Pasture Types and
Echinoc oc c us
Qian Wang,* Dominique A. Vuitton,†
Yongfu Xiao,* Christine M. Budke,‡
Maiza Campos-Ponce,§ Peter M. Schantz,¶
Francis Raoul,† Wen Yang,* Philip S. Craig,#
and Patrick Giraudoux†
Our study showed that open pastures had more small
mammal burrows than fenced pastures in Tibetan pastoral-
ist communities in 2003. This characteristic was linked to a
higher prevalence of Echinococcus multilocularis in dogs
and indicates that pasture type may affect E. multilocularis
pathogenic cestode. Foxes are frequently definitive hosts
(adult stage), and small mammals are intermediate hosts
(larval stage or metacestode). Human AE, albeit restricted
to localized endemic areas, is a public health concern in
central Europe (1). In western China (2,3), dogs are defin-
itive hosts of AE and have transmitted infection to humans
more often than was realized historically (4). Recent mass
ultrasound screenings in Tibetan pastoral communities of
Sichuan Province, People’s Republic of China, document-
ed an average AE prevalence of 2% (5) and a maximum
prevalence of 14.3% (6) in humans.
Since the 1980s, partial fencing of pastures around
Tibetan pastoral winter settlements has become common
because of changes in land property regulations (7). In a
previous study, we showed that partial fencing promoted
AE transmission in these communities (8). This increased
disease prevalence is likely due to the greater population of
small mammal intermediate hosts of the parasite on the
Tibetan plateau and leads to more infection in community
dogs (8). When yak, sheep, and horse grazing lowers the
height of vegetation, Ochotona curzoniae, a very suscepti-
uman alveolar echinococcosis (AE) is an infection
caused by Echinococcus multilocularis, a highly
ble host for E. multilocularis, may be found at greater den-
sities than on natural meadows (9). This study was
designed to investigate the effect of partial fencing on the
general abundance of small mammals in the Tibetan pas-
toralist winter settlements and its potential consequences
for contamination pressure. The study was approved by the
ethical committees of Sichuan Institute of Parasitic
Diseases and all collaborating investigators.
Based on documented high prevalence of AE and
observed fencing practices in the area (8), Qiwu, Yiniu,
and Xiazha townships in Shiqu County of Ganzi Tibetan
Autonomous Prefecture, located at a mean elevation of
4,200 m in northwest Sichuan Province, were selected as
study sites to carry out investigations in spring and autumn
2003. For the 3 townships, the populations were 2,238,
2,515, and 2,471 and the areas 1,046 km2, 955 km2, and
834 km2, respectively. Thirty kilometers of transect over
30 settlements in the 3 townships (18 villages), which were
randomly selected according to landscape patterns, i.e.,
valley, valley entrance, piedmont, and flat land, were sur-
veyed. Small mammal populations were monitored by
using index methods. These methods are based on detect-
ing surface indicators of small mammals, i.e., holes and
feces, and are used to link small mammals and their habi-
tats on large areas (10–12). Sampling was performed by 2
investigators walking along a 1-km transect drawn across
each settlement, according to a standardized protocol.
Along each transect, 50 areas were sampled for small
mammal burrows; each area was 200 m2. Areas of fenced
pastures were measured in 22 settlements by using a glob-
al positioning system (GPS) (GPS 12, Garmin
International Inc., Olathe, KS, USA). In 15 settlements in
which dog feces samplings were conducted in Yiniu and
Xiazha townships, feces specimens were collected from
dogs after purging with arecoline, according to the recom-
mendations of World Animal Health Organization/World
Health Organization (13), and droppings were collected
from the ground when accessible (4). Helminths found in
the feces were removed, counted, and placed in 10% for-
mal saline or 85% ethanol. Copro-polymerase chain reac-
tion testing was conducted by using species-specific
primers for E. multilocularis DNAamplification according
to Dinkel et al. (14) as modified by van der Giessen et al.
