 and the tonnage of carcass meat exported from the UK were derived from UK Custom and Excise Data (9).
We included in our analysis all countries covered by the EU surveillance network. Because exposure was expressed as a total amount rather than per capita, we based the analysis on number of vCJD cases rather than rates. We plotted the incidence of vCJD (number of cases) by country against the following factors: 1) number of cases of indigenous BSE, 2) number of live bovines imported from the United Kingdom from 1980 to 1990, and 3) tonnage of carcass meat imported from the United Kingdom from 1980 to 1996. For the last 2 plots, we used logarithmic scales to improve visualization of the data.
We have included carcass meat data until 1996, when all UK bovine imports were banned by the EU. However, for live bovine imports we limited our analysis to the period 1980–1990. In 1990 the EU restricted live bovine exports from the UK to animals <6 months of age and required that the importing country must ensure that any imported cattle from the UK were slaughtered at <6 months of age (10). For the correlation analyses, we included only the non-UK vCJD patients who are thought likely to have acquired infection outside the UK. A factor likely to be important for BSE exposure is the temporal distribution of UK exports. The number of BSE-infected cattle entering the human food supply is estimated to have peaked in the UK around 1989 (7), although with respect to exports, peak exposure may have been later, around 1992–1993. For example, 85% of Germany’s imports of UK carcass meat between 1980 and 1990 were before 1988. In contrast, 70% of the livestock imports to the Netherlands were from 1987 through 1990. To account for this fact, we weighted the number of live bovines and the carcass meat tonnage imported each year by the size of the UK BSE epizootic that year (reported clinical cases) and normalized the data by the maximum number of BSE cases detected in a year during the epizootic. Nonparametric Spearman rank correlation coefficients (rs) were calculated to evaluate whether evidence of a correlation between exposure and outcome existed.
Figure 1 shows a scatter plot of the number of cases of indigenous BSE in non-UK countries and the number of non-UK vCJD cases per country. Although the confidence intervals (CIs) are wide, evidence of a correlation between these 2 variables (rs 0.70, 95% CI 0.37–0.87, p = 0.001) exists in the countries belonging to the EU network (Table 2). When we included in our analysis Japan and Saudi Arabia, the only 2 countries outside the EU network in which vCJD cases have been detected, the correlation coefficient fell to 0.55 (95% CI 0.17–0.79, p = 0.008) (Table 2). Non-UK vCJD cases in EU network countries were also correlated with the number of live bovine imports from the UK (Figure 2; rs 0.73, 95% CI 0.42–0.89, p<0.001) and the amount of carcass meat imported from the UK (Figure 3; rs 0.75, 95% CI 0.45–0.89, p<0.001). Including Japan and Saudi Arabia produced similar results (live bovines rs 0.65, 95% CI 0.31–0.84; carcass meat rs 0.73, 95% CI 0.45–0.88) (Table 2).
We evaluated whether our findings were dependent on the data from France, which has the largest number of non-UK cases, by repeating the analyses excluding France. Evidence remained that all 3 exposures were correlated with vCJD incidence (Table 2). We also repeated the analysis including the 6 cases detected outside the UK but thought to have been acquired in the UK. The inclusion of these cases resulted in a reduction in all 3 correlation coefficients (Table 2).
Live bovine and carcass meat imports from the United Kingdom during the 1980s and the first half of the 1990s correlate with the numbers of vCJD cases in countries outside the UK. This finding suggests that live bovine and/or carcass meat imports from the UK may have been an important source of exposure in at least some of the countries in which vCJD has been detected. These results are consistent with an analysis of data from France, which suggested that UK bovine imports were