salmonella

Enteritidis Pilot Project (SEPP), begun in 1992 by USDA with special funding from Congress, was one of the first EQAPs in the United States (in 1994, SEPP became the Pennsylvania Egg Quality Assurance Program (PEQAP)). Currently, there are at least nine voluntary EQAPs operated and administered by States or other organizations (Refs. 30 through 36). In addition, certain egg companies operate an EQAP within their own facilities (Ref. 28).

Currently, EQAPs are voluntary for producers. These programs have similar requirements, but vary in how they implement these requirements. All programs require use of NPIP “U.S. S. Enteritidis Clean” chicks or equivalent, biosecurity, rodent control, and cleaning and disinfection of poultry houses. Although most programs require some environmental testing, the amount varies from once to four or five times during the life of a flock. If an environmental test is SE-positive (i.e., SE is detected at any level in any sample), several programs require egg testing, with diversion if the egg testing is SE-positive. Several programs also have State government oversight and recordkeeping requirements. All programs have some educational programs for participants.

G. The Food Code

FDA regularly publishes the Food Code, which provides guidance on food safety, sanitation, and fair dealing that can be uniformly adopted by State and local governments for the retail segment of the food industry. The Food Code provisions are not Federal requirements; however, they are designed to be consistent with Federal food laws and regulations. The Food Code is written so that all levels of government can easily adopt its text into a legal requirement.

Beginning with the 1993 edition, the Food Code was issued in its current format and was revised every 2 years. In 2002, with the support of the Conference for Food Protection, FDA decided to move to a 4-year interval between complete Food Code revisions. FDA published the 2005 Food Code, which is the first full edition to publish since the 2001 edition. During the 4-year interim period, a Food Code Supplement that updated, modified, and clarified certain provisions was made available. The provisions relevant to egg safety at establishments serving highly susceptible populations can be found in the 2001 Food Code in sections 3-202.11(C), 3-202.13, 3-202.14(A), 3-401.11(A)(1)(a) and 3-801.11(B)(1), (B)(2), (D)(1), (D)(2), (E)(1), and (E)(2). These Food Code provisions include the use of pasteurized eggs in recipes where eggs are raw or undercooked (e.g., Caesar salad, hollandaise sauce, eggnog), and if eggs are combined, unless the eggs are cooked to order and immediately served or combined immediately before baking and thoroughly cooked. The 2001 provisions all substantively remain the same in the 2005 Food Code, but sections 3-801.11(D)(1) and (D)(2) are now designated as 3-801.11(C)(1) and (C)(2), and sections 3-801.11(E)(1) and (E)(2) are now designated as 3-801.11(F)(1) and (F)(2). In addition, FDA amended the definitions of “Eggs” and “Egg Products” in the 2005 edition of the Food Code to clarify the difference between “egg” (shell egg) and “egg product” (liquid, frozen, or dry egg). Also, FDA clarified that baluts and reptile eggs are excluded from the egg-related provisions of the Food Code.

Through careful examination of State retail food codes, FDA has identified 47 States and territories (out of 56 States and territories) that have either adopted the 2005 Food Code or provisions that require the same prevention measures for highly susceptible populations (Ref. 37).

H. Rationale for the Final Rule

This rule is the most recent in a series of farm-to-table egg safety efforts begun by FDA and FSIS in the 1990s. These efforts are described in more detail in the proposed rule (69 FR 56824 at 56827 through 56829). Among these initiatives was the FDA and FSIS 1998 joint SE risk assessment (Ref. 21), discussed in detail in the proposed rule (69 FR 56824 at 56829), which concluded that a broad-based policy, encompassing interventions from farm to table, is likely to be more effective in eliminating egg-associated SE illnesses than a policy directed solely at one stage of the production-to-consumption continuum. In 2004, after FDA's proposed rule was published, FSIS published a draft risk assessment for SE in shell eggs and

Salmonella

spp. in egg products. This risk assessment was then published as final in October 2005 (Ref. 22).

There are currently several Federal regulations related to egg safety at the food service level. These regulations include a final rule issued by FSIS for refrigeration and labeling of eggs during transport and storage when packed for the ultimate consumer (63 FR 45663, August 27, 1998) and an FDA final rule that requires labeling of eggs and refrigeration of eggs at retail establishments (65 FR 76092, December 5, 2000). However, this is the first and only Federal rule that addresses the introduction of SE into the egg during production. Interventions that can reduce the number of SE-contaminated eggs at the production phase are of particular interest. Because progress in reducing the number of illnesses and outbreaks appears to have slowed or stopped, these additional preventive measures are needed to reduce further the risk of SE illnesses and meet our public health goals. Because eggs remain the primary source of SE infections, continued actions to improve egg safety are the most effective way to reduce the overall number of SE infections and outbreaks and to achieve our public health goals.

II. Highlights of the Final Rule and Summary of Significant Differences Between the Proposed and Final Rules

A. Highlights of the Final Rule

The provisions in the final rule are described briefly in the following paragraphs, and are discussed in more detail later in the preamble of this document.

• Persons who produce shell eggs from a farm operating with 3,000 or

more laying hens, unless that farm sells all of its eggs directly to consumers or does not produce shell eggs for the table market, are subject to this final rule (21 CFR 118.1(a)).

• Shell egg producers need only comply with refrigeration and registration requirements if all of their shell eggs from a particular farm receive a treatment as defined in the final rule (§ 118.1(a)(2)).

• Persons who transport or hold shell eggs for shell egg processing or egg products facilities are required to comply with the refrigeration requirements of this final rule (§ 118.1(b)).

• Shell egg producers are required to use the following SE prevention measures:

• Have and implement a written SE prevention plan that includes all mandatory SE prevention measures (21 CFR 118.4);

• Procure pullets that are SE-monitored, or raise pullets under SE-monitored conditions (§ 118.4(a));

• Use a biosecurity program, meaning a program that includes limiting visitors on the farm and in poultry houses; maintaining personnel and equipment practices that will protect against cross-contamination from one poultry house to another; preventing stray poultry, wild birds, cats, and other animals from entering poultry houses; and prohibiting employees from keeping birds at home (§ 118.4(b));

• Use a program to control rodents, flies, and other pests that includes monitoring for pest activity and removing debris and vegetation that may provide harborage for pests (§ 118.4(c)); and

• Clean and disinfect poultry houses before new laying hens are added if an environmental or egg test was positive for SE during the life of the flock; cleaning and disinfecting must include removing all visible manure, dry cleaning to remove dust, feathers, and old feed, and disinfecting (§ 118.4(d)).

• Shell eggs being held or transported are required to be refrigerated at or below 45 degrees Fahrenheit (°F) ambient temperature beginning 36 hours after time of lay (§ 118.4(e)).

• Shell egg producers must conduct environmental testing for SE when laying hens are 40 to 45 weeks of age and 4 to 6 weeks after molt (21 CFR 118.5).

• Shell egg producers must conduct egg testing for SE when an environmental test is positive for SE (21 CFR 118.6).

• Administration of the SE prevention measures requires having one or more supervisory personnel, who do not have to be onsite employees, who are responsible for ensuring compliance with each farm's SE prevention plan (21 CFR 118.9).

• Shell egg producers must maintain a written SE prevention plan and records documenting compliance with the requirements in the plan (21 CFR 118.10).

• Shell egg producers must retain records for 1 year after the flock to which they pertain has been taken permanently out of production (§ 118.10(c)).

• Shell egg producers must make records available within 24 hours from the time of receipt of the official request (§ 118.10(d)).

• Shell egg producers must register with FDA (21 CFR 118.11).

B. Significant Differences Between the Proposed and Final Rules

The final rule reflects the following significant changes from the proposed rule:

• Persons who transport or hold shell eggs for shell egg processing or egg products facilities must comply with the refrigeration requirements. Only shell egg producers were subject to the proposed refrigeration requirements.

• Shell egg producers are required to have and implement written SE prevention plans.

The proposed rule did not require that plans be written.

• The requirements for protective clothing and sanitizing stations have been removed from biosecurity program requirements.

• The requirement to “wet clean the positive poultry house” has been removed.

• Egg processors are now permitted to equilibrate refrigerated eggs to room temperature just prior to processing.

• The requirement to begin egg testing within 24 hours after notification of a positive environmental test has been changed to require that results of egg testing be obtained within 10 calendar days after receiving notification of the positive environmental test.

• The required time period to perform environmental testing for SE after molting has been changed from 20 weeks to 4 to 6 weeks after molt.

• Diverted eggs must have labeling on the shipping container, and all documents accompanying the shipment must state “Federal law requires that these eggs must be treated to achieve at least a 5-log destruction of

Salmonella

Enteritidis or processed as egg products in accordance with the Egg Products Inspection Act, 21 CFR 118.6(f).”

• The requirement that one onsite supervisor at each farm be responsible for administration of the SE prevention measures has been changed to allow for more than one supervisor and for offsite supervisors to be responsible.

• Shell egg producers must document that pullets were SE-monitored or raised under SE-monitored conditions.

• “SE monitored” has been defined to mean that pullets are raised under SE control conditions that prevent SE, including the following: (1) Procurement of chicks from SE-monitored breeder flocks that meet NPIP's standards for “U.S. S. Enteritidis Clean” status (9 CFR 145.23(d)) or equivalent standard, (2) environmental testing, and (3) cleaning and disinfection of the environment as needed based upon the results of the environmental testing.

• Shell egg producers must maintain records documenting compliance with each of the SE prevention measures.

• Shell egg producers must maintain records documenting review and modifications of the SE prevention plan and corrective actions.

• Shell egg producers must register with FDA.

C. Compliance Dates

The compliance date is July 9, 2010; except that, for producers with fewer than 50,000 but at least 3,000 laying hens, the compliance date is July 9, 2012. The compliance date for persons who must comply with only the refrigeration requirements is July 9, 2010.

III. Comments on the Proposed Rule

FDA received approximately 2,000 timely submissions in response to the initial comment period on the proposed rule. In addition, approximately 20 timely submissions were received in response to the reopened comment period. The majority of submissions came from individuals and groups advocating animal welfare issues that, for reasons discussed later in this document, are outside the scope of this rulemaking. The remaining comments came from various trade associations, State government agencies, industry, consumer groups, scientific associations, and individual consumers. These comments raised approximately 60 major issues. To make it easier to identify comments and our response to the comments, the word “Comment” will appear in parentheses before the description of the comment, and the word “Response” will appear in parentheses before our response. We have also numbered each comment to make it easier to identify a particular comment. The number assigned to each comment is purely for organizational

purposes and does not signify the comment's value or importance or the order in which it was submitted.

A. General Comments

1. Enforcement by Voluntary EQAPs

(Comment 1) Several comments stated that FDA should implement what some comments referred to as a “recognition regime,” under which parts of the final rule would not apply to (or would be presumptively complied with by) State and industry EQAPs with standards equivalent to the Federal rule. Some comments suggested that all shell egg producers should be subject to the testing and diversion requirements of the final rule, but that egg producers participating in recognized EQAPs would have to meet only the on-farm SE control measures specified by the EQAP. The comments suggested that, as part of the recognition of the EQAPs, FDA should also recognize audits and inspections conducted by State agencies to measure compliance with those programs, rather than conducting separate Federal inspections.

(Response) FDA recognizes that existing voluntary EQAPs have been successful in reducing SE contamination in poultry houses in certain States (

see

discussion in section I.G of this document). However, for several reasons, we do not agree that States with EQAPs that are recognized by FDA should not be subject to this rule.

First, as discussed, these programs are not uniformly administered or equally comprehensive in their prevention measures. In addition, currently the EQAPs that exist are voluntary for shell egg producers. Although the existing EQAPs all have similar requirements, they vary in how those requirements are implemented. This rule will establish uniform, nationwide requirements to prevent SE in shell eggs during production, storage, and transportation. FDA believes that these requirements will further reduce SE illness and deaths associated with egg consumption.

On the other hand, we agree that we can enlist the assistance of existing EQAP organizations and officials in implementing FDA's regulation. The rule provides that a State or locality may, in its own jurisdiction, enforce this rule by carrying out inspections under § 118.12(b) (21 CFR 118.12(b)) and by using the administrative remedies in § 118.12(a) unless FDA notifies the State or locality in writing that its assistance is no longer needed. FDA plans to provide guidance to States and localities through an enforcement and implementation guidance subsequent to this final rule.

2. Vaccination of Layers Against SE

(Comment 2) Some comments agreed with FDA's conclusion, discussed in the proposed rule, that there is insufficient scientific support for a requirement that layers be vaccinated against SE (69 FR 56824 at 56847). Some of these comments stated that FDA should encourage voluntary vaccination efforts by, for example, allowing producers that can demonstrate the effectiveness of their vaccination programs to follow an alternative protocol for environmental testing before depopulation. One comment encouraged the use of SE vaccinations as an added prevention measure against SE contamination of shell eggs and recommended that an option of using a vaccination program should be available to shell egg producers. In support, the comment stated that data exists from the United States and Europe that the comment said demonstrates the efficacy of vaccination programs. The comment did not provide additional data in support of these statements.

