A spatiotemporal epidemiological investigation of the impact of environmental change on the transmission dynamics of Echinococcus spp. in Ningxia Hui Autonomous Region, China
Background: Human echinococcoses are zoonotic parasitic diseases
of major public health importance globally. According to recent
estimates, the geographical distribution of echinococcosis is
expanding and becoming an emerging and re-emerging problem in
several regions of the world. Echinococcosis endemicity is
geographically heterogeneous and might be affected by global
environmental change over time. The aims of my research were: 1)
to assess and quantify the spatiotemporal variation in land cover
and climate change in Ningxia Hui Autonomous Region (NHAR); 2) to
identify highly endemic areas for human echinococcoses in NHAR,
and to determine the environmental covariates that have shaped
the local geographical distribution of the disease; 3) to develop
spatial statistical models that explain and predict the
spatiotemporal variation of human exposure to Echinococcus spp.
in a highly endemic county of NHAR; and 4) to analyse
associations between the environment and the spatiotemporal
variation of human exposure to the parasites and dog infections
with Echinococcus granulosus and Echinococcus multilocularis in
four echinococcosis-endemic counties of NHAR.
Methods: Data on echinococcosis infections and human exposure to
E. granulosus and E. multilocularis were obtained from different
sources: 1) A hospital-based retrospective survey of human
echinococcosis cases in NHAR between 1992 and 2013; 2) three
cross-sectional surveys of school children conducted in Xiji
County in 2002–2003, 2006–2007 and 2012–2013; and 3) A
cross-sectional survey of human exposure and dog infections with
E. granulosus and E. multilocularis conducted in Xiji, Haiyuan,
Guyuan and Tongxin Counties. Environmental data were derived from
high-resolution (30 m) imagery from Landsat 4/5-TM and 8-OLI and
meteorological reports provided by the Chinese Academy of
Sciences. Image analysis techniques and a Bayesian statistical
framework were used to conduct a land cover change detection
analyses and to develop regression models that described and
quantified climate trends and the environmental factors
associated with echinococcosis risk at different spatial scales.
Results: The land cover changes observed in NHAR from 1991 to
2015 concurred with the main goals of a national policy on
payments for ecosystem services, implemented in the Autonomous
Region, in increasing forest and herbaceous vegetation coverages
and in regenerating bareland. Statistically significant positive
trends were observed in annual, summer and winter temperatures in
most of the region, and a small magnitude change was found in
annual precipitation, in the same 25-year period. The south of
NHAR was identified as a highly endemic area for cystic
echinococcosis (CE; caused by E. granulosus) and alveolar
echinococcosis (AE; caused by E. multilocularis). Selected
environmental covariates explained most of the spatial variation
in AE risk, while the risk of CE appeared to be less spatially
variable at the township level. The risk of exposure to E.
granulosus expanded across Xiji County from 2002–2013, while
the risk of exposure to E. multilocularis became more confined in
communities located in the south of this highly endemic area. In
2012–2013, the predicted seroprevalences of human exposure to
E. granulosus and dog infection with this parasite were
characterised by similar geographical patterns across Xiji,
Haiyuan, Guyuan and Tongxin Counties. By contrast, the predicted
high seroprevalence areas for human exposure and dog infection
with E. multilocularis did not coincide spatially. Climate, land
cover and landscape fragmentation played a key role in explaining
some of the observed spatial variation in the risk of infection
with Echinococcus spp. among schoolchildren and dogs in the south
of NHAR at the village level.
Conclusions: The findings of this research defined populations at
a high risk of human exposure to E. granulosus and E.
multilocularis in NHAR. The research provides evidence on the
potential effects of landscape regeneration projects on the
incidence of human echinococcoses due to the associations found
between the infections and regenerated land. This information
will be essential to track future requirements for scaling up and
targeting the control strategies proposed by the National Action
Plan for Echinococcosis Control in China and may facilitate the
design of future ecosystem management and protection policies and
a more effective response to emerging local environmental risks.
The predictive models developed as part of this research can also
be used to monitor echinococcosis infections and the emergence in
Echinococcus spp. transmission in the most affected areas