Egg quality assurance programs and egg-associated salmonella enteritidis infections, United States.
A Salmonella enterica Salmonella enterica is a rod shaped, flagellated, Gram-negative bacterium, and a member of the genus Salmonella. Serovars
S. enterica has an extraordinarily large number of serovars serovar Enteritidis epidemic in the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. began in 1978, spread to much of the country in the following decade, and began declining in 1996. We examined correlations between annual changes in S. Enteritidis incidence in humans and introductions of egg quality assurance programs (EQAPs) in some states to reduce S. Enteritidis contamination of eggs. Before EQAPs, 62% of the changes in S. Enteritidis incidence were higher than the baseline for each state. After EQAPs, 73%-84% of the changes were below the baseline. Regression analysis In statistics, a mathematical method of modeling the relationships among three or more variables. It is used to predict the value of one variable given the values of the others. For example, a model might estimate sales based on age and gender. showed that a 1% increase in the number of eggs produced under an EQAP was associated with a 0.14% decrease in S. Enteritidis incidence (p < 0.05). These data indicate that EQAPs probably played a major role in reducing S. Enteritidis illness in these states.
********** An epidemic of infections caused by Salmonella enterica serovar Enteritidis in the United States began in New England New England, name applied to the region comprising six states of the NE United States—Maine, New Hampshire, Vermont, Massachusetts, Rhode Island, and Connecticut. The region is thought to have been so named by Capt. in 1978 and spread to much of the rest of the country in the next decade. Though the spread has declined in all regions since 1996 (Figure 1), the number and incidence of S. Enteritidis infections have not shown substantial decline since 1999 (1). Since grade A shell eggs have been implicated im·pli·cate
tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates
1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot.
2. as a major source of S. Enteritidis infections in humans in the United States (2), interventions have been introduced to reduce S. Enteritidis infection in poultry and eggs and the resulting illness in humans (3-10). These interventions include State Egg Quality Assurance Programs (EQAPs), which are voluntary programs that are based on Hazard Analysis A hazard analysis is a process used to characterize the elements of risk. The results of a hazard analysis is the identification of unacceptable risks and the selection of means of controlling or eliminating them. Critical Control Point (HACCP HACCP
hazard analysis critical control points. ) principles and designed around production, management, and monitoring practices to mitigate risk for S. Enteritidis contamination of eggs (3,11,12). Motivations for egg producers to adopt an EQAP may include scientific, public health, public relations public relations, activities and policies used to create public interest in a person, idea, product, institution, or business establishment. By its nature, public relations is devoted to serving particular interests by presenting them to the public in the most , or marketing reasons (13). Initially, producers enrolled voluntarily into state- or industry-sponsored EQAPs. However, in some states, commercial egg producers are required to participate in EQAPs because egg processors, food commodity brokers, insurance companies, and integrated commercial companies are increasingly demanding producer participation in EQAPs as a condition of egg sales (12).
[FIGURE 1 OMITTED]
Research to date has focused on verifying the role and effectiveness of EQAPs in mitigating S. Enteritidis in layer flocks and eggs (4,5,13). Effectiveness might be indicated by reductions of S. Enteritidis prevalence in layer flocks (11,14,15), farm environments (11,16), and eggs produced by infected in·fect
tr.v. in·fect·ed, in·fect·ing, in·fects
1. To contaminate with a pathogenic microorganism or agent.
2. To communicate a pathogen or disease to.
3. To invade and produce infection in. flocks (5) after introducing EQAPs. Reported reductions in S. Enteritidis rates in markets with EQAPs have been used to explain the effectiveness of EQAPS in reducing S. Enteritidis illness in humans (2,3,11,16,17). Some evidence shows that interventions that reduce the storage time of shell eggs, internal or ambient temperature Outside temperature at any given altitude, preferably expressed in degrees centigrade. , or prevalence of S. Enteritidis-positive flocks or that increase diversion of eggs from S. Enteritidis-positive flocks to pasteurization pasteurization (păs'chrĭzā`shən, -rīzā`shən), partial sterilization of liquids such as milk, orange juice, wine, and beer, as well as cheese, to destroy , may help reduce the incidence of S. Enteritidis in humans (18). However, little is known about the contribution of each intervention to the overall reduction in the number of S. Enteritidis cases. The present study analyzes flock-based EQAPs to assess their actual contribution to the reduction of S. Enteritidis incidence in humans.