Another comment stated that the available research and field evidence support a conclusion that vaccines used with other SE control measures will reduce SE.

(Response) FDA agrees with the comments supporting only voluntary vaccination of layers. As we stated in the proposed rule, there are insufficient data on the efficacy of vaccines, particularly data reflecting field trials under “real world” conditions, to support a mandatory vaccination requirement (69 FR 56824 at 56847). We also believe that data on the efficacy of vaccines are insufficient to allow substitution of vaccination for any of the SE prevention measures required in this final rule. If individual producers have identified vaccines that are effective for their particular farms, we encourage the use of the vaccine as an additional SE prevention measure.

3. Delegation of Inspection Responsibilities to Other Federal or State Agencies

(Comment 3) Two comments urged FDA to delegate farm inspection responsibilities to USDA's FSIS and Agricultural Marketing Service (AMS) or the State Departments of Agriculture, because these agencies are already involved in oversight of various aspects of egg production. Similarly, another comment stated that APHIS and FSIS are more qualified than FDA to address disease and pathogen risk reduction in live animal production operations.

(Response) FDA disagrees with the suggestion that we should delegate inspection responsibilities under this rule to USDA or the States. Although we coordinate our respective egg safety efforts with FSIS and AMS, each agency has distinct responsibilities and skills, all of which benefit consumers of shell eggs and egg products. These responsibilities and skills do not necessarily overlap as a practical matter (for example, AMS personnel are in certain shell egg packing plants, but not in the layer houses). Furthermore, the rule provides that any State or locality that is willing and able to assist FDA in enforcing the rule may do so in its own jurisdiction.

4. Induced Molting

(Comment 4) Several comments responded to the request in the proposed rule for comment and data concerning induced molting (69 FR 56824 at 56846 through 56847). We received a number of comments encouraging FDA to ban induced molting of laying birds. These comments stated that this practice stresses the immune function of chickens, resulting in the promotion of SE contamination in shell eggs and egg products; that it leads to plucking and consumption of feathers that may be contaminated with

Salmonella;

and that the plucking may itself also stress the immune system. The comments provided some references for these assertions. Another comment stated that USDA supports elimination of forced molting to reduce SE contamination and that the American Veterinary Medical Association also opposes the practice.

Other comments supported the absence in the proposed rule of provisions addressing molting. These comments stated that the research on which claims about post-molt SE shed are based have primarily been laboratory, rather than field research, involving large challenge doses of SE that would not be duplicated in the field and strains of chickens different from those common in commercial laying operations. The comments stated that there is only emerging research into how to use a variety of diets to control the natural process of molting in the egg production setting.

(Response) We addressed the issue of induced molting at length in the proposed rule (69 FR 56824 at 56846 through 56847). We discussed the limitations of studies cited to support the assertion that induced molting increases SE contamination of eggs and stated that we did not believe that we had adequate data upon which to rely for a final decision on the issue of the

relationship between induced molting and SE contamination of the environment and of eggs. Although the proposed rule specifically requested comment and data related to our discussion of induced molting, we did not receive any new data on the relationship between induced molting and SE contamination of the laying environment and of eggs. As a result, we do not have adequate evidence to support including a prohibition on induced molting in the final rule.

5. Indemnification

(Comment 5) One comment suggested that we research whether the Public Health Service Act (the PHS Act) would allow us to indemnify persons whose economic interests are adversely affected by this rule, for example, as a result of diversion of shell eggs to breaker facilities. The comment suggested that, should we conclude that we lack such legal authority, we should consider whether to request it from Congress. Another comment suggested that a Federal compensation package may be needed for smaller producers that lack pasteurization capability.

(Response) Unlike APHIS, FDA is not required or explicitly authorized by Federal statute to compensate persons whose economic interests are adversely affected by certain Agency actions.

1

Further, FDA notes that although some producers will face economic costs from the diversion of eggs to the table market, as discussed in section V of this document (Analysis of Economic Impacts), the economic benefit from illnesses averted is expected to greatly exceed the cost of this rule. The suggestion that FDA seek statutory authority to pay compensation to indemnify producers is outside the scope of this rule.

1

Under the Animal Health Protection Act, USDA is required to compensate the owner for any animal, article, or means of conveyance that the Secretary of Agriculture requires to be destroyed (7 U.S.C. 8306(d)). Under the Plant Protection Act, USDA is authorized to pay compensation to any person for economic losses incurred as a result of action taken by the Secretary of Agriculture under a declaration of extraordinary emergency (7 U.S.C. 7715).

B.

Comments on “Shell Egg Producers Covered by the Requirements in This Part” (Proposed and Final § 118.1)

Exemption of Producers With Small Flocks

(Comment 6) Several comments addressed our proposed exemption of shell egg producers with small flocks, defined as flocks of less than 3,000 laying hens at a particular farm. Most of these comments argued that these small flocks are less likely to have adequate SE prevention measures and that excluding them would be contrary to the public health goal of the rule. The comments suggested that smaller facilities are less likely to have adequate refrigeration capacity, effective rodent control, an effective biosecurity program, measures in place to limit laying hens' exposure to manure on building floors and exposure to the outdoors; that they may pose a greater risk that they will transport and hold eggs without proper refrigeration; and that they may be less likely to obtain replacement pullets or chicks from breeders who participate in the SE prevention programs. One comment similarly suggested that eggs from these smaller producers might be associated with a disproportionate share of sporadic illnesses and even some outbreaks. The comments did not provide data to support these concerns; one comment from one of the larger trade associations stated that it was not aware of research that would support any conclusion that smaller operations would be either more or less likely to have an SE problem than larger, commercial operations.

One comment proposed that FDA reduce the exemption to producers with less than 500 chickens or require all producers not selling directly to consumers to comply with the rule. This comment suggested that FDA may not be aware of outbreaks associated with eggs from these producers because the eggs are not likely to be shipped interstate.

One comment cited our $1.01 per hen ($0.05 per dozen) estimate of the cost to farms with between 3,000-19,999 layers as an illustration of the large financial burden that the rule imposes on these farms.

(Response) We do not believe that there is at this time sufficient evidence to warrant extending the rule's coverage to producers with fewer than 3,000 laying hens. As we explained in the proposed rule (69 FR 56824 at 56832), because producers with fewer than 3,000 layers do not contribute significantly to the table egg market, imposing any one or all of the restrictions on them will have little measurable impact on the incidence of SE. We have no information documenting that there is an elevated risk of sporadic illness or outbreaks associated with eggs sold directly from farmer to consumer or from a producer with fewer than 3,000 laying hens.

FDA disagrees with the statement that we may be unaware of outbreaks associated with eggs from small producers because these producers are less likely to ship eggs interstate. The outbreak data relied on by FDA is in general submitted by State Departments of Health to CDC. As noted earlier, cases of salmonellosis must be reported to local health departments, who in turn provide information to States and to CDC.

FDA recognizes that the cost per hen is higher for smaller farms. However, though not specifically broken out in the regulatory impact analysis, for farms with between 3,000 and 19,999 layers, the public health benefits of the rule exceed the costs by more than $90 million annually and costs do not exceed benefits for any of the individual provisions of the rule. There are a number of features of the rule itself and in our plans for implementation to facilitate smaller farms' compliance with the rule. For example, this final rule has a staggered compliance schedule, which provides smaller egg producers (those with between 3,000 and 49,999 layers) 3 years to comply with the final rule. FDA will continue to evaluate the impact of this rule on smaller farms and will consider taking appropriate steps to mitigate those impacts, where it is possible to do so without reducing safety. In addition, FDA intends to provide guidance on the recordkeeping and other provisions of the rule, including small entity compliance guidance. We plan to use guidance, to the extent feasible, as a vehicle to identify areas where compliance could be achieved via flexible approaches that would mitigate the financial impact while preserving the public health benefits of the rule. We plan to solicit public and industry input on this guidance.

Therefore, FDA has retained the exemption from all provisions of this final rule for farms with fewer than 3,000 layers.

C.

Comments on “Definitions” (Proposed and Final § 118.3)

1. Poultry House

(Comment 7) One comment questioned the proposed definition of a poultry house, which requires that different sections of a single building separated by walls be considered as separate houses. The comment noted that the definition would not address the risk of airborne transmission of SE. The comment stated that “there is considerable evidence that SE can be transmitted through dust and other airborne particles,” citing three references in support. The comment noted that the proposed rule did not require that separate sections in a building have separate ventilation systems, but did require biosecurity

procedures to ensure that there is no introduction or transfer of SE from one section to another. The comment suggested that the definition of a poultry house should clarify that the biosecurity procedures should include transfer through airborne particles.

(Response) FDA recognizes that SE may be transmitted through dust and other airborne particles. However, FDA does not believe that separate ventilation for each section of a house should be mandated because there is great variation in design and placement of houses and ventilation systems, and separate ventilation may not be necessary in every circumstance. Depending on the layout of a farm and the type and number of houses, a producer should decide whether ventilation needs to be addressed as part of farm-specific biosecurity measures to prevent the introduction or transfer of SE from one section to another.

The proposed definition of “poultry house” stated “For structures comprising more than one section containing poultry, each section is enclosed and separated from the other sections,

and each section has a biosecurity program in place to ensure that there is no introduction or transfer of SE from one section to another.

” (Emphasis added.) The final phrase has been removed from this section and added as an introduction to § 118.4(b) (biosecurity) to make clear that you must “take steps to ensure that there is no introduction or transfer of SE into or among poultry houses,” and that “[a]mong such biosecurity measures you must, at a minimum” include a number of specific measures in the biosecurity plan. If the design of a farm and its poultry houses needs an additional measure of ventilation to prevent cross-contamination, then such a measure should be added to the biosecurity plan.

In addition, in the final rule we have revised the definition of “poultry house” to clarify that “[f]or structures comprising more than one section containing poultry, each section that is separated from other sections is considered a separate house.”

2. Treatment

(Comment 8) Some comments stated that a survey of egg processors to determine their current pasteurization practices supports a 5-log reduction, although many processors achieve a substantially greater pathogen reduction. The comments stated that the survey indicated that 50 percent of survey respondents reported that they achieve a 5-log reduction, and the other 50 percent reported a 7-log or greater reduction. The comments stated that the current 5-log reduction requirement appears to provide an adequate margin of safety, because specified temperatures and holding times do not take into account the additional kill achieved in the product while it is heating up to, and cooling down from, the pasteurization temperature.

(Response) FDA agrees with the comments that a 5-log reduction in SE via pasteurization or an alternative approach or the processing of egg products to achieve an equivalent level of protection is appropriate to ensure the safety of shell eggs. Therefore, we have retained the definition for the term “treatment” (or “treated”) in § 118.3 of the final rule as “a technology or process that achieves at least a 5-log destruction of SE for shell eggs, or the processing of egg products in accordance with the Egg Products Inspection Act. We established this standard in 1997, in response to a USDA/AMS request to FDA on criteria for shell egg pasteurization. AMS then published this standard in its

Federal Register

notice on official identification of pasteurized shell eggs on September 24, 1997 (62 FR 49955).

Additionally, both FDA and FSIS are evaluating additional measures to improve egg safety, and FSIS intends to issue proposed rules in the near future for egg products plants and egg handlers, including egg handlers who operate in-shell pasteurization treatments. FDA and FSIS will continue to work closely together to ensure that our egg safety measures are consistent, coordinated, and complimentary.

D.

Comments on “Salmonella Enteritidis (SE) Prevention Measures” (Proposed and Final § 118.4)

1. Chicks and Pullets (§ 118.4(a))

FDA reopened the comment period on May 10, 2005, to seek further comment and information on industry practices and programs that prevent SE-monitored chicks from becoming infected by SE during the period of pullet rearing until placement into laying hen houses (70 FR 24490). We received approximately 20 submissions that provided additional information and data on the specific questions that FDA presented.

(Comment 9) Several comments stated that on-farm prevention practices must address each stage in the life of laying flocks, including the pullet-rearing stage. These comments stated that applying the FDA-mandated practices to layers only after they have been placed in layer hen houses may be too late to ensure protection against SE, as the layers' ovaries may already be contaminated with the pathogen. The comments urged FDA to make clear in the rule that all of the SE prevention practices apply to both pullet rearing houses and layer houses. The comments noted that this approach would be consistent with the practice of existing EQAPs SE prevention measures that are applicable specifically to pullets.

Many comments suggested that FDA add a new requirement that producers certify that pullets they procure have come from a facility that has an SE-monitoring program. The comments recommended that pullet houses undergo environmental tests for SE for each flock at approximately 10 weeks of age. The comments stated that, if the test is positive, the producer could still accept the pullets, but the producer should be required to test environmentally after placement. In addition, the comments suggested that FDA require that pullet houses should be cleaned and disinfected prior to placement of the next pullet flock. Finally, the comments suggested that FDA require testing for layers used to backfill (replacing dead or diseased layers with other layers) and older flocks that are moved to another facility.

