rican, and possibly the Japanese patient, may have been infected during periods of residence in the UK, but most cases (28 of 34) occurring outside the UK were in persons who had never visited the UK. Although vCJD cases have occurred in countries with very low incidence of BSE, no cases have been reported in countries with higher incidence of BSE, such as Switzerland (460 reported cases of BSE) and Germany (395 cases) (5). This fact raises questions as to the source of infection in the vCJD cases outside the UK. Were the patients exposed to indigenous cases of BSE or to infected bovine material imported from the UK? An analysis of infection risk in France suggests that the most likely source of vCJD in that country is imported infected material from the United Kingdom (6). In the Republic of Ireland, the transmission of BSE to humans was estimated to be equally likely from indigenous BSE or from UK imports (7). Given the apparently weak association between the occurrence of indigenous BSE and vCJD in some countries, we studied the occurrence of vCJD cases outside the UK in relation to the level of imported bovines and bovine products from the UK during the 1980s and the first half of the 1990s.
A European Union (EU) surveillance network, established in 1993, ensures prospective surveillance for CJD by using standard methods (8) in 18 European countries and the United States, Canada, Israel, and Australia. By August 24, 2006, 32 cases of vCJD had been identified in these countries (excluding the UK) (Table 1). Two more cases had been identified in countries outside the surveillance network, Japan and Saudi Arabia. Case-patients in Canada (n = 1), the United States (n = 2), Ireland (n = 2), and possibly Japan (n = 1) were considered as likely to have been infected during periods of residence in the UK.
Data on indigenous BSE cases detected by both passive and active surveillance were obtained from the World Organization for Animal Health webpage (www.oie.int/eng/info/en_esbmonde.htm) (5). The number of live cattle 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