The distribution of small mammal burrows was highly
skewed. Kolmogorov-Smirnov test indicated that the data
did not fit a normal distribution (p<0.001 in both cases)
either inside or outside fenced pastures. Normality was not
obtained after Box-Cox transformations. Thus, the burrow
density of small mammals was compared between open
and fenced pastures by using nonparametric tests that con-
sidered landscape factor. Spearman correlation tests were
used to quantify the relationship between the burrow
1008Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 12, No. 6, June 2006
*Sichuan Provincial Center for Disease Control and Prevention,
Chengdu, Sichuan, People’s Republic of China; †University of
Franche-Comte, Besançon, France; ‡Texas A & M University,
College Station, Texas, USA; §Free University, Amsterdam, the
Netherlands; ¶Centers for Disease Control and Prevention,
Atlanta, Georgia, USA; and #University of Salford, Salford, United
density of small mammals on open pastures and the sur-
face of fenced pastures in settlements in which the fenced
areas were all measured, controlling for the landscape fac-
tor. Amultiple logistic regression model was used to relate
median burrow density of small mammals to dog infection
in the settlements. The dependent variable was a pres-
ence/absence vector (0/1) (dog was negative or positive for
E. multilocularis). Independent variables included dog’s
age and sex, droppings collected versus purged fecal sam-
ples, and median density of small mammal burrows. All
these analyses used SPSS release 10 (SPSS, Chicago, IL,
Landscape type influenced the abundance of small
mammal burrows (p<0.001). Post hoc Tukey multiple
comparison test on ranks confirmed that the densities of
small mammal burrows were different among different
landscape types (p<0.05), except for the comparison
between flatland and piedmont. The burrow densities of
small mammals on open pastures were significantly high-
er than those on fenced pastures in 3 of 4 landscapes
The Spearman correlations showed larger fenced areas
associated with higher density of small mammal burrows in
the open pastures in all landscape types (Table 2). The rela-
tionships between the area of fenced pastures and the bur-
row density of small mammals inside the fenced pastures in
the 4 landscapes were not significant (valley [rs=–0.08, p =
0.32], flatland [rs=–0.46, p = 0.02], piedmont [statistics not
applicable because of 3 observations only], and valley
entrance [rs = 0.08, p = 0.736]), except for flatland.
Feces samples, of which 159 (63.1%) were purged,
were obtained from 252 dogs (mean age 4.4 years; 183
males). E. multilocularis infection rate was 16.7%
(42/252); the infection rate was 18.2% (29/159) for purged
samples and 14.0% (13/93) for sampled droppings.
Multiple logistic regressions showed that the median den-
sity of small mammal burrows in the open pastures was
significantly positively related to dog infection (p = 0.003,
odds ratio 1.05, 95% confidence interval 1.02–1.08). No
correlation to dog age (p = 0.52), sex (p = 0.78), or sample
collection method was seen (p = 0.380).
The higher median burrow density of small mammals
was linked to a higher prevalence of E. multilocularis in
dogs in these Tibetan pastoralist communities. Thus, par-
tial fencing increases populations of potentially suscepti-
ble small mammal species in open pastures and
consequently higher contamination pressure by dogs.
In a previous study, we showed that partial fencing
around Tibetan settlements in winter pasture was signifi-
cantly and independently associated with the risk for
human AE in surveyed villages (8). We assumed that the
underlying reason might be overgrazing, exacerbated by
reducing communal pastures near the settlements because
of introduction of partial fencing around group tenure pas-
tures acquired by Tibetan pastoralist families. Overgrazing
may have promoted population outbreaks of small mam-
mal intermediate hosts of the parasite and increased the
density of the small mammal intermediate host, especially
O. curzoniae. This increase consequently favored higher
dog E. multilocularis infection and, thus, transmission to
humans (8). This study supports this hypothesis.
This study was supported by the Sichuan Provincial Health
Department, China, and the US National Institutes of
Health/National Science Foundation (Ecology of Infectious
Diseases program, grant #1565). Q.W. was supported by a PhD
grant from the French Embassy in Beijing.
Dr Wang is an associate fellow at the Division for Disease
Control Coordination, Sichuan Provincial Center for Disease
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 12, No. 6, June 2006 1009
Pasture Types and E. multilocularis
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Control and Prevention, Chengdu, Sichuan, People’s Republic of
China. His research interests include application of socioeconom-
ics to epidemiologic research.
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Address for correspondence: Qian Wang, Sichuan Provincial Center for
Diseases Control and Prevention, 10 University Rd, Chengdu, Sichuan
610041, People’s Republic of China; email: firstname.lastname@example.org