(Response) We agree that SE prevention measures should be in place during the pullet phase of shell egg production and have modified the rule accordingly. We believe this will reduce the risk of placing infected birds into poultry houses. The final rule requires producers to procure pullets from sources where the environment has been tested and found environmentally negative prior to introduction into the laying flock. The environmental testing is required of pullets at 14 to 16 weeks of age and cleaning and disinfection of the pullet environment is required if the environmental test is positive. The cleaning and disinfection procedures include removing all manure, dry cleaning the positive pullet house to remove dust, feathers, and old feed, and following cleaning, disinfecting of the positive pullet house with spray, aerosol, fumigation, or another appropriate disinfection method. Additionally, if the environmental test is positive for SE, producers must begin egg testing within 2 weeks of the start of egg laying. The requirements also include procuring chicks from SE-monitored breeder flocks that meet standards set by NPIP for “U.S. S. Enteritidis Clean” status or equivalent standard.

FDA does not agree that a specific requirement is needed to test birds used to backfill and to test older flocks that are moved to another facility. Section 118.5(a) of the final rule requires

producers to perform environmental testing for SE in a poultry house when any group of laying hens constituting the flock within the poultry house is 40 to 45 weeks of age. Therefore, any layers used to backfill and older layers moved into a poultry house will be, or would have been, environmentally tested at 40 to 45 weeks of age, as are all other layers.

(Comment 10) Several comments supported the proposed requirement that all pullets and chicks be procured from a hatchery or breeding flock that participates in NPIP. These comments noted that NPIP participants have developed effective strategies that have reduced the prevalence of many poultry diseases including SE.

(Response) We have retained the requirement that pullets that are purchased be procured as chicks from SE-monitored breeder flocks that meet NPIP's standards for “U.S. S. Enteritidis Clean” status or an equivalent standard.

2. Biosecurity (§ 118.4(b))

(Comment 11) Some comments stated that FDA should revise its biosecurity requirements to allow egg producers greater flexibility. In addition, some comments challenged specific biosecurity measures as being insufficiently supported by data demonstrating their effectiveness in controlling or preventing SE contamination. Specifically, comments questioned the value of requiring personal protective equipment and sanitizing stations between houses on one farm, limiting visitors, controlling movement of workers from house to house, preventing employees from having poultry at home, and preventing stray poultry, wild birds, and other animals from entering the grounds. According to the comments, on a farm it is the presence of mice near chickens that maintains the SE infection and contributes to SE spread from building to building. One comment asserted that biosecurity efforts on the farm should be focused on “rodents and other issues threatening to introduce or maintain SE.” The comment does not explain what “other issues” the commenter is referring to. The comment also asserted that PEQAP does not have a biosecurity requirement.

(Response) FDA agrees with the comments that biosecurity measures could be more flexible in the final rule without jeopardizing the effectiveness of the SE prevention measures. Specifically, we believe egg producers may be able to devise and implement effective means other than protective clothing and sanitization stations to prevent cross-contamination between houses. For example, in some circumstances placing footbaths and farm-specific footwear at the entrance to a complex, maintaining house specific equipment, or using non-street clothing in the layer houses may be sufficient to prevent cross-contamination between houses. Therefore, we have removed from the biosecurity provisions the requirements for the use of protective clothing and sanitizing stations between houses. This change addresses the diverse poultry housing situations that exist throughout the country by allowing each producer to implement biosecurity practices and procedures appropriate for a particular farm and situation. We also agree that it is impractical to require egg producers to prevent stray animals from entering the grounds. Therefore, we have narrowed the provision for stray animals to apply only to the poultry houses.

However, FDA disagrees with the comments questioning the value of other specific biosecurity requirements. As discussed in the proposed rule (69 FR 56824 at 56835), limiting visitors on the farm and in poultry houses, maintaining practices that will protect against cross-contamination when persons move between poultry houses, and prohibiting employees from keeping birds at home are all vital biosecurity provisions that are commonly in use. According to the Layers 99 study (Ref. 29), 66 percent of farm sites already practice some form of biosecurity; that study found that poultry houses where visitors were not allowed were less likely to test positive for SE.

Biosecurity is a critical part of a farm's SE prevention measures. You must implement these biosecurity measures to prevent the introduction or transmission of SE into or between poultry houses. Furthermore, contrary to the comment, PEQAP requires all participants to maintain an acceptable biosecurity program (Ref. 30). As discussed in section I.G of this document, all current EQAPs require use of NPIP “U.S. S. Enteritidis Clean” chicks or equivalent, biosecurity, rodent control, cleaning and disinfection of poultry houses, and many programs require some environmental testing as well.

We will make further specific recommendations for biosecurity steps and options for achieving these steps, based on current science and best practices, in a guidance that we plan to issue subsequent to this final rule. We emphasize, however, that biosecurity is an important and integral part of any poultry farm's SE prevention program, and that the biosecurity requirements in the final rule are minimum standards; egg producers may incorporate additional biosecurity measures into their SE prevention plans if they believe such measures are warranted.

(Comment 12) One comment stated that if FDA insists on a biosecurity requirement, it should address the movement of pullets, spent hens (hens that have permanently ceased egg production), people, equipment, eggs, flats (a receptacle for storing or transporting eggs most often constructed of cardboard or plastic), and egg shells.

(Response) The comment was not specific as to how these matters should be addressed and did not provide any supporting data concerning the need for particular requirements. However, it was not our intention that the proposed rule's biosecurity provisions addressing the risk of cross-contamination from visitors or the movement of “equipment” be interpreted as an exclusive list of measures to take to prevent the introduction of SE into or among poultry houses. We have amended § 118.4(b) to make this clear, by adding general introductory language, moved from the proposed definition of “poultry house,” that producers must “take steps to ensure that there is no introduction or transfer of SE into or among poultry houses.”

(Comment 13) One comment suggested that the proposed rule is premised on a mistaken belief by FDA that biosecurity alone can prevent the introduction and spread of SE.

(Response) As reflected in the rule, FDA understands that biosecurity is only one element of the measures that a producer must have to prevent SE. Producers must follow additional SE prevention measures, including pullet measures; rodent, fly and other pest control; cleaning and disinfection; and refrigeration.

(Comment 14) One comment questioned whether organic poultry producers would be able to comply with the requirement in the proposed rule (§ 118.4(b)(4)) that requires egg producers to “prevent stray poultry, wild birds, and other animals from entering grounds and facilities.” The comment stated that this requirement is in conflict with a requirement under the USDA National Organic Program (7 CFR part 205) that organic poultry producers must provide outside access for all livestock. The comment also stated that farms that are based on a pastured poultry system, which typically provides a substantial percentage of the birds' diet from pasture, would have difficulty complying with this requirement.

(Response) We agree that it would be difficult to prevent stray poultry and

other animals from entering the grounds of the farm, and we believe it is sufficient to keep stray animals out of the poultry house. Therefore, in the final rule, we have changed the requirement for stray animals so that it applies only to poultry houses rather than the entire grounds. Further, we have consulted with AMS, which administers the National Organic Program, and AMS has informed us that this requirement would not make it impossible for eggs to qualify as organic (Ref. 38).

3. Pest Control (§ 118.4(c))

(Comment 15) Some comments supported the rodent control program requirement in proposed § 118.4(c)(1), but questioned the role of flies in the spread of SE and recommended elimination of the pest monitoring under proposed § 118.4(c)(2). The comments further stated that if measured outside the poultry house, the fly count might reflect flies that are present from external locations, such as animal housing at adjacent properties.

(Response) FDA disagrees that the provision for monitoring flies in § 118.4(c)(2) should be removed or modified. In the proposed rule we described research by FDA and others showing that flies harbor SE within the poultry house environment (69 FR 56824 at 56835). According to the Layers 99 study, flies, like rodents, have access to feed troughs on nearly all farms. Further, the fly monitoring procedure can be performed inside the layer house, thus creating an accurate reflection of the presence of flies there.

For clarification, FDA has replaced the term “pest” in § 118.4(c)(2) in the final rule with “flies” because “pest,” which is defined to mean any objectionable animal including, but not limited to, rodents, flies, and larvae, is too broad in the context of this specific provision.

(Comment 16) One comment stated that PEQAP addresses rodent control, but does not address fly control. The comment recommended that fly control be included in the FDA regulation, but that the States individually and independently decide the number of flies allowed for maintaining compliance with the regulation. The comment suggested that under State or local requirements or when a farm has a problem, the spot cards be used to determine the numbers and, therefore, the appropriate control program.

(Response) FDA disagrees with the comment that the States should individually and independently decide the number of flies allowed for maintaining compliance with the regulation. This rule establishes minimum national standards based on measures that have been shown to prevent SE. The comment did not provide any rationale for addressing flies on a State-by-State basis. Further, the rule provides flexibility in how fly presence is determined, allowing not just spot cards, but also Scudder grills, sticky traps, or other appropriate monitoring methods. FDA intends to publish guidance on the requirement to monitor for flies and on the level of fly activity considered acceptable.

The literature suggests that 50 or fewer hits on a spot card or sticky trap per week or a count of less than 20 on a Scudder grill indicate satisfactory fly control ((Refs. 39 and 40).

4. Cleaning and Disinfection (§ 118.4(d))

(Comment 17) One comment suggested that mandatory cleaning and disinfection measures should not require removal of “all visible manure” in a hen house following a positive environmental test and depopulation, but should allow for flexibility with respect to manure removal. The comment stated that complete removal of all manure would destroy biological controls for flies (such as parasitic wasps). The comment also argued that this requirement is impractical, because many producers only remove manure from the houses during those times of year when they can immediately apply it to fields. Several comments stated that the requirement to remove all visible manure is impractical for large, complex poultry farming operations, because commercial in-line, multi-tiered cage layer houses with related accessories and equipment for watering, feeding, egg collection, manure deflection, storage, and removal might be impossible to bring into compliance. The complex machinery (some electrical) is very difficult to clean at best and is just not compatible with wet cleaning. It would also be difficult to accomplish this cleaning in very cold climates because of freezing, in that the layers were an important source of house heat until they were removed for replacement. The comment also noted it might be difficult to enforce a requirement such as “removal of all visible manure.”

(Response) We disagree that flexibility should be allowed with respect to manure removal after a positive environmental test. First, even if it is true that complete removal of all manure would “destroy biological controls for flies” (presumably, by removing parasitic wasp larvae), the wasp population could be restored by the firm, if biological controls are an intended and effective component of the firm's fly control efforts. Data available to FDA indicate that there are non-biological methods of control available to producers (i.e., chemical and mechanical methods) and that these methods are used by most laying hen houses. Moreover, the available data indicate that the role of parasitic wasps in controlling flies is currently being debated in the scientific literature, with most of the work being done in cattle feedlots. Meyer

et al.

(1990) (Ref. 41) and Andress and Campbell (1994) (Ref. 42) found parasite treatments had no apparent affect on adult fly populations, while Weinzierl and Jones (1998) (Ref. 43) concluded that parasitism significantly reduced the fly population. In the one study we are aware of concerning the use of parasitic wasps to control flies in the context of poultry facilities, variable results were obtained (Kaufman

et al.,

2001) (Ref. 44).

Furthermore, limited data suggest that total cleanout of manure is feasible even where parasitic wasps are used to control flies. A study by Hinton and Moon (2003) (Ref. 45) on the effect of a total cleanout on fly control in chicken houses compared the effect of a total cleanout of manure from chicken houses to two partial cleanout methods. Initially, the increase in flies was greatest in those houses with total cleanout, but subsequent differences between the three cleaning methods were small and the fly densities remained relatively stable for 3 months in all houses. Although this study did not specifically evaluate parasitic wasps, it supports a finding that total cleanout of poultry houses will not adversely affect fly control efforts (Ref. 45).

Second, the fact that manure cannot always be applied to fields does not mean that it should not be removed from poultry houses. Manure removed from a house can be composted, stored in a manure barn, or spread on a field depending on the time of year that it is removed.

Finally, we do not understand why manure removal at a large operation would be impractical. We acknowledge that a large operation has more manure to handle, but FDA has visited large operations that do clean out the manure, and we are unaware of any unique problems for such operations.

Because manure is a reservoir of SE that has been shed by infected laying hens, once a poultry house has had an SE-positive environmental or egg test, it is important that all visible manure be removed. Removing all visible manure before new laying hens are placed into a house will help to prevent the SE from

infecting the replacement flock via the manure and rodents.

Therefore, FDA concludes that, to prevent the spread or perpetuation of SE from one flock to another, a producer must remove all visible manure from a poultry house before new laying hens are added to the house when an environmental test was positive for SE at any point during the life of the flock that was housed in the poultry house prior to depopulation. The agency realizes that the floor in a concrete-floored house could appear light gray, but we do not expect to see any accumulation of manure in a house that has had the manure removed, and we do not anticipate practical difficulties in our ability to enforce this requirement. We plan to publish guidance on acceptable manure removal subsequent to this final rule.

(Comment 18) Several comments objected to the wet cleaning requirement in the proposed rule and suggested alternatives such as allowing flexibility so long as the cleaning and disinfection procedures are sufficient to eliminate SE. The comments stated that wet cleaning is impractical during the coldest months in some States; that it can encourage the growth of SE by creating an environment for growth of microorganisms in the poultry house; and that wet cleaning will harm some mechanical and electrical parts of equipment and cages. The comments argued that there is no scientific consensus in favor of wet cleaning.

