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, 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 (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 during distribution and handling, traceback investigations from 1996 to 1999, and use of pasteurized eggs. However, these measures were not implemented in 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 (), 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.