Baseline incidence was defined as S. Enteritidis incidence in the year in which an EQAP was adopted in a state or group of states affected by the S. Enteritidis epidemic. We calculated S. Enteritidis incidence for a state or group of states as the number of reported human S. Enteritidis isolates in a year divided by that state's or group of states' population for that year expressed per 100,000 persons. We defined a state affected by the S. Enteritidis epidemic as one for which the S. Enteritidis incidence was >1/100,000 in any year between 1980 and 1999.
States that adopted EQAPs were grouped into state- and industry-sponsored EQAPs. We grouped EQAPs into state-sponsored and industry-sponsored types on the basis of whether the state government was actively involved in third-party monitoring, supervision, provision of technical advice, and procedure of handling houses that are found to be S. Enteritidis positive. In this study, state-sponsored EQAPs were defined as having active state Department of Agriculture and Department of Health involvement in providing technical advice, supervising and monitoring the programs, requiring third-party auditing, testing eggs for contamination with S. Enteritidis if houses were positive, and diverting eggs found to be contaminated contaminated,
v 1. made radioactive by the addition of small quantities of radioactive material.
2. made contaminated by adding infective or radiographic materials.
3. an infective surface or object. with S. Enteritidis to pasteurization and hard cooking. Industry-sponsored EQAPs were defined as lacking state government involvement, recommending but not requiring third-party audits of the program, and recommending immediate extra cleaning of S. Enteritidis--contaminated houses upon depopulation DEPOPULATION. In its most proper signification, is the destruction of the people of a country or place. This word is, however, taken rather in a passive than an active one; we say depopulation, to designate a diminution of inhabitants, arising either from violent causes, or the want of of the houses (19).
We calculated the percentage change in annual S. Enteritidis incidence relative to the baseline (hereafter In the future.
The term hereafter is always used to indicate a future time—to the exclusion of both the past and present—in legal documents, statutes, and other similar papers. referred to as the change in S. Enteritidis incidence):
(1) [DELTA]R[I.sub.it] = [MATHEMATICAL EXPRESSION A group of characters or symbols representing a quantity or an operation. See arithmetic expression. NOT REPRODUCIBLE IN ASCII ASCII or American Standard Code for Information Interchange, a set of codes used to represent letters, numbers, a few symbols, and control characters. Originally designed for teletype operations, it has found wide application in computers. ] where, I stands for SE incidence; [DELTA]RI for change in SE incidence;
i = 1, 2, ..., N for slate; t = -T, ..., -1,0,1, ..., T for time, [t.sub.0] = year of EQAPs introduction
We then divided the change in S. Enteritidis incidence for a given year by the number of years before or after the intervention to get the annualized annualized
Of or relating to a variable that has been mathematically converted to a yearly rate. Inflation and interest rates are generally annualized since it is on this basis that these two variables are ordinarily stated and compared. percentage change in S. Enteritidis incidence (hereafter referred to as the annualized change in S. Enteritidis incidence). We used two methods to examine changes in S. Enteritidis incidence: a simple change-point procedure and regression analysis.