(Response) We agree that wet cleaning may not be practical in all situations and have removed the requirement from the final rule. As discussed in the proposed rule (69 FR 56824 at 56836), it is important that, once a poultry house has had an SE-positive environmental or egg test, a producer make every effort to rid the environment of SE before new laying hens are placed into that house to prevent the SE problem from being perpetuated in the replacement flock. The final rule retains the requirement in this circumstance to dry clean the poultry house to remove dust, feathers, and old feed prior to the addition of new laying hens to the house and following cleaning, to disinfect the positive poultry house with spray, aerosol, fumigation, or another appropriate disinfection method.

5. Refrigeration (§ 118.4(e))

(Comment 19) Several comments raised concerns about the requirement in § 118.4(e) of the proposed rule that egg producers should refrigerate shell eggs if they are held longer than 36 hours. Some comments urged FDA to change the time at which refrigeration is required to 72 hours after production. The comments noted that 72 hours would accommodate shell egg production over weekends and smaller producers that have pickups less frequent than daily, while at the same time ensuring that eggs are not accumulated and held over long periods without refrigeration.

One comment argued that the requirement to refrigerate eggs within 36 hours could actually be counter-productive with respect to the safety of eggs destined for use in the table market. The comment reasoned that more checks and cracks will occur when previously refrigerated eggs are washed due to the greater change in temperature. The comment recommended that FDA not set a prescriptive time requirement for refrigeration of table eggs unless further research justifies the need, but that if a time limit for refrigeration must be set, it should be set at 72, not 36, hours.

(Response) We disagree that eggs should remain unrefrigerated for up to 72 hours after laying. Our proposed requirement that eggs be refrigerated if stored more than 36 hours was based on data indicating that, although fresh shell eggs provide an inhospitable environment for

Salmonella

to multiply, the chemical and physical barriers against bacterial movement and growth in shell eggs degrade as a result of the time and temperature of holding (69 FR 56824 at 56836 through 56887). As they degrade, shell eggs provide an increasingly more hospitable environment for the growth of SE. Studies have shown that SE, when inoculated into the albumen (whites) of whole shell eggs, multiplied to high numbers if the eggs were not properly refrigerated (Refs. 46, 47, and 48).

The 36-hour limit for unrefrigerated holding is supported by a model, contained in the 1998 joint SE risk assessment (Ref. 21), which was developed to examine the relationship among holding time, holding temperature, and yolk membrane breakdown as an indicator of SE risk. (The yolk membrane separates the nutrient-rich yolk and any SE bacteria that might be present in the albumen; breakdown or loss of the yolk membrane results in rapid growth of SE present in the albumen.) The model showed that, at 70 to 90 °F (i.e., temperatures that might be observed in unrefrigerated egg holding areas in farms or warehouses or in transport vehicles), there was much less breakdown of yolk membrane in eggs held no longer than 36 hours than in eggs held no longer than 72 hours. According to the model, eggs held at 70 °F will experience at least a 16-percent breakdown of yolk membrane after 36 hours and a 25-percent breakdown after 72 hours. Eggs held at 80 °F will suffer at least a 22-percent breakdown after 36 hours and a 39-percent breakdown in the yolk membrane at 72 hours. At 90 °F, there is at least a 33-percent breakdown after 36 hours and at least a 62-percent breakdown of the yolk membrane after 72 hours. In the 2005 FSIS risk assessment (Ref. 22), refrigeration was modeled again; this risk assessment found that limiting eggs to just 12 hours without refrigeration, the shortest timeframe between laying and refrigeration that was evaluated, provided the greatest public health benefit among the time frames studied.

Although, as we stated in the proposed rule, we believe that it is very important that eggs be placed into refrigerated storage as soon as possible after they are laid, we recognize that this may not be practical for all producers. It may take several hours or longer after the eggs are laid before they are collected or picked up for transport. According to the Layers 99 study (Ref. 28), almost half of the farm sites surveyed had egg pickups every 1 to 2 days. In light of all of these data, we are retaining in the final rule the requirement of 36 hours as the maximum amount of time eggs may be held unrefrigerated on the farm.

(Comment 20) Several comments questioned the proposed refrigeration temperature requirement of 45 °F. One comment stated that holding eggs at 45 °F would result in two problems related to egg quality and safety. First, the comment stated that ambient moisture would condense on the cold eggs and cause them to “sweat” before they are washed/sanitized, increasing the chance of surface contamination penetrating the eggs. Second, the comment stated that when cold eggs are moved into the egg washer, which uses hot water, checks or cracks can develop in the shell, lowering the quality of the egg and increasing the risk of future surface bacterial or fungal contamination getting into the interior of the eggs.

(Response) FDA does not agree that a 45 °F refrigeration requirement is too low. This requirement is consistent with FDA's final rule on refrigeration of shell eggs at retail (65 FR 76092), and like that requirement, the rule is based on research demonstrating that

Salmonellae

do not grow well or rapidly at temperatures less than or equal to 45 °F. FDA finds that the scientific evidence on the growth of SE in eggs shows that control of storage temperature of shell eggs can significantly reduce the rate of

multiplication of any SE present (Refs. 46, 47, and 48).

FDA agrees that there can be quality and safety problems such as thermal checks (hairline cracks in the shell) associated with refrigerating eggs immediately prior to processing into either table eggs or egg products. Therefore, FDA is modifying the rule to allow an equilibration step (a step during which the eggs reach room temperature) before eggs are processed. Specifically, under § 118.4(e) of the final rule, shell eggs that have been refrigerated may be held at room temperature for no more than 36 hours just prior to processing to temper them, which will reduce the risk of hairline cracks in the shell that could contribute to bacteria entering the egg during washing if the egg is too cold. We believe the benefits of refrigeration accompanied by equilibration outweigh any possible risk associated with sweating of the eggs.

(Comment 21) One comment stated that the rule is silent on the refrigeration of eggs that are segregated at the grading operation for processing at egg products plants. These are the eggs that do not meet grade requirements, are checked (that is, the shell is cracked, but the shell membrane is intact), or have dirt on the shell. The comment explained that the last two types of eggs pose a significant food safety risk if handled improperly and can be processed only in a USDA-inspected egg products plant. Additionally, the comment stated it may take several days to accumulate a quantity of checked and dirty eggs for shipment. Similarly, the comment stated that surplus eggs produced by hatchery flocks are accumulated and sent to egg products plants for processing and could present a hazard if not properly refrigerated. The comment noted that most shell egg packers and hatcheries currently refrigerate these eggs, but the comment urged FDA to amend the proposed rule to require that eggs segregated at grading operations and at hatcheries and intended for further processing also be subject to the refrigeration requirements proposed for on-farm storage.

Another comment noted that USDA only requires refrigeration at the packer's facility after packing for the consumer. The comment stated that nest run eggs (eggs that are packed as they come from the production facilities without having been washed, sized, and/or candled for quality) and restricted eggs, (eggs whose use is limited by FSIS under the Egg Products Inspection Act because they are, for example, checked or dirty) are not required to be refrigerated. This comment further stated that to maintain the maximum benefit of SE illness reduction from refrigeration, eggs should be refrigerated throughout the distribution chain.

(Response) We sought comment in the proposed rule on whether to require refrigerated transport of shell eggs not already required by regulation or within USDA's jurisdiction; for example, transport of shell eggs from a farm or a packer to a food manufacturing facility. We further stated that we would consider putting into place requirements similar to those we finalized for refrigerated storage of shell eggs at retail (i.e., transport of shell eggs at or below 45 °F ambient temperature).

FDA agrees with the comment that the refrigeration requirement in the proposed rule only addresses eggs held at the farm for more than 36 hours after time of lay. The proposed requirement does not address nest-run eggs, surplus hatching eggs sent to the table egg market, eggs shipped to egg products facilities and then sent to the table egg market, or any other eggs that are held or transported at locations other than at the producer's layer farm. Holding or transporting these eggs without refrigeration allows growth of any SE that may be present in the eggs. We also agree with the comment that, to maintain the maximum benefit of SE illness reduction from refrigeration, eggs should be refrigerated throughout the distribution chain. Therefore, to reduce this potential growth of harmful bacteria, we have modified § 118.4(e) in the final rule to require refrigeration during all storage and transportation beginning at 36 hours after time of lay.

Following are three examples of eggs requiring refrigeration under the final rule, which would not have required refrigeration previously: (1) Unwashed eggs more than 36 hours old from a farm with 3,000 or more layers that have left the producer's farm and are being transported to or are at a shell egg processing facility or are being held in a warehouse; (2) eggs from a farm with 3,000 or more layers that are more than 36 hours old and are being shipped from an egg products facility (USDA-inspected plant) to a shell egg processing facility; and (3) eggs from a hatchery that are more than 36 hours old, were never used for hatching, and are now being transported to a shell egg processing facility. For clarification, in the final rule we are defining “egg products facility” as “a USDA-inspected facility where liquid, frozen, and/or dried egg products are produced,” and “shell egg processing facility” as “a facility that processes (e.g., washes, grades, packs) shell eggs for the table egg market.”

In addition, as discussed in response to comment 20, for those eggs to be processed as table eggs but which are not processed for the ultimate consumer within 36 hours from the time of lay and therefore are required to be held and transported under refrigeration, we are permitting an equilibration step.

E.

Comments on “Environmental Testing for Salmonella Enteritidis (SE)” (Proposed and Final § 118.5)

(Comment 22) Several comments challenged the proposed requirement that egg producers conduct environmental testing when a flock has reached 40 to 45 weeks of age, and if the flock has molted, 20 weeks after the end of the molting process. The comments suggested that instead FDA follow the practice of some EQAPs, which require testing of the layer house environment at the end of the laying period, prior to depopulation. One comment stated that environmental samples should be obtained anytime within the time period of active production, or between the 40th and 60th week of production. In addition, the comment stated that if the environmental samples taken at this time are negative there is no need to conduct additional samples for those birds that have undergone an induced molt.

Another comment stated that the 1998 joint SE risk assessment (Ref. 21), as well as draft 2004 USDA risk assessment (Ref. 49) support a revision to the proposed testing time for post-molt layers from 20 weeks, as proposed, to a 4 to 6 week range post-molt. In support of this suggestion, the comment noted that the 2004 FSIS draft risk assessment finds the greatest risk of infected eggs immediately after molt, but at this time hens are laying few eggs. As a result, the comment estimated that if the increased risk used in the draft risk assessment is multiplied by expected lay post-molt, the greatest number of infected eggs from infected molted flocks will occur between 4 to 6 weeks post-molt.

(Response) We do not agree that the timing for environmental testing of unmolted flocks should be modified. As stated in the proposed rule, environmental testing for SE is an indicator of whether SE prevention measures are working effectively. Testing provides an opportunity for producers to evaluate the SE status of their poultry houses and to take appropriate action if their prevention measures are not preventing SE. Information from an EQAP with a testing protocol indicates that the

highest numbers of positive environmental samples are found when laying hens are 40 to 45 weeks of age (Ref. 50). Additionally, the Layers 99 study found that flocks less than 60 weeks of age (younger flocks) were five times more likely to test positive for SE than older flocks (Refs. 27 through 29). In the absence of any new data, we are retaining in the final rule the requirement that environmental testing for SE be conducted for the flock in each poultry house when each group of laying hens making up that flock is 40 to 45 weeks of age. An SE-positive environmental test at the 40 to 45 week time period notifies a producer that there is a problem with SE contamination. At this point, action can be taken to determine if there are SE-contaminated eggs and to keep SE-contaminated eggs out of the table egg market. Additionally, a positive environmental test during the 40 to 45 week period (just after peak lay) gives a producer sufficient notice to make arrangements for cleaning and disinfection of the contaminated poultry house at depopulation.

FDA does, however, agree that the post-molt environmental test should be moved from 20 weeks post-molt to 4 to 6 weeks post-molt. As the comment noted, the FSIS 2004 draft risk assessment (Ref. 49) (as well as the final version of the risk assessment, Ref. 22, published in 2005) described research by Ebel and Schlosser (Ref. 23) that indicated that “[e]vidence from field studies suggests that molted flocks, in the first 20 weeks of post-molt production, will produce SE-contaminated eggs more frequently than non-molted flocks” (Ref. 22 at page 29). As FSIS explained in the draft and final risk assessments, “[t]he stress of molting is thought to result in an increased susceptibility of hens to SE infection” (Id.). FSIS relied in its analysis on data contained in the “

Salmonella

Enteritidis Pilot Project Progress Report” (Ref. 51) and the study by Holt on immunological factors in laboratory hens (Ref. 52), which were referenced in the proposed rule. As we stated in our response to comment 4, the data underlying the FSIS risk assessment, which we reviewed in the proposed rule, do not support a prohibition on induced molting. However, these data do suggest that there may be some elevated risk that hens may become infected with SE in the post-molt period, before 20 weeks have passed. In light of these studies, we have decided that it would be prudent to conduct environmental SE testing earlier post-molt than was proposed. Therefore, to evaluate the status of a laying hen house post-molt to determine the effectiveness of SE prevention measures during the post-molt laying cycle, we have amended § 118.5(b) to require an environmental test at 4 to 6 weeks after the end of any molting process.

