.................................................................
Estimating the human health risk
from possible BSE infection of
the British sheep ¯ock
N. M. Ferguson, A. C. Ghani, C. A. Donnelly, T. J. Hagenaars
& R. M. Anderson
Department of Infectious Disease Epidemiology, Faculty of Medicine,
Imperial College of Science, Technology and Medicine, St Mary's Campus, Norfolk
Place, London W2 1PG, UK
..............................................................................................................................................
Following the controversial failure of a recent study
1
and the small
numbers of animals yet screened for infection
2
, it remains uncer-
tain whether bovine spongiform encephalopathy (BSE) was trans-
mitted to sheep in the past via feed supplements and whether it is
still present. Well grounded mathematical and statistical models
are therefore essential to integrate the limited and disparate data,
to explore uncertainty, and to de®ne data-collection priorities. We
analysed the implications of different scenarios of BSE spread in
sheep for relative human exposure levels and variant Creutzfeldt±
Jakob disease (vCJD) incidence. Here we show that, if BSE entered
the sheep population and a degree of transmission occurred, then
ongoing public health risks from ovine BSE are likely to be greater
than those from cattle, but that any such risk could be reduced by
up to 90% through additional restrictions on sheep products
entering the food supply. Extending the analysis to consider
absolute risk, we estimate the 95% con®dence interval for
future vCJD mortality to be 50 to 50,000 human deaths consider-
ing exposure to bovine BSE alone, with the upper bound increas-
ing to 150,000 once we include exposure from the worst-case ovine
BSE scenario examined.
The aim of this study was not to evaluate the probability that BSE
has entered the sheep ¯ock, but rather, given the pessimistic
assumption that infection has occurred, to explore its potential
extent and pattern of spread. In this, we used epidemiological
parameter estimates from experimental BSE infections of sheep,
and, where data are unavailable, assumed (given the observed
similarities in BSE and scrapie pathogenesis in sheep) that other
aspects of disease epidemiology resemble those of scrapie. Analyses
were constrained to be consistent with the failure to detect the BSE
agent in a small sample of 180 brains
2
collected between 1996 and
2000 from sheep diagnosed with scrapie (giving an upper bound for
BSE prevalence within apparently scrapie-affected sheep of 2%;
Fig. 1a), and are also broadly consistent with an assessment of
historical exposure of the ovine population to meat and bonemeal
(MBM)
3
.
Key to our analysis are estimates of the infectivity in animal
tissues during disease incubation. Data are limited for BSE in sheep
acquired by oral challenge, but using new experimental results and
published data from studies of both scrapie
4±7
and sheep BSE
8,9
pathogenesis, we constructed an infectiousness pro®le. This pro®le
was based on temporal changes in the density of the agent in
different tissues, weighted by the proportion of such tissue in the
host's body (Fig. 1b). This pro®le differs from that of BSE in
cattle
10,11
, with a more rapid rise in overall infectivity early in the
incubation period in a wide range of tissues (for example, spleen
and lymph nodes). The sheep±human infectiousness pro®les
(Fig. 1b) adjust for tissue-speci®c usage in food
12
and the effect of
the 1997 speci®ed risk materials (SRM) ban in sheep.
The distribution of the BSE incubation period in sheep is not well
characterized, but on the basis of the limited available data, we used
letters to nature
420 NATURE | VOL 415 | 24 JANUARY 2002 | www.nature.com
0
1
2
3
4
5
6
7
8
1980 1983 1986 1989 1992 1995 1998
Year
Infectivity entering food supply
(per year ×10
3
)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1
BSE feed risk
BSE cases
Infectivity
BSE feed risk
d
0
0.2
0.4
0.6
0.8
1
9 8 7 6 5 4 3 2 1 0 10
Years
Survival probability
0
0.1
0.2
0.3
0.4
0.5
IPD density
Survival
probability
Incubation
period
distribution
c
10
–4
10
–3
10
–2
10
–1
1
0 6 12 18 24 30 36
Incubation time (months)
Infectiousness
Human infectivity before SRM
Human infectivity after SRM
Human infectivity with offal ban
Sheep–sheep infectivity
b 10
7
10
6
10
5
10
4
10
3
10
2
10
–4
10
–3
10
–2
10
–1
1
Prevalence (%)
Sample size
Upper 95% bound on
prevalence if no cases
detected
Sample size
for 95% chance
of observing at least
1 case
a
0
1
2
3
4
1997 1999 2001 2003
10% maternal
No maternal
Figure 1 Epidemiological inputs to transmission model. a, Relationship between sample
size and detectable prevalence in screening studies. b, Infectiousness of sheep as a
function of time from infection (see Methods). Sheep and human pro®les are separately
normalized to give maxima of 1. c, Survival probability of sheep as a function of age, and
assumed incubation period distribution (IPD) of BSE in sheep. The survivorship function
was estimated from annual data from the June census, slaughter, export and
disappearance statistics, and data on the seasonality of lamb slaughter. d, Before
mid-1988, both reported and unreported clinical BSE cases could be used for food
(red-shaded curve). After that time, BSE was made noti®able and cases were destroyed,
so we assume none entered food. The blue-shaded curve represents the rate of slaughter
(per year) of pre-clinical infected cattle weighted by infectiousness relative to disease
onset, assuming infectiousness grows at the exponential rate of 4 per year. The over-30-
month scheme ended most bovine exposure in 1996, with estimates of residual levels
(inset) being dependent on the extent of maternal transmission of BSE. The solid black
curve represents the estimated infection hazard to cattle and sheep posed by infectivity in
contaminated feed, relative to the maximum level reached in 1988.
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