Change-point Analysis Framework
We constructed a graph with a horizontal axis representing time in years and a vertical axis representing S. Enteritidis incidence (Figure 2A). If an intervention is effective, S. Enteritidis incidence should decrease after the baseline year (line b, Figure 2A). If the S. Enteritidis incidence had been increasing before the intervention, a smaller increase in incidence after the baseline would also show evidence of effectiveness (line c, Figure 2A). If the S. Enteritidis incidence had been decreasing before the intervention, we would expect a faster decrease in incidence after the baseline. Similarly, the lack of change in S. Enteritidis incidence observed before, during, and after the intervention would be evidence of lack of effect (line d, Figure 2A), and an increase in S. Enteritidis incidence (line e, Figure 2A) would be evidence that the intervention was associated with an acceleration of the epidemic. The effectiveness of an intervention can further be assessed by using the annualized change in S. Enteritidis incidence (Figure 2B). To show evidence of an intervention's effectiveness, we would expect the annualized change in S. Enteritidis incidence after intervention to be below the baseline rate (dotted line b, Figure 2B) or the preintervention rate (dotted line b compared to a, Figure 2B). A more modest effect after intervention that shows the epidemic continuing to grow at a diminished annualized rate would find the change in incidence above baseline but below the preintervention level (dotted line c compared to a, Figure 2B). An ineffective intervention would result in an annualized change in S. Enteritidis incidence after intervention that is equal to the rate before intervention (dotted line d compared to a, Figure 2B). An annualized change in S. Enteritidis incidence above the preintervention rate (line e compared to a, Figure 2B) would be evidence that the intervention was associated with an acceleration of the epidemic. If changes in S. Enteritidis incidence continued at about the same rate or were sustained for a number of years, the Years, The
the seven decades of Eleanor Pargiter’s life. [Br. Lit.: Benét, 1109]
See : Time annualized change in S. Enteritidis incidence would, in time, trend toward the baseline. We calculated Yates corrected chi-square values to verify whether changes in observations of annualized S. Enteritidis incidence were statistically significant.
[FIGURE 2 OMITTED]
We examined observations of pre-EQAP annualized rates of change in S. Enteritidis incidence for a period of up to 5 years and for a variable period of up to 8 years of post-EQAP observations. The time periods selected were considered to be long enough to include any relevant lag effects and short enough to exclude confounding confounding
when the effects of two, or more, processes on results cannot be separated, the results are said to be confounded, a cause of bias in disease studies.
confounding factor influence of other interventions, such as those that require refrigerating re·frig·er·ate
tr.v. re·frig·er·at·ed, re·frig·er·at·ing, re·frig·er·ates
1. To cool or chill (a substance).
2. To preserve (food) by chilling. eggs. To analyze the timing of the decrease in S. Enteritidis incidence, we grouped states on the basis of duration of postintervention follow-up and then type of EQAP and compared the annualized changes in S. Enteritidis incidence for each of the 5 years before adopting EQAPs and up to 5 years after adopting EQAPs. For example, states that adopted EQAPs in 1996 had 3 years of common experience with the intervention from 1996 to 1999 and formed a group based on this common length of time. The annualized changes in S. Enteritidis provided a measure for comparing incidence of S. Enteritidis before, during, and after EQAP adoption.
We also examined the percentage change in S. Enteritidis incidence by using a pooled regression model. The pooling method can be used to combine cross-section and time-series data. This technique allows for the error terms to have equal variance on the chosen values of the explanatory variables within a state, but unequal variance between states (20-25), which results in efficient and unbiased parameter estimates. We estimated a pooled regression equation Regression equation
An equation that describes the average relationship between a dependent variable and a set of explanatory variables. for five cross-sectional states (Connecticut, Louisiana, Indiana, Pennsylvania Indiana is a borough in Indiana County, Pennsylvania, United States, part of the Pittsburgh DMA. The population was 14,895 at the 2000 census. It is the county seat of Indiana County. , and California) for 5 years post-EQAP by using SHAZAM SHAZAM Solomon, Hercules, Atlas, Zeus, Achilles, Mercury (Captain Marvel's Elders)
SHAZAM Selena, Hippolyta, Ariadne, Zephyrus, Aurora, and Minerva (Captain Marvel comics, deities that supported Mary Marvel) (20). The pooled regression equation was:
(2) [Y.sub.it] = [X.sub.it] [beta] + [[epsilon].sub.it], where i = 1, 2, ..., N and stands for state; t = 1, ..., T for time, Y for the percentage change in SE incidence; X for explanatory variables; [beta] for kX1 column vector In linear algebra, a column vector is an m × 1 matrix, i.e. a matrix consisting of a single column of elements.