(Comment 23) Several comments suggested that FDA revise the proposed rule to make the environmental sampling plan flexible.

In support of this suggestion, some comments stated that because the rule would cover very diverse egg laying facilities in the United States (e.g., free-range farms and confinement operations using cages or nesting boxes), one single sampling plan would not be effective. One comment recommended a different sampling plan requirement for each operation type. The comment suggested that all confinement “barns” could be sampled under the same plan, and recommended that for such operations FDA require that a minimum of one manure drag sample be obtained from each bank of cages. The comment stated that more research is needed to determine the most appropriate sample sites for operations that are cage-free, pasture-raised, or free-range. Another comment noted that the sampling plan should also be flexible because of variations in operations within geographic areas and across geographic regions, for example, difference in manure collection/disposal systems.

(Response) FDA agrees that because the final rule covers very diverse egg laying facilities, the same sampling plan may not be practical for all operations and that the sampling plan requirement should be flexible to accommodate variations in housing styles. The proposed rule did not specify a particular plan; rather it provided at § 118.7(a) that “[w]ithin each poultry house, you must sample the environment using a scientifically valid sampling procedure.” In the final rule, to make more clear that the appropriateness of a sampling plan depends on the house being sampled, we have modified the language in § 118.7(a) to require “a sampling plan appropriate to the poultry house layout.” Specific sampling instructions have been incorporated into the environmental testing method, “Environmental Sampling and Detection of

Salmonella

in Poultry Houses.”

(Comment 24) One comment questioned whether FDA could appropriately determine whether a producer is using a “scientifically valid sampling procedure,” as required in proposed § 118.7(a). The comment suggested that, for example, there might be no reason to believe that sampling every cage row is more effective than sampling 32 random sites in a laying house. Another comment stated that the only ways to generate drag samples that can be compared across the various types of poultry house are the two discussed in the proposal: Drag swabbing the aisles (the “whole aisle” method) and swabbing a certain number of feet of egg belt (the “limited feet from 32 sites” method) because eggs are collected by hand in only a few houses. Another comment stated that while the procedure for sampling manure pits in a high rise facility with caged layers is fairly straightforward, nonconfinement operations do not have a clear direction on what is the most appropriate sampling site. The comment asserted that it would be unreasonable to expect an operation with 10,000 layers to develop a scientifically valid sampling program when FDA cannot define what is scientifically valid.

(Response) In the proposal FDA described the “whole aisle” and “limited feet from 32 sites” swabbing methods and acknowledged differences in the types of poultry houses and the challenges involved in sampling all houses representatively and consistently. We asked for comments about the appropriateness of different methods of drag swabbing and received no comments that would support one method over the other. To specifically acknowledge differences between poultry houses, the rule now requires “a sampling plan appropriate to the poultry house layout.” FDA believes that there are sufficient data for producers to develop sampling plans for all poultry environments. Over the past ten years, FDA has performed environmental sampling in a variety of poultry houses, which have contained from 3,500 to 250,000 birds and have varied from high rise to shallow pit to sunken water pit houses. The results of this sampling indicate that the manure area and eggbelts are the two best areas to sample (Ref. 53). FDA has incorporated specific sampling instructions into the environmental testing method, “Environmental Sampling and Detection of

Salmonella

in Poultry Houses.”

(Comment 25) One comment stated that because it is common for producers in Hawaii to have multi-age flocks in one poultry house, it would be difficult to perform SE testing for specific flocks that reach the age at which testing is required. The comment further stated that if there is an environmental positive test result for a typical farm in Hawaii (5 to 10 acres), there would be no space to store the eggs to wait for egg

test results. The comment argued that a positive environmental test result could mean depopulation of the entire farm and, even if the egg tests are negative, it could still mean the end of the farm.

(Response) The comment reflects a misunderstanding of the rule. Section 118.5 requires environmental testing of the entire poultry house when any group of laying hens in that house is 40 to 45 weeks of age. If multi-age flocks are housed in the same poultry house, egg producers must perform environmental testing on the entire house whenever any group of laying hens in that house reaches 40 to 45 weeks of age. Furthermore, upon finding an environmental sample positive for SE, there is no requirement to store or otherwise hold the eggs. The eggs from a flock in a house that has tested environmentally positive for SE may continue to be marketed as table eggs until the producer is notified that an egg test is determined positive for SE. At that point, the producer must divert those eggs to treatment.

(Comment 26) One comment argued that a testing regulatory scheme would not be effective in preventing illnesses from SE. This comment stated that environmental and egg testing only indicates the status of the house at the time of the test.

(Response) Environmental and egg testing alone do not prevent SE, but instead serve as an indicator and verification step that the SE prevention plan is working properly. Further, a positive egg test can prevent contaminated eggs from reaching consumers and thereby protect the public health.

Diversion (§§ 118.5 and 118.6)

(Comment 27) We received many comments on our proposed requirement that eggs from a SE-positive layer house environment must be diverted to pasteurization, unless testing of four pools of 1,000 eggs each yields SE-negative results. One comment supported the diversion requirement as a reasonable way to keep higher-risk eggs out of the table egg market, but stated that the requirement could pose an economic risk to shell egg producers that do not have their own egg pasteurization capabilities. Other comments similarly noted that this requirement could have an economic impact on egg producers that lack ready access to egg pasteurization facilities, because they will have to sell their eggs to “breakers” who already have an adequate supply of eggs (through ownership of laying houses or pre-existing contacts with such houses). As a result of this arrangement, egg producers will have to take whatever price they can get from the breakers and the price will inevitably be much lower than the price they would have gotten if the eggs had not come from an SE-positive layer house. Some comments expressed concern that egg product buyers might not want to purchase product known to have come from eggs diverted because of SE, further reducing the breaker's incentive to buy the diverted eggs.

Thus, these comments expressed concern that this diversion would result in a cost to the industry much greater than that projected by FDA in the proposal. One comment stated that, even if they were willing to buy the diverted eggs, breakers might offer a price too low to make it economically feasible to retain the flock. That same comment noted that diversion to the pet food supply chain would not be an option because SE-positive eggs would have to be run through the processing plant, and stated that destruction may be the only alternative in most cases.

(Response) FDA recognizes that diversion of eggs may be expensive or impracticable. We do not agree that we have underestimated these costs. Further, these costs are outweighed by the public health benefit realized by diverting contaminated eggs.

In addition, FDA believes there may be some confusion about the diversion requirement. Under the rule, diversion is required under the following three scenarios: (1) When the environment tests positive for SE, and the producer chooses not to test eggs from that house to determine whether the eggs are also positive; (2) when the eggs in a house test positive for SE; and (3) by order of an FDA, State, or local representative after a finding that shell eggs have been produced or held in violation of this regulation.

(Comment 28) One comment requested that FDA include hard cooking as an acceptable method of diversion.

(Response) If diversion is required, you do not necessarily have to send the eggs to a breaker. You may instead divert them to an alternative process that achieves at least a 5-log reduction in SE, using, for example, in-shell pasteurization of shell eggs or hard cooking of shell eggs.

In the proposed rule, FDA defined treatment as “a technology or process that achieves at least a 5-log destruction of SE for shell eggs, or the processing of egg products in accordance with the Egg Products Inspection Act.” We have retained this definition in the final rule. Thus, as long as the hard-cooking process achieves at least a 5-log destruction of SE, it is an acceptable method of diversion.

(Comment 29) One comment stated that Hawaii has no egg breaking facilities, and that the costs of shipping diverted eggs to breaking facilities in California or elsewhere in the continental United States would be prohibitive. The comment also noted that in the past some breaking facilities on the West coast have refused to accept eggs from Hawaii. The comment requested that the rule be made more flexible to address the situation facing Hawaii and other States with inadequate or no egg diversion capacity.

(Response) FDA recognizes that there is regional variation in the cost of diversion for eggs. For a full discussion of this variation, see section V.F of this document. We understand that there are currently no breaking facilities in Hawaii and that it may not be economically feasible to ship diverted eggs to the continental United States or Canada. For egg producers in Hawaii, and for others also unable to avail themselves of breaker facilities, the cost of diversion per egg is the lost value of a table egg. In the proposed rule, we estimated that the price to a producer for one dozen diverted eggs in Hawaii is $0.53, or $0.044 per egg. We recognize that this cost is more than double the cost of diversion for egg producers in other regions; however, per our usual approach for public health regulations promulgated under the FFDCA and the PHS Act, we are establishing minimum national standards that will equally apply to all States. We acknowledge that diversion for egg producers in situations such as those in Hawaii may be particularly financially challenging. As discussed above, we will use guidance as appropriate to mitigate the impacts associated with implementation of the rule.

F. Comments on “Egg Testing for Salmonella Enteritidis (SE)” (Proposed and Final § 118.6)

(Comment 30) One comment agreed with the sampling protocol established in § 118.6(c) for egg testing for SE, but stated that 24 hours is not a practical timeline to begin egg testing after a positive environment is found. The comment suggested that § 118.6(c) require egg producers to immediately notify the appropriate state agency of the positive environmental findings and that egg sampling commence within 2 weeks after the environmental test results are received. Another comment suggested that FDA revise the time period allowed between receiving a positive environmental sample and conducting the required egg testing from

24 to 72 hours to allow for weekends or holidays when laboratory facilities would most likely not be available to complete the tests. Several comments further argued that the 24-hour requirement for initiating egg testing is impossible, as even collecting the eggs within 24 hours might be difficult at times. In addition, the comments argued that to arrange testing for 1,000 eggs requires scheduling of several items, including people, labs, and media, and cannot be done in 24 hours.

(Response) For the reasons identified in the comments, FDA agrees that 24 hours may not be practical to begin egg testing. Therefore, we have modified § 118.5(a)(2)(ii) and (b)(2)(ii) in the final rule. Rather than setting a time when egg testing must begin, the rule establishes a deadline for conducting and completing such testing and receiving the results. The final rule requires that the results of egg testing for the first 1000 eggs must be obtained within 10 calendar days of receiving notification of the positive environmental test. This time period allows for the farm to obtain a laboratory to do the work and collect the eggs and for the laboratory to perform and complete the tests.

(Comment 31) Two comments stated that the egg sampling procedure should be witnessed by a regulatory agency, such as a State Department of Agriculture.

(Response) FDA disagrees. Other FDA regulations, such as Hazard Analysis and Critical Control Point (HACCP) Procedures for the Safe and Sanitary Processing and Importing of Juice (21 CFR part 120) and Procedures for the Safe and Sanitary Processing and Importing of Fish and Fishery Products (21 CFR parts 123 and 1240), do not require sampling and other testing to be overseen by FDA or State officials to be effective. The egg sampling requirement is expected to be routine and a regular component of the on-farm plan to prevent SE.

Furthermore, to assist FDA in ensuring compliance, the final rule requires that each facility establish and maintain records of plan activities, including egg sampling. Such records will assist FDA in determining whether sampling was performed appropriately.

G. Comments on “Sampling Methodology for Salmonella Enteritidis (SE)” (Proposed and Final § 118.7)

(Comment 32) One comment stated that FDA should distinguish between a sampling plan used to verify or monitor an on-farm program and a sampling plan used for an SE outbreak trace back. The comment also asked for clarification of the scientific justification for the requirement in § 118.7 that egg producers pull a 1,000 egg sample, regardless of the size of the operation. The comment questioned whether sampling for monitoring purposes needs to be as extensive as that undertaken for outbreak trace back situations.

Another comment noted that due to potential breakage, a sample size of 1,050 eggs would eliminate the problem of having to use cracked or broken eggs (i.e., the laboratory can select 1,000 eggs from this 1,050 egg pool).

(Response) The rule requires egg testing after receipt of notification of a positive environmental test (unless the eggs are treated). Sampling after a positive environmental test is intended to effectively detect SE-positive eggs from a flock.

The rule requires that egg producers collect and deliver for testing a minimum of 1,000 intact eggs representative of a day's production four times at 2-week intervals, resulting in a total test of 4,000 eggs over an 8-week period. This sampling scheme is based on data from the SE risk assessment indicating that an SE-contaminated flock may be producing SE-contaminated eggs with a prevalence of 1 in 1,400 (Ref. 54). The sampling scheme would result in a 95 percent probability of accurately detecting an SE-positive egg from a flock producing contaminated eggs with the prevalence calculated in the risk assessment (Ref. 54).

We agree with the potential for breakage raised in the comment concerning the sample size for egg testing and have modified § 118.7(b) in the final rule so that the requirement is to “collect and deliver for testing a minimum of 1,000

intact

eggs representative of a day's production” (Emphasis added).

With regard to the comment regarding making a distinction between a sampling plan for monitoring SE on the farm and for an SE outbreak trace back, FDA notes that this final rule does not address SE outbreak trace backs and is solely designed for the prevention of SE in shell eggs during production, storage and transportation. SE outbreak trace back is beyond the scope of this regulation and will not be addressed here.