We included Louisiana in the regression model, although it was unaffected by the epidemic, to improve the degrees of freedom for the model. Only four of the states that were affected by the S. Enteritidis epidemic had 5 years of post-EQAP experience. Also, we included a dummy variable This article is not about "dummy variables" as that term is usually understood in mathematics. See free variables and bound variables.
In regression analysis, a dummy variable in the model to control for states that were not affected by the S. Enteritidis epidemic.
Independent variables (and types) were percentage of eggs produced in participating farms (continuous), type of EQAP (binary: state- or industry-sponsored: yes/no), number of United States Department of Agriculture United States Department of Agriculture (USDA),
n.pr established in 1862, USDA is responsible for the safety of meat, poultry, and egg products. It conducts ongoing research in areas from human nutrition to new crop technologies and also helps ensure open (USDA USDA,
n.pr See United States Department of Agriculture. ) S. Enteritidis outbreak traceback investigations (continuous), proportion of population at high risk for S. Enteritidis (children <5 years and seniors >65 years) (continuous), and whether the state was in the northeast geographic region (Connecticut, Pennsylvania, New York New York, state, United States
New York, Middle Atlantic state of the United States. It is bordered by Vermont, Massachusetts, Connecticut, and the Atlantic Ocean (E), New Jersey and Pennsylvania (S), Lakes Erie and Ontario and the Canadian province of ) (binary: yes/no). The proportion of eggs produced under EQAPs by state and year was the index to measure participation in EQAPs.
We sent a detailed questionnaire to state veterinarians Veterinarians and veterinary surgeons (vets) are medical professionals who operate exclusively on animals. Well-known and notable veterinarians include:
All parties that have an interest, financial or otherwise, in a firm-stockholders, creditors, bondholders, employees, customers, management, the community, and the government. (e.g., state departments of agriculture, laboratory workers, and egg industry officials) in state S. Enteritidis mitigation efforts.
The questionnaire collected data on whether egg producers in the state had adopted an EQAP, and if so, the type of EQAP to which most producers in the state adhered (e.g., industry-or state-sponsored), year of EQAP initiation, estimated proportion of total commercial layer-flock participation in the EQAP by year, and elements of the EQAP to which participants were required to adhere. The annual number of S. Enteritidis cases was obtained from reports by state and local health departments to the National Salmonella salmonella
Any of the rod-shaped, gram-negative, non-oxygen-requiring bacteria that make up the genus Salmonella. Their main habitat is the intestinal tract of humans and other animals. Surveillance System (1). Estimates of the annual population data for states were obtained from the Bureau of the Census Noun 1. Bureau of the Census - the bureau of the Commerce Department responsible for taking the census; provides demographic information and analyses about the population of the United States
Census Bureau of the U.S. Department of Commerce (26).
The annual numbers of eggs produced by state from 1972 to 1999 were obtained from USDA's National Agricultural Statistics Service (NASS Nass (năs), river, 236 mi (380 km) long, rising in the Coast Mts., W British Columbia, Canada, and flowing SW to Portland Inlet of the Pacific Ocean. It is navigable for 25 mi (40 km) and has valuable salmon fisheries. ) (27). To calculate the proportion of eggs produced under an EQAP for each state, we assumed no difference in egg production per layer between layers raised under an EQAP and those raised under no EQAP. We then calculated the proportion of eggs produced under each EQAP as a product of the proportion of total layer flocks that participated in the EQAP and the annual total number of eggs produced by each state. This calculation may overestimate o·ver·es·ti·mate
tr.v. o·ver·es·ti·mat·ed, o·ver·es·ti·mat·ing, o·ver·es·ti·mates
1. To estimate too highly.
2. To esteem too greatly. the annual total number of eggs produced for human consumption. The category "table eggs" would provide a closer estimate of eggs produced for human consumption. However, due to confidentiality concerns, NASS does not publish complete information on table egg production.