H. Comments on “Testing Methodology for Salmonella Enteritidis (SE)” (Proposed and Final § 118.8)

(Comment 33) One comment recommended that FDA modify its required environmental testing method to conform to the methods currently being used by the industry, states and laboratories. One such method is that used by the NPIP. The comment stated that the proposed environmental testing method requires the use of an extra selective agar, bismuth sulfate (BS) agar, which has not been proven to be effective in isolating SE from environmental samples. The comment argued that BS agar is the agar of choice for isolating S. Typhi from clinical samples, but that it is not effective for environmental samples of SE. The comment suggested that the isolation with BS agar is an unnecessary step that should be eliminated from the method.

(Response) The method we proposed for environmental testing is set forth in “Detection of

Salmonella

in Environmental Samples from Poultry Houses,” which was proposed for inclusion in FDA's Bacteriological Analytical Manual (BAM), or an equivalent method with respect to accuracy, precision, and sensitivity in detecting SE. The environmental testing method FDA proposed was very similar to the NPIP environmental testing method. For example, it included the same pre-enrichment and enrichment broth. It was different only in that it specified what specific plating agars should be used, and it required the use of three, not two, plating agars. The selective plating agars identified in the proposed rule method were brilliant green with novobiocin (BGN), xylose-lysine tergitol 4 (XLT4), and BS. BGN and XLT4 are two of the selective plating agars that have been used by some laboratories using the NPIP method.

With respect to the use of BS, FDA has performed additional plating with layer house environmental SE colonies on BS agar and has reconsidered the method for conducting environmental testing. As a result of this review FDA has eliminated the use of BS for environmental testing in the final rule and has changed the method to reflect the elimination of the BS agar. The method specified in the final rule, “Environmental Sampling and Detection of Salmonella in Poultry Houses,” requires only two agars, BGN and XLT4.

The comment did not challenge the specification that BGN and XLT4 be the plating agars used, and we have not changed this specific requirement in the final rule. As in the proposed rule, if other methods are at least equivalent to the specified method in accuracy, precision and sensitivity in detecting SE, they may be used instead of the method specified.

(Comment 34) With respect specifically to environmental testing, a

comment noted that the test does not allow for pooling of samples, which the comment stated would reduce the number of samples the laboratory would have to run with no loss in sensitivity of the test. The comment stated that pooling would reduce costs by 75 percent.

(Response) Although there are data showing that pooling of food samples, under specified conditions, does not compromise method sensitivity, we are not aware of any data, and the comment did not provide any such data, to support pooling for environmental sampling. Until such data become available, it would be imprudent of FDA to specify a test that includes compositing of environmental swabs.

(Comment 35) One comment raised concerns about the proposed egg testing method. The comment stated that the method proposed by FDA differs from the method used by APHIS, as well as other methods used by industry, states and laboratories. In addition to the concern that the method that we proposed is not the same as that used by APHIS, the comment identified two other specific concerns with the proposed egg testing method. First, the comment stated that the proposed egg testing method requires the use of BS, an isolation media that is the media of choice for isolating

Salmonella

Typhi from clinical samples. Second, the comment stated that only two selective agar plates should be inoculated (BGN and XLT4) instead of the five proposed in the method for egg testing.

(Response) Neither the description of the method discussed in the preamble of the proposed rule nor the reference to the method contained in the codified portion of the proposed rule are correct for the egg testing methodology. The method referred to in the codified portion of the proposed rule was actually a comparison study involving varying media and pre-enrichment. The method for testing eggs adopted in the final rule is the method in the BAM, chapter 5, “

Salmonella.

”

Addressing the comments in turn, we disagree that we should adopt the APHIS egg testing method. Like the BAM method, the APHIS method first involves the disinfection of eggs and then the cracking, pooling and mixing of eggs. The two methods diverge at the third step, which is incubation: In the BAM method the pools are incubated at room temperature for 96 hours, while in the APHIS method the pools are incubated for only 72 hours.

The two methods also are different in subsequent steps. In the BAM method, there is a pre-enrichment step in which a portion of the egg pool is enriched with trypticase soy broth supplemented with ferrous sulfate and incubated for 24 hours, after which the pre-enriched sample is placed into 2 selective enrichment broths (tetrathionate and Rappaport-Vassiliades), and subsequent inoculation onto three selective media: BS, xylose lysine desoxycholate (XLD), and Hektoen enteric (HE). In the APHIS method, there is no pre-enrichment step. Instead, egg samples from the incubated eggs are inoculated onto 2 selective agars (brilliant green and XLD). In both methods colonies that grow on the agar plates are sampled to characterize the organism as

Salmonella

by the reaction on two agar slants.

FDA believes that, for the purposes of this final rule, its method is preferable to the APHIS “Egg Sampling Method” (58 FR 41048, August 2, 1993). First, the addition of ferrous sulfate at the pre-enrichment step in FDA's method provides iron, which is needed by

Salmonella

for growth and which may not be present in sufficient quantity in the egg; thus, this step may increase the likelihood of detection. Second, the two selective enrichment media (tetrathionate and Rappaport-Vassiliades) used in FDA's method contain agents that are selective (inhibitory) against the non-

Salmonella

organisms. The inhibition of non-

Salmonella

organisms enhances the test by reducing competition and possible overgrowth from other organisms. Third, the use of three, rather than two, selective plating agars maximizes the possibility of detecting as many SE strains as possible. We note that the APHIS egg sampling method was developed and has been in use since 1993. While it has been and remains a valid sampling method, the FDA method is more sensitive and can better detect the presence of

Salmonella

in food, and our adoption of this newer and more sensitive test will better support the public health goals of this rule. In summary, FDA believes that the specific method prescribed for egg testing in this final rule is tailored to the goals of the rule.

With respect to the two more specific comments, FDA does not agree with the recommendation to eliminate BS in the method for egg testing, for the reasons explained in the previous paragraphs. Nor do we agree that the other two selective agar plates should be BGN and XLT4, rather than HE and XLD. In a comparison study of selective plating agars using selected high moisture foods (Ref. 55), the newer selective plating agars performed comparably with the BAM recommended agars (BS, HE, and XLD) but offered no advantage. The BAM is a collection of procedures preferred by analysts in FDA laboratories for the detection in food and cosmetic products of pathogens and microbial toxins. With some limited exceptions, these methods have been used and peer reviewed by FDA scientists as well as by scientists outside FDA. A new agar such as that proposed in the comments would be added to the BAM only after research indicated superior performance in the context of a variety of foods, and where the agar has been validated by collaborative studies. Therefore, the final rule does not deviate from the proposal in recommending the use of the BAM-recommended plating agars. However, we note that another test that is equivalent to the specified test in accuracy, precision and sensitivity for detecting SE may be used.

(Comment 36) One comment recommended that FDA allow for improvements in the methodology for

Salmonella

testing to be easily and quickly adopted by the industry upon validation of the new method, and that FDA work with other Federal agencies with approved testing methods, such as APHIS and FSIS, to facilitate approval of methods and to reduce the need for one facility to use several different methods for

Salmonella

testing. The comment stated that APHIS, FSIS, and scientific organizations all have approved methods for detecting

Salmonella

and SE. The comment further stated that methods need to provide consistent results, yet be flexible enough to allow the industry to adapt quickly when improvements are made. For example, rapid testing methods are available and approved by some Federal agencies (e.g., FSIS). The comment argued the current proposed rule would not allow a producer to use a rapid method for testing of environmental or egg samples. The comment recommended that FDA conduct a literature review and, if necessary, additional research to determine what methods are appropriate to detect SE in the environment and egg samples, with the goal of identifying methods that are appropriate for the purpose of the testing and less costly (in both time and money) to the industry.

(Response) In the final rule, FDA is allowing for other methods to be used for both environmental and egg testing, provided they are equivalent to the methods we specify in accuracy, precision, and sensitivity in detecting SE.

I. Comments on “Administration of the Salmonella Enteritidis (SE) Prevention Measures” (Proposed and Final § 118.9)

(Comment 37) Several comments suggested that FDA modify the requirement in proposed § 118.9 that one qualified individual at each farm have training equivalent to a standardized curriculum recognized by FDA or be otherwise qualified through job experience to administer the SE prevention measures. The comments proposed instead that FDA require training of a qualified individual responsible for each farm, even if that person is not an onsite employee. These comments noted that many producers employ one individual to oversee multiple farm locations, and that this person generally has more experience and training than the onsite employees and can provide better oversight on developing and implementing SE prevention measures.

(Response) We agree and are amending the language in § 118.9 in the final rule to allow for one or more supervisory personnel, who do not have to be onsite employees, to be responsible for ensuring compliance with each farm's SE prevention measures.

(Comment 38) One comment expressed concern about the burden small producers may experience in complying with the proposed requirement that at least one individual at each farm must successfully complete standardized FDA-curriculum or equivalent training of up to 2 to 3 days on SE prevention measures for egg production. The comment requested that FDA consider developing a training program that could be implemented without requiring travel from the egg operation. Further, the comment requested that FDA not impose deadlines for such training that could be difficult for such small producers to meet.

(Response) FDA plans to work with trade associations, State regulatory officials, and academia/extension officials to develop and offer training opportunities at venues that should satisfy the needs of small, medium, and large size facilities. Further, in the final rule, FDA has reduced the burden of the training requirement by allowing one or more supervisory personnel to serve as the trained administrator for all of the firm's facilities rather than requiring a dedicated, trained individual at each facility. FDA believes this will substantially reduce the burden for small producers to comply. Finally, FDA notes that the rule provides that equivalent job experience can be substituted for training.

J.

Comments on “Recordkeeping Requirements for the Salmonella Enteritidis (SE) Prevention Measures” (Proposed and Final § 118.10)

(Comment 39) In the proposed rule, FDA proposed certain recordkeeping requirements and solicited comments on whether additional recordkeeping measures should be required for a comprehensive SE prevention plan, and whether a written SE prevention plan should be required. Several comments supported the proposed recordkeeping requirements but did not comment on expanding them; one comment stated that there is no need for FDA to expand its recordkeeping requirements beyond those proposed. In addition, several comments supported expanding the proposed recordkeeping requirements to include a written SE prevention plan and records for compliance with SE prevention measures. Several comments noted that such records have been very useful in conducting inspections of facilities to determine compliance with the egg quality assurance program requirements and for identifying problems in the producer's SE prevention plan when a test is positive. Another comment stated that records documenting compliance with all aspects of the SE prevention plan will be essential for a producer to determine if their plan is effective and in making adjustments to improve their plan. One comment opposed the requirement of a written SE prevention plan, stating that while a written plan would undoubtedly be an important management tool, and indeed many operations have such a plan, it is not necessary for FDA to mandate such a document. The comment stated FDA should not place undue emphasis on paperwork, as opposed to actual results. The comment suggested that FDA work with interested parties to develop a model SE prevention plan that could be provided to egg producers for their use.

(Response) FDA agrees with the comments that the final rule should require a written SE prevention plan as well as records to document the effective implementation of that plan. This written SE prevention plan will set forth a producer's plan to implement the regulation's prevention, testing, and diversion measures. A written plan is necessary for producers to ensure that they have effectively and consistently implemented SE prevention measures. Further, a written plan greatly facilitates FDA inspection. SE prevention measures may be quite different among farms, given different facility design and size, and yet be equally effective in preventing SE contamination. Knowledge of the specific prevention measures taken on a farm, as discussed in an SE prevention plan, will assist FDA to assess compliance with the prevention measures.

In addition, reviewing records of implementation of a facility's specific SE prevention measures is the best mechanism for FDA to use to determine whether preventive measures have been implemented over a period of time. These required documents include records of implementation and compliance with all SE prevention measures. Such documents, for example, would include documents that pullets were SE monitored or raised under SE monitored conditions, records of SE environmental and egg testing, and records of activities required by the rule, such as treatment or diversion of eggs, as well as records indicating review of the plan and any changes or modifications made to the plan. Keeping careful written records will help producers ensure that they have effectively and consistently implemented SE prevention measures and will also assist FDA in determining whether the plan is being followed and in identifying problems in the producer's plan when a test is positive. If changes or modifications need to be made, recording such changes or modifications will help ensure such changes are implemented.

Therefore, under § 118.10, FDA is requiring that egg producers covered by all of the requirements in the rule (§ 118.1(a)(1)) maintain the following records documenting their SE prevention measures: (1) A written SE prevention plan; (2) documentation that pullets were “SE-monitored” or were raised under “SE-monitored” conditions, including environmental testing records for pullets; (3) records documenting compliance with the SE prevention measures; and (4) records of review and of modifications of the SE prevention plan and corrective actions taken. FDA intends to issue guidance regarding the recordkeeping requirement.

(Comment 40) Two comments stated that FDA should require purchasers of diverted eggs (e.g., egg breaking facilities, shell pasteurization facilities, hard-cooked operations, or other facilities where the eggs could be treated) to maintain records indicating that the diverted eggs have been treated. These comments, submitted by an agricultural department and poultry and livestock commission of two major shell egg producing states, argued that without records there would be no

ability to ensure the purchaser would treat the eggs and not simply divert them back to the table egg market.

(Response) FDA agrees with the comments' concern that purchasers of diverted eggs might resell them for the table egg market without treating them and that buyers might not know that the eggs must receive a treatment. To address this concern, FDA has modified this final rule by adding § 118.6(f), which requires that when shell egg producers divert eggs, the pallet, case, or other shipping container must be labeled and all documents accompanying the shipment must contain the following statement: “Federal law requires that these eggs must be treated to achieve at least a 5-log destruction of

Salmonella

Enteritidis or processed as egg products in accordance with the Egg Products Inspection Act, 21 CFR 118.6(f).” The statement must be legible and conspicuous. FDA believes this additional requirement will help reduce the likelihood that these eggs will end up on the market without having been treated. We note that USDA-FSIS, not FDA, regulates egg-breaking facilities under the Egg Products Inspection Act (21 U.S.C. 1031

et seq.

).

The costs and benefits of this provision are addressed in section V of this document, Regulatory Impact Analysis.

(Comment 41) One comment questioned the proposed rule to the extent it did not require an SE prevention plan until a producer has a positive environmental test. The comment stated that this delay increases the risk of producing SE-positive eggs that are distributed into the table egg market prior to the test and increases the difficulty of the producer reducing or eliminating SE from the environment and the flock.

(Response) The assertion in the comment that the proposed rule did not require an SE prevention plan until a producer has a positive environmental test is incorrect. Neither the proposed nor final rules make having an SE prevention plan contingent upon a positive environmental test.

(Comment 42) One comment commended FDA's statement that “we intend to consider records that come into our possession under this rule as generally meeting the definition of a trade secret or commercial confidential materials” (69 FR 56824 at 56841). However, the comment requested that FDA identify in the final rule what information will be considered confidential commercial information (CCI) or a trade secret, and under what legal authority FDA will defend this designation against any legal challenges.

(Response) FDA's regulations in 21 CFR part 20 govern the disclosure of information under the Freedom of Information Act (FOIA), including the disclosure of CCI and trade section information. The agency's general policies, procedures, and practices relating to the protection of confidential information received from third parties apply to information received under this rule. It is not necessary that FDA designate information upfront as CCI or trade secret because these determinations can be made before releasing any information. If FDA denies a request under FOIA, it will rely on the provisions in that statute which permit the agency to withhold information.

(Comment 43) One comment questioned FDA's assertion that section 361 of the PHS Act (42 U.S.C. 264) gives it legal authority to inspect records. The comment argued that FDA's reliance upon section 361 of the PHS Act is misplaced and cannot be used to impose records inspection on food establishments where, according to the comment, such inspection is not allowed under section 704(a) of the Federal Food, Drug, and Cosmetic Act (FFDCA) (21 U.S.C. 374(a)).

(Response) In the final rule, FDA relies on sections 402(a)(4) and 701(a) of the FFDCA (21 U.S.C. 342(a)(4) and 371(a)) and sections 311, 361, and 368 of the PHS Act (42 U.S.C. 243, 264, and 271) to require access to certain records. FDA does not rely on section 704(a) of the FFDCA for authority to access records in this rule. Furthermore, the PHS Act provides authority for records access that is independent of the FFDCA. Specifically, section 361 of the PHS Act authorizes the Secretary of Health and Human Services (the Secretary) to make and enforce such regulations as “are necessary to prevent the introduction, transmission, or spread of communicable diseases from foreign countries into the States * * * or from one State * * * into any other State.” The basis for the recordkeeping requirements in the final rule is further explained in section IV of this document, Legal Authority.

(Comment 44) One comment encouraged FDA to incorporate an automated recordkeeping requirement into the proposed rule. The comment stated that an automated system would enhance and support the recordkeeping requirements outlined in the proposed rule. The comment argued that such a system could provide farm-specific data, and an efficient, cost-effective way to research compliance. The comment stated that an automated system would greatly reduce the recordkeeping burden placed upon egg producers as well as the time, frequency, and cost associated with FDA inspections.

(Response) FDA believes that the least burdensome way of implementing the recordkeeping requirements is to specify the information that must be contained in the records, but not the format in which the records are kept. Automated technology may not be available or within the means of all producers covered by the rule. We note that egg producers may choose to use automated recordkeeping as long as they maintain all of the required records.

K. Comments on Registration Requirements for Shell Egg Producers (Final § 118.11)

(Comment 45) In the proposed rule (69 FR 56841 at 56841 through 56842), FDA solicited comments about whether we should require that shell egg producers register with FDA. Several comments supported requiring registrations by egg producers covered by the SE prevention measures. These comments stated that registration of all producers covered by any of the SE prevention measures would be the most efficient method of obtaining the information needed to conduct annual inspections and allocate resources.

Further, several comments stated that such a requirement should be consistent with the program developed under the agency's bioterrorism regulations. The comments further stated that by identifying each farm's location and size, a registration requirement would enable more efficient inspection, as well as better management and oversight of a shell egg recall.

One comment stated that, to create a level playing field across the United States, registering all producers is necessary and that FDA may be able to cooperate with USDA/APHIS, which is presently developing a premises identification program for all animal premises in the United States.

(Response) FDA agrees with the comments and is requiring that egg producers who must comply with all of the SE prevention measures in this rule, and also those producers who must comply only with the refrigeration requirements in this rule, register with FDA and provide information on the name of each farm, its location, layer capacity, and the number of houses. Persons who transport or hold shell eggs for shell egg processing or egg products facilities but who are not egg producers are not required to register with FDA, although they are subject to the refrigeration requirements in § 118.4.

FDA intends to conduct inspections of egg farms to ensure that shell eggs are being produced under controls that will prevent SE contamination and reduce the likelihood that SE-contaminated eggs will cause foodborne illness. We will use the producer registration information to create a database used to efficiently conduct inspections and allocate inspection resources. Covered egg producers must register within 30 days of becoming an egg producer or, if already an egg producer, by the applicable effective date of the rule. Additionally, registered egg producers are required to notify FDA within 120 days of ceasing egg production (excluding seasonal egg producers or those who temporarily cease operation due to labor disputes, fire, natural disasters, or other temporary conditions).

Producers can register online via the Internet, by completing a paper form and mailing or faxing it to FDA, or by sending a CD-ROM containing the relevant registration information to FDA. If ceasing egg production, producers can notify FDA either online via the Internet or by completing a paper form and mailing or faxing it to FDA.

(Comment 46) One comment objected to requiring producers who pack eggs to register, stating that every producer with packing facilities is registered with the FDA under the registration rule and should not be required to register a second time. The comment agreed that producers that do not pack eggs, but sell eggs that will ultimately go into the table egg market, should be registered so that FDA can ensure these firms are following the on-farm production and testing requirements of the SE rule.

(Response) Farms are not required to register under FDA's Registration of Food Facilities regulation (21 CFR 1.226(b)). If a farm also has a packing or processing facility, then only the packing or processing facility is required to register under the registration rule if those packing and processing activities do not qualify under the farm exemption (see “farm” definition for activities that are covered in the farm exclusion under 21 CFR 1.227(b)(3)). Because the packing/processing facility registration information may not fully identify the farm location, FDA is requiring that information in this regulation. If the information that would be provided by an egg producer during registration has already been provided under the registration regulation, the producer may submit its registration number rather than registering again.

(Comment 47) One comment objected to the proposed registration requirement as an unnecessary burden and an unreasonable invasion of privacy. The comment argued that FDA only should check for compliance. The comment further argued that “unexpected visits are not appropriate as a respect for other people and the reality is that no one can hide what you want to see in 24 hours.” The comment further argued that registration will result in a loss of privacy for the producer and is unnecessary for the success of the program.

(Response) FDA disagrees with this comment. As stated above, registration will aid in the identification of egg producers for inspection and compliance purposes. We will use the producer registration information to create a database that we will use to efficiently conduct inspections and allocate inspection resources. With regard to “unexpected visits,” section 704 of the FFDCA (21 U.S.C. 374) authorizes FDA inspections without advance notice and FDA's practice of making such inspections precedes this rule and is independent of whether registration is required.

(Comment 48) One comment expressed concern that information submitted to register facilities would be subject to the Federal Freedom of Information Act (5 U.S.C. 552), and that public release of this information could result in a decrease of security at the producer sites. The comment stated that FDA has other means at its disposal to learn the site information needed to administer this program and still respect the need for security at the producer sites.

(Response) FDA recognizes that this information may be subject to disclosure under FOIA, unless there is statutory authority there or elsewhere that protects it. However, we disagree that the risk of such disclosure outweighs the public health benefits of collecting this information. As stated previously, registration will facilitate FDA's identification of egg producers for inspection and compliance purposes. We will use the producer registration information to create a database that we will use to efficiently conduct inspections and allocate inspection resources.

L. Comments on “Enforcement and Compliance” (Proposed and Final § 118.12)

There were no comments on this section.

M. Comments on Request for Comments as to Whether FDA Should Mandate Special Requirements for Food Establishments That Specifically Serve Highly Susceptible Populations

(Comment 49) We received a number of responses to our request in the proposed rule for comments on whether the current FDA Food Code system (under which states may adopt and implement provisions of the FDA Food Code) is adequate to protect highly susceptible populations from salmonellosis, or whether instead we should establish mandatory Federal standards for food establishments that serve eggs to highly susceptible populations, such as the elderly. Several of these comments supported the Federal codification of the egg-related Food Code provisions for food establishments specifically serving highly susceptible populations, and one comment opposed codification.

One comment supporting codification stated that egg producers do not have full control or responsibility for egg safety, and that food establishments and consumers must share in the responsibility for egg safety. The comment opposed to setting Federal standards stated that the egg safety goal cannot be achieved through mandatory Federal requirements at the food establishment level. The comment recommended continuing mandatory on-farm efforts while continuing educational efforts at retail and consumer levels.

(Response) FDA agrees that food establishments that specifically serve highly susceptible populations can play an important role in egg safety As we discussed in section I.H., a majority of states and territories have adopted into their own retail food codes the relevant egg-associated provisions of the FDA Food Code (sections 3-202.11(C), 3-202.13, 3-202.14(A), and 3-801.11(B)(1) and (B)(2), (C)(2), (E), and (F)(1) and (F)(2) of FDA's 2005 Food Code (see discussion under section I.H of this document regarding the changes made from the 2001 Food Code)). In addition, other state, local, Federal, or voluntary standards applicable to these facilities may have similar egg safety provisions, although we were not able to identify or quantify all such standards. We agree with the comment that encouraged us to continue education efforts at the retail and consumer levels. We also agree that codification of the FDA Food Code provisions is not a necessary exercise of our authority. Instead, we have determined that we will continue to encourage states to adopt the relevant provisions of the FDA Food Code.

(Comment 50) One comment suggested that we make mandatory those parts of the Food Code related to the pooling of eggs in all institutions, including but not limited to those serving specifically at-risk populations in section 3-8 of the Food Code. The comment stated that many of the large outbreaks have been related to commercial or government institutions that misuse eggs, especially when they break and pool large numbers of eggs. The comment stated that even if the eggs are delivered SE-free, the hand breaking and pooling of eggs can result in a contaminated pool due to inadequate hand washing, unclean utensils, temperature abuse during the breaking process and cross-contamination from other raw foods. The comment also stated that the FDA Food Code should be modified to incorporate a requirement that pasteurized egg products be substituted for shell eggs if the eggs are to be pooled, as a model for States to follow.

(Response) FDA has determined that the relevant egg safety provisions of the Food Code should not be mandatory, for the reasons discussed in the preceding response, including those provisions related to the pooling of eggs.

The comment concerning modification of the FDA Food Code is beyond the scope of this rule.

IV. Legal Authority

As outlined in section II.B of this document, after considering comments received in response to the proposal, FDA made changes in the final rule, including the addition of some requirements. The proposed rule contained an explanation of its legal basis under authorities in sections 311, 361, and 368 of the PHS Act (42 U.S.C. 243, 264, and 271) and sections 402(a)(4) and 701(a) of the FFDCA (21 U.S.C. 342(a)(4) and 371(a)). The PHS Act authorizes the Secretary to make and enforce such regulations as “are necessary to prevent the introduction, transmission, or spread of communicable diseases from foreign countries into the States * * * or from one State * * * into any other State” (section 361(a) of the PHS Act). This authority has been delegated to the Commissioner of Food and Drugs. Under section 402(a)(4) of the FFDCA, a food is adulterated if it is prepared, packed, or held under insanitary conditions whereby it may have been contaminated with filth or rendered injurious to health. Under section 701(a) of the FFDCA, FDA is authorized to issue regulations for the efficient enforcement of the FFDCA. These authorities, as well as others specified in the following paragraphs, support the new requirements in the final rule.