To estimate a proxy for the proportion of the state's population at high risk for S. Enteritidis, we used the resident population <5 years of age and >65 years of age and total resident population. Data for estimates of the resident population by age and state for 1989-1999 were obtained from the U.S. Census Bureau Noun 1. Census Bureau - the bureau of the Commerce Department responsible for taking the census; provides demographic information and analyses about the population of the United States
Bureau of the Census (26). We obtained the number of successful S. Enteritidis outbreak traceback investigations (investigation to establish origin of S. Enteritidis-contaminated eggs) by state from USDA's S. Enteritidis Task Force Status Reports for 1990 to 1993 (8). Similar information was not available for tracebacks from 1996 to 1999, when the Food and Drug Administration was responsible for tracebacks. The typical procedure when a traceback leads to farms is for the regulatory body to take environmental samples of manure manure, term used in the United States to refer to excreta of animals, with or without added bedding; also called barnyard manure. In other countries the term often refers to any material used to fertilize the soil. areas, egg belts and escalators, fans, and feed. If the environment tests positive for S. Enteritidis, the farmer can either divert the eggs to pasteurization or hard cooking for the lifetime of the flock, divert the eggs until they test negative for S. Enteritidis, or depopulate de·pop·u·late
tr.v. de·pop·u·lat·ed, de·pop·u·lat·ing, de·pop·u·lates
To reduce sharply the population of, as by disease, war, or forcible relocation. the flock.
Egg Production Under EQAP
We received analyzable results from 41 states. No response was received from Idaho, Maine, Mississippi, New Jersey, New Mexico New Mexico, state in the SW United States. At its northwestern corner are the so-called Four Corners, where Colorado, New Mexico, Arizona, and Utah meet at right angles; New Mexico is also bordered by Oklahoma (NE), Texas (E, S), and Mexico (S). , Virginia, Washington, Wisconsin Washington is the name of some places in the U.S. state of Wisconsin:
Area, 24,181 sq mi (62,629 sq km). Pop. . These states accounted for [approximately equal to] 9% of U.S. shell egg production from 1989 to 1999. State officials in 15 of the 41 states reported that egg producers in their respective states had adopted one of two kinds of EQAPs from 1989 to 1999. Ten (Connecticut, Pennsylvania, California, South Carolina South Carolina, state of the SE United States. It is bordered by North Carolina (N), the Atlantic Ocean (SE), and Georgia (SW). Facts and Figures
Area, 31,055 sq mi (80,432 sq km). Pop. (2000) 4,012,012, a 15. , Maryland, Ohio, Michigan, Utah, New York, Alabama) adopted state-sponsored EQAPs, and 5 (Louisiana, Indiana, Oregon, Florida, Georgia) adopted industry-sponsored EQAPs. Eleven of the 41 responding states were affected by the S. Enteritidis epidemic, of which 9 had state-sponsored programs and 2 had industry-sponsored programs. The proportion of eggs produced under EQAPs among the 41 responding states increased from 1% in 1989 to 46% in 1999, and eggs produced under EQAPs among the 11 states that had EQAPs and were affected by the S. Enteritidis epidemic increased from 3% in 1989 to 79% in 1999 (Table 1).
We calculated 55 preintervention and 40 postintervention annualized changes in S. Enteritidis incidence for 11 states that were affected by the S. Enteritidis epidemic and adopted EQAPs (Table 2). Before adopting any EQAP (state- or industry-sponsored), S. Enteritidis incidence relative to the baseline was higher in 62% of the observations and lower in 38% of the observations (Figure 3). After EQAPs were introduced, S. Enteritidis incidence increased relative to the baseline in 28% of the post-EQAP observations and decreased in 73% of the observations, which indicates a significant reduction (Yates-corrected chi-square = 9.61, p = 0.0019).