Section 118.4(e) requires that persons who transport or hold shell eggs for shell egg processing or egg products facilities must comply with refrigeration requirements. It is well documented that shell eggs may contain

Salmonella,

including transovarian transmitted SE, which can result in serious, life-threatening illness. Temperature abuse of shell eggs, such as by failing to refrigerate eggs as required by the rule, can lead to the multiplication of SE in shell eggs, and thus, increase the likelihood of illness if the eggs are not thoroughly cooked. The refrigeration requirement in § 118.4(e) prohibits food from being held under insanitary conditions and allows for the efficient enforcement of the FFDCA (21 U.S.C. 342(a)(4) and 371(a)). Further, this requirement is necessary to prevent the spread of communicable disease from one state into another state. (42 U.S.C. 264).

Section 118.10 requires that egg producers have written SE prevention plans and maintain records documenting compliance, as well as records of review and modification to the plan and any corrective actions taken. Through records maintenance and review, an egg producer can, over time, develop a comprehensive picture of its prevention measures and identify shortcomings or potential shortcomings. A written plan and records documenting implementation of that plan are necessary for producers to ensure that they have effectively and consistently implemented the plan. For example, without records documenting environmental sampling procedures, a producer cannot ensure that the environment was sampled using a plan appropriate to the poultry house layout.

Similarly, records maintenance and access provide FDA with the opportunity to oversee, in a comprehensive way, the implementation of the producer's SE prevention plan, thereby preventing SE contamination of eggs. SE prevention measures may be quite different among farms, given different facility design and size, and yet be equally effective in preventing SE contamination. Knowledge of the specific prevention measures taken on a farm, as specified in an SE prevention plan, will assist FDA to assess compliance with the prevention measures. In addition, reviewing records is the best mechanism for FDA to use to determine whether preventive measures have been implemented over a period of time. Because the preventive measures are essential to the production of safe eggs as a matter of design, the statutory scheme is benefited by agency access to records that demonstrate that these measures are being systematically applied.

By requiring records, we will be able to ensure that producers follow the SE prevention measures so that eggs are prepared, packed and held under sanitary conditions (21 U.S.C. 342(a)(4) and 371(a)) and in a manner designed to prevent the spread of communicable disease via SE-contaminated eggs (42 U.S.C. 264).

Section 118.11 requires registration by egg producers who must comply with either all of the SE prevention measures or only with the refrigeration requirements. It is essential that we know, via registration, certain information about egg producers, such as whether a producer has 3,000 or more laying hens at a particular farm, so that we can identify and inspect those farms subject to the rule. Inspection is necessary to ensure that shell eggs are being produced in compliance with SE prevention measures, thereby reducing the likelihood of foodborne illness. Therefore, the registration requirement is necessary to prevent the spread of communicable disease from one state into another state. (42 U.S.C. 264).

Section 118.6(f) requires that for diverted eggs, the pallet, case, or other shipping container must be labeled and all documents accompanying the shipment must contain the specified statement to indicate that the eggs must be treated to destroy SE. This requirement is supported by sections 201(n), 403(a)(1), and 701(a) of the FFDCA (21 U.S.C. 321(n), 343(a)(1), and 371(a)) and sections 311, 361, and 361 of the PHS Act. Under section 403(a)(1) of the FFDCA, a food is misbranded if its labeling is false or misleading in any particular. Section 201(n) of the FFDCA provides that in determining whether labeling is misleading, the agency shall take into account not only representations made about the product, but also the extent to which the labeling fails to reveal facts that are material in light of such representations made or suggested in the labeling or material with respect to consequences that may result from use of the product under conditions of use prescribed in the labeling or under customary or usual conditions of use. FDA previously has relied on these authorities when it required label statements on shell eggs not processed to destroy all viable

Salmonella

(65 FR 76092, December 5, 2000).

The rule requires eggs to be diverted in certain circumstances, including after a positive egg test, to ensure that SE will

be destroyed before the eggs are consumed. Without treatment, these eggs would present the greatest risk of causing SE illnesses. As discussed in section V of this document, the eggs that must be diverted to a treatment are worth less than eggs that may be used for the table egg market. This creates an economic incentive to send the eggs to the table egg market. Further, without labeling, a purchaser might not know that particular eggs are subject to the diversion requirement. Therefore, the agency concludes that information that the eggs must be treated to destroy SE is material information that must be provided on the shipping container and accompanying documentation and that the requirement is necessary to prevent the spread of communicable disease from one state into another state. (42 U.S.C. 264).

As explained in the proposal, activities that are intrastate in character, such as the production and final sale of shell eggs to an institution for ultimate consumption by a consumer within one State, are subject to regulation under section 361 of the PHS Act (

State of Louisiana

v.

Mathews,

427 F. Supp. 174, 176 (E.D.La. 1977)). The proposed rule explained FDA's reasoning for tentatively determining that the SE prevention measures in this rule must apply to producers of shell eggs who sell their eggs intrastate, other than directly to consumers. For the reasons discussed therein, we are making that determination final.

V. Analysis of Economic Impacts—Final Regulatory Impact Analysis

A.

Introduction

FDA has examined the impacts of the final rule under Executive Order 12866, the Regulatory Flexibility Act (5 U.S.C. 601-612), and the Unfunded Mandates Reform Act of 1995 (Pub. L. 104-4). Executive Order 12866 directs agencies to assess all costs and benefits of available regulatory alternatives and, when regulation is necessary, to select regulatory approaches that maximize net benefits (including potential economic, environmental, public health and safety, and other advantages; distributive impacts; and equity). The agency believes that this final rule is an “economically significant” regulatory action as defined by Section 3(f)(1) of the Executive Order.

The Regulatory Flexibility Act requires agencies to analyze regulatory options that would minimize any significant impact of a rule on small entities. Using the Small Business Administration (SBA) definitions of small for chicken and egg producers, FDA estimates that more than 99 percent of all egg farms are small. Though more than 45,000 farms with less than 3,000 layers are exempt from all provisions of the rule, the agency certifies that the rule will have a significant economic impact on a substantial number of small entities. This is discussed further in section VI of this document.

Section 202(a) of the Unfunded Mandates Reform Act of 1995 requires that agencies prepare a written statement, which includes an assessment of anticipated costs and benefits, before finalizing “any rule that includes any Federal mandate that may result in the expenditure by State, local, and tribal governments, in the aggregate, or by the private sector, of $100,000,000 or more (adjusted annually for inflation) in any one year.” The current threshold after adjustment for inflation is $130 million, using the most current (2007) Implicit Price Deflator for the Gross Domestic Product. FDA expects this final rule to result in 1-year expenditures that would meet or exceed this amount. This is discussed further in section VII of this document.

B.

Need for Regulation

Private markets operating within the framework of the legal system promote the health and safety of consumers. Limitations of both the marketplace and the legal system, however, can result in inadequate control of some health and safety hazards, and reduce societal welfare.

In a perfectly competitive market in which consumers and producers both have sufficient information, the optimal level of production of eggs will be provided at an optimal level of safety. In the egg market, however, consumers and producers do not have sufficient information on the SE status of particular eggs. In the case of SE-contaminated eggs, although farmers and producers do have an incentive to put safety programs into place, the lack of awareness and information about the risk suggests that an inefficiently high demand exists for eggs that are produced without using adequate measures to prevent SE.

2

Because the demand for specific eggs is not sufficiently affected by safety considerations, the farmer's incentive to invest in safety measures is diminished. Consequently, the market does not provide the incentives necessary for optimal egg safety.

2

For example, although many consumers may be generally aware of the association between shell eggs and SE, they may not know that a few common methods of preparing eggs for consumption will not eliminate SE in a contaminated egg.

With sufficient information for consumers and producers, a legal system that awards compensation for harm done due to SE-contaminated eggs has the potential to remedy market imperfections by providing producers with incentives to provide the level of safety that is best for society. The legal system does not ensure the optimum level of shell egg safety because consumers who become ill due to SE contamination often do not know the reason for, or source of, their illness. Even in cases where consumers are aware that their illness was contracted from eggs, imperfect information makes it difficult to determine who is ultimately responsible for their illness, since the particular source of the SE contamination of the eggs is not known in many circumstances.

In sum, the imperfect information about the risk associated with SE from particular shell eggs means that neither the legal system nor the marketplace may be able to provide adequate economic incentives for the production of eggs sufficiently free of SE contamination. The Government may therefore be able to improve social welfare through targeted regulation. In what follows, we will look at the costs and benefits of the provisions in the rule and comments addressing the benefits and costs of options presented in the proposed rule. We will also look at the costs and benefits of other measures to control SE that we considered, but did not include in this final rule.

C.

Comments on the Preliminary Regulatory Impact Analysis in the Proposed Rule and Responses

(Comment 51) One comment agreed that FDA should exempt small producers generally from the final rule, but suggested that the proposed testing and diversion requirements should apply to all egg producers, regardless of size. The comment argued that testing of the environment and shell eggs provides verification that on-farm sanitation programs are effective in controlling SE and allows for preventive measures including diversion if a positive test occurs, which could prevent illnesses and outbreaks. The comment suggested that imposing testing and diversion requirements on small producers would limit the burden on these small businesses without reducing the public health benefit from the final regulation.

(Response) Some benefits would be derived by requiring farms with less than 3,000 layers to divert potentially positive eggs upon both a positive environmental and a positive egg test.

However, the cost per case averted on farms with less than 3,000 layers, producing less than 1 percent of the shell eggs on the market (accounting for 300 to 1,000 SE-related illnesses per year and less than 1 death per year), is approximately $205,000 per case averted, which would not be a cost-effective public health intervention on over 45,000 very small egg farms.

(Comment 52) One comment noted that, over the last several years, numerous shell egg production facilities in the United States were built to produce eggs only for processing into egg products; these facilities may divert eggs for sale as table eggs when market conditions or seasonal production patterns warrant. The comment stated that this diversion is done when demand for egg products is weak and the producer can avoid or minimize potential economic loss by moving temporary surpluses to the table egg market. The comment stated that, although under the proposed rule producers whose entire production will be processed into egg products need comply only with the refrigeration requirements for on-farm storage, these producers who may divert their eggs to the table egg market must comply with all of the egg production requirements when any part of their production is not processed into egg products or does not receive a treatment that achieves at least a 5-log destruction of SE. The comment stated that, while many firms that produce shell eggs for use primarily in the manufacture of egg products now have extensive on-farm programs to ensure the safety of eggs and egg products, some of these producers will need to impose additional food safety measures at the production site in order to be able to continue to occasionally divert eggs to the table egg market. The comment questions whether the agency considered these expenditures in determining total costs of the proposed rule on the egg industry.

(Response) Those farms that produce only a portion of their eggs for sale on the table egg market have been covered within the scope of this rule and their costs are included in the costs and the benefits analysis of the final rule.

(Comment 53) One comment states that the requirement that eggs be refrigerated at a temperature of no greater than 45 °F within 36 hours of laying is not realistic. The comment recommended instead that the rule require that eggs held at the farm be refrigerated at a temperature no greater than 55 degrees, provided the eggs are not to be stored on the farm for more than 4 days. The comment states that eggs are generally held in on-farm coolers for a relatively short period of time; that there is evidence that any low level of SE within a naturally infected egg will not undergo significant multiplication until the albumen begins to degrade; and that, even at room temperature, significant growth may take several weeks. The comment stated that the cost involved in remodeling and operating on-farm coolers to maintain a 45-degree ambient temperature, rather than a 55-degree ambient temperature, would not show a reasonable cost/benefit ratio.

(Response) Not all farms will need to remodel their on farm coolers to maintain a 45-degree ambient temperature. However, many will, and the costs associated with that remodeling are significant. In the analysis detailed in section V.F of this document, FDA estimates annualized costs for farms that build cooling facilities from scratch, remodel existing cooling facilities, use extra power to reduce temperature, use refrigerated shipping, and use refrigerated preproduction storage, to be $20.1 million using a 7 percent discount rate and $16.4 million using a 3 percent discount rate. Using the 2005 FSIS risk assessment (Ref. 22), FDA estimated that the refrigeration at 45 degrees within 36 hours of lay through the preproduction stage, in the absence of the other provisions in the final rule, would reduce the number of annual SE related illnesses by nearly 45,000. With all provisions in the final rule fully implemented, refrigeration would reduce the number of SE related illnesses by nearly 29,000. Including all costs of egg-related SE illnesses (i.e., both mild cases and the less frequent though more severe ones including hospitalization, chronic arthritis, or even death), FDA estimated the average cost of an SE illness to be $17,900. This provision, when implemented with the rest of the final rule, is estimated to provide nearly $520 million in benefits annually and nearly $500 million in annual net benefits.

(Comment 54) One comment stated that, for environmental testing, consideration should be given to the sampling of a given proportion of available sites as opposed to a given number of samples regardless of the size of the flock or the number of houses. The comment stated that a farm may have a single age group in more than one house.

(Response) This comment reflects a misunderstanding of the proposal. Sampling is performed on a per house basis. Section 118.7(a) requires that an environmental test must be done for each poultry house in accordance with § 118.5(a) and (b). Within each poultry house, you must sample the environment using a sampling plan appropriate to the poultry house layout. We agree that sites/houses are the appropriate sampling location. Costs and benefits of environme

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