[FIGURE 3 OMITTED]
In the analysis restricted to the nine affected states that adopted state-sponsored EQAPs, we calculated 45 preintervention and 31 postintervention annualized changes (Table 2). S. Enteritidis incidence was higher than the baseline in 62% of the pre-EQAP observations and lower in 38% of the observations (Figure 4). After the state-sponsored EQAPs were introduced, S. Enteritidis incidence increased relative to the baseline in 16% of the observations and decreased in 84%, which indicates a significant reduction (Yates-corrected chi-square = 14.05, p = 0.00018).
[FIGURE 4 OMITTED]
To analyze the timing of reductions in S. Enteritidis incidence, we defined groups of 11, 7, 6, and 4 states with at least 1 year, 2 years, 3 years, and 5 years of post-EQAP follow-up, respectively. In each group, S. Enteritidis incidence was increasing before adoption of EQAPs and decreased afterwards af·ter·ward also af·ter·wards
At a later time; subsequently.
afterwards or afterward
later [Old English æfterweard]
Adv. 1. . The effect of the intervention was apparent in the first year and was sustained (Figure 5).
[FIGURE 5 OMITTED]
Results of the Regression Model for States that Adopted EQAPs
Descriptive statistics descriptive statistics
see statistics. for variables used in the regression model are presented in Table 3. A 1% increase in the quantity of eggs produced under an EQAP (state- or industry-sponsored) was associated with a 0.14% (p < 0.05) reduction in the change in S. Enteritidis incidence (Table 4). A state-sponsored EQAP was associated with a decrease of 72.25% (p < 0.1) in the change in S. Enteritidis incidence. A 1% increase in the population at high risk for S. Enteritidis was associated with an 8.15% (p < 0.05) increase of the change in S. Enteritidis incidence. An increase of 1 in the number of successful USDA S. Enteritidis outbreak traceback investigations was associated with an increase of 2.82% (p < 0.001) in the change in S. Enteritidis incidence. No significant associations were found for changes in S. Enteritidis incidence and states affected by the S. Enteritidis epidemic or located in the Northeast region.
Discussion and Conclusions
Although a decline in prevalence of S. Enteritidis in layer-flock eggs might indicate effectiveness of EQAPs in mitigating S. Enteritidis (4,6,10,12,16,28), a connection with reductions of S. Enteritidis infections in humans is necessary to indicate effectiveness of the programs in mitigating human illness. Our simple change-point procedure showed a connection between the introduction of EQAPs at the state level and significant reductions in S. Enteritidis incidence in humans. The regression analysis found that increasing the quantity of eggs produced under EQAPs was associated with reducing S. Enteritidis incidence.
Several factors limited this study. Whether an EQAP was introduced at the beginning of the year or at the end of the year might make a difference, and defining a baseline year might introduce error in the analysis. However, data about the month in which EQAPs were introduced were lacking for most states that adopted these programs. Although some EQAPs are similar in that they were designed through close collaboration among states, they vary in practice and motivation, which limits generalizations about all EQAPs, whether state or industry sponsored. We found verifying the exact practices of each EQAP to be difficult because EQAPs range from self-certification programs, like the 5-Star United Egg Producers program (19) practiced in Indiana and Oregon that does not require microbiologic testing for chicks, pullets, layers, and eggs, to the more structured, regulated, rigorous, and costly Pennsylvania Egg Quality Assurance Program (14). Eleven of 15 states with EQAPs reported that they required periodic sampling and testing of layer environments, layers, and eggs for S. Enteritidis, but 4 (Oregon, Louisiana, Indiana, Georgia) did not. All states that required microbiologic testing, except for Florida, involved their state governments in setting up and monitoring their EQAP programs.
We did not study interactions in the regression model because of few data points and degrees of freedom, which limited the robustness of its results. We were more interested in the direction (positive or negative) of the estimate of the percentage of eggs produced under EQAPs than the magnitude. Also, our results were based on unverified respondent estimates of the proportion of eggs produced under EQAPs, information about the type of EQAP, and when the EQAP was instituted. Further, because accurately estimating prevalence of diabetes, cancer, HIV/AIDS HIV/AIDS Human Immunodeficiency Virus/Acquired Immune Deficiency Syndrome , and pregnancy at the state level was difficult, we used the population of children <5 years of age and seniors >65 years of age for each state to represent the population at high risk for S. Enteritidis.
We assumed that eggs produced in a state are applied to meet the consumption needs of that state, and changes in S. Enteritidis incidence within the state would reflect the effect of the state's EQAP, but this assumption may not be accurate. Eggs in the United States are distributed widely across the nation through a dynamic system that makes it difficult to track the source and destination of eggs by state. Although data about the source and destination of eggs and egg products are desirable, they are not currently available (29).
Not all egg producers immediately join EQAPs, and the percentage of eggs produced in a state under an EQAP varies as producers adopt or leave EQAPs. The simple change-point analysis did not account for these variations and assumed that EQAPs were homogeneous within and among states. The regression model allowed EQAPs to be homogeneous within states and heterogeneous among states.
Our model could not estimate unreported cases in a meaningful way, although these cases constitute most cases of salmonellosis salmonellosis (săl'mənĕlō`sĭs), any of a group of infectious diseases caused by intestinal bacteria of the genus Salmonella, (14). The larger proportion of S. Enteritidis cases goes unreported (30). Other factors may have affected S. Enteritidis incidence in humans that we did not account for in this model because of lack of specific data, such as improvements in egg refrigeration refrigeration, process for drawing heat from substances to lower their temperature, often for purposes of preservation. Refrigeration in its modern, portable form also depends on insulating materials that are thin yet effective. during distribution and handling, traceback investigations from 1996 to 1999, and use of pasteurized pas·teur·ize
tr.v. pas·teur·ized, pas·teur·iz·ing, pas·teur·iz·es
To subject (a beverage or other food) to pasteurization.
pas eggs. However, these measures were not implemented in tandem Adv. 1. in tandem - one behind the other; "ride tandem on a bicycle built for two"; "riding horses down the path in tandem"
tandem with the EQAPs within or among states. Therefore, the close temporal association between implementing EQAPs and decreasing rates of S. Enteritidis infection indicate the importance of EQAPs as a control strategy.
The results of our study indicate that flock-based interventions have had a positive effect on health by reducing S. Enteritidis incidence in humans. These data further indicate that EQAPs probably played a major role in reducing S. Enteritidis illness in the United States. Considering that as of 1999, less than half of shell eggs in the United States were produced under EQAPs (Table 1), and that the number of cases and relative rate of S. Enteritidis have not shown significant decline since 1999, adopting EQAPS by producers and states would likely improve the public's health and prevent reemergence of egg-based Salmonella.
Table 1. Eggs produced under EQAPs as a percentage of total egg production, 1989-1999 (a) % of eggs produced under EQAPs United States States with EQAPs affected by Year (N = 41) (b) S. Enteritidis epidemic (N = 11) 1989 1.2 2.5 1990 1.7 2.8 1991 3.6 7.0 1992 5.2 10.5 1993 5.5 10.9 1994 8.6 18.0 1995 10.5 22.2 1996 17.6 38.3 1997 27.0 59.1 1998 34.7 68.8 1999 46.1 78.6 (a) EQAP, Salmonella enterica serovar Enteritidis egg quality assurance programs. (b) Forty-one states responded to the survey. A state affected by the S. Enteritidis epidemic had an S. Enteritidis isolation rate >1/100,000 population in any year from 1980 to 1999. States with EQAPs affected by the S. Enteritidis epidemic were California, Connecticut, Indiana, Maryland, Michigan, New York, Ohio, Oregon, Pennsylvania, South Carolina, and Utah. Table 2. Annualized rates of change of Salmonella enterica serovar Enteritidis incidence before and after adoption of EQAPs in states affected by the epidemic (a,b) With state- or With industry- state- sponsored sponsored S. Enteritidis incidence EQAPs (%) EQAPs (%) Increasing before introduction of EQAPs 34 (62) 28 (62) Decreasing before introduction of EQAPs 21 (38) 17 (38) Increasing after introduction of EQAPs 11 (28) 5 (16) Decreasing after introduction of EQAPs 29 (73) 26 (84) (a) EQAP, egg quality assurance program. This analysis included 11 states that had state- or industry-sponsored EQAPs and 9 states with state-sponsored EQAPs. Departments of agriculture and health provided technical advice, supervision, and monitoring to state-sponsored EQAPs. State-sponsored required auditing by third parties, tested eggs for contamination with S. Enteritidis if layer houses were found to be positive, and diverted eggs found to be contaminated with S. Enteritidis to pasteurization and hard cooking. (b) Percentages may not equal 100% because of rounding. Table 3. Descriptive statistics for variables in the regression model (a) Variable Average SD Rate of change in Salmonella enterica serovar 3.2 44.9 Enteritidis incidence (%) after EQAP adoption % eggs produced under EQAP by states 63.6 29.5 % a state's population at high risk for 20.6 0.5 S. Enteritidis (b) States with state-sponsored EQAP (%) (c) 60 50 States affected by the S. Enteritidis epidemic (%) 20 40 Successful S. Enteritidis outbreak traceback 0.3 1.1 investigations by state per year (d) States in the northeast region of United 40 50 States (D) (e) (a) EQAP, egg quality assurance program; D, dummy variable. (b) Children <5 and seniors >65 as a proxy for population at high risk for S. Enteritidis. (c) Not industry-sponsored EQAP. (d) Number of S. Enteritidis outbreak investigations from United States Department of Agriculture S. Enteritidis Task Force Status Reports for 1990 to 1993. (e) Northeast region includes Connecticut, Pennsylvania, and New York. Table 4. Regression model estimated rates of change in Salmonella enterica serovar Enteriditis incidence associated with unit changes in related variables (a) Change in S. Unit of Enteritidis Explanatory variable change rate (%) p value Intercept (b) -120.65 < 0.01 Eggs produced under EQAP (%) 1 -0.14 < 0.05 State population at high risk for S. 1 -8.15 < 0.01 Enteritidis (%) (c) State had a state-sponsored EQAP (d) Yes -72.25 < 0.1 State was affected by S. Enteritidis Yes -3.60 epidemic (e) Successful S. Enteritidis outbreak Numeral 2.82 < 0.01 traceback investigations by state per year (f) State was in the northeast region Yes 12.36 of the United States (g) (a) EQAP, egg quality assurance program. (b) Intercept term is the baseline case, which represents no eggs produced under EQAAs, zero percent of the population at high risk for S. Enteritidis, no states affected by S. Enteritidis epidemic, no successful outbreak investigations, and all states outside of the northeast region. (c) Children <5 and seniors >65 years. (d) Not industry-sponsored EQAP. (e) A state affected by S. Enteritidis epidemic had an isolation rate >1/100,000 persons from 1980 to 1999. (f) Number of S. Enteritidis outbreak investigations from USDA S. Enteritidis Task Force status reports for 1990 to 1993. (g) Northeast region includes Connecticut, Pennsylvania, and New York.
We thank David Swerdlow for information to begin this research; Mary Evans Patrick for S. Enteritidis data in an accessible form; David Henzler, Maria Moll, and Marshall Deasy III for facilitating a visit to Pennsylvania's EQAP; and all the state public health, veterinary, agricultural, and egg industry officials in the 41 states for participating in this study.
* Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. , Atlanta, Georgia, USA
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Address for correspondence: Gerald A. Mumma, Prevention Effectiveness Branch, Division of Prevention Research and Analytic Methods, Epidemiology Program Office, Centers for Disease Control and Prevention, 1600 Clifton Road Clifton Road is main street in Clifton neighborhood of Saddar Town in Karachi, Sindh, Pakistan.
Its name dates from the British Colonial rule, and its market is posh areas of Karachi. , Mailstop K73, Atlanta, GA 30333, USA; fax: 770-488-8488; email: email@example.com
Dr. Mumma is an economist with the Prevention Effectiveness Branch of the Centers for Disease Control and Prevention. He leads the Prevention Effectiveness Fellowship and conducts food safety economics research.