a geographic information system on the potential
TRANSCRIPT
A geographic information system on the potential
distribution and abundance of Fasciola hepatica
and F. gigantica in east Africa based on Food
and Agriculture Organization databases
J.B. Malonea,*, R. Gommesb, J. Hansenb, J.M. Yilmac,J. Slingenbergb, F. Snijdersb, F. Nachtergaeleb, E. Atamanb
a School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803, USAb Food and Agriculture Organization, Viale della Terme di Caracalla, Rome 00100, Italy
c Faculty of Veterinary Medicine, Addis Ababa University, P.O. Box 34, Debre Zeit, Ethiopia
Received 23 April 1997; accepted 23 February 1998
Abstract
An adaptation of a previously developed climate forecast computer model and digital
agroecologic database resources available from FAO for developing countries were used to
develop a geographic information system risk assessment model for fasciolosis in East Africa, a
region where both F. hepatica and F. gigantica occur as a cause of major economic losses in
livestock. Regional F. hepatica and F. gigantica forecast index maps were created. Results were
compared to environmental data parameters, known life cycle micro-environment requirements and
to available Fasciola prevalence survey data and distribution patterns reported in the literature for
each species (F. hepatica above 1200 m elevation, F. gigantica below 1800 m, both at 1200±
1800 m). The greatest risk, for both species, occurred in areas of extended high annual rainfall
associated with high soil moisture and surplus water, with risk diminishing in areas of shorter wet
season and/or lower temperatures. Arid areas were generally unsuitable (except where irrigation,
water bodies or floods occur) due to soil moisture deficit and/or, in the case of F. hepatica, high
average annual mean temperature >238C. Regions in the highlands of Ethiopia and Kenya were
identified as unsuitable for F. gigantica due to inadequate thermal regime, below the 600 growing
degree days required for completion of the life cycle in a single year. The combined forecast index
(F. hepatica�F. gigantica) was significantly correlated to prevalence data available for 260 of the
1220 agroecologic crop production system zones (CPSZ) and to average monthly normalized
difference vegetation index (NDVI) values derived from the advanced very high resolution
Veterinary Parasitology 78 (1998) 87±101
* Corresponding author. Tel.: 001 504 346 3232; fax: 001 504 346 5715; e-mail: [email protected]
0304-4017/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved
PII S 0 3 0 4 - 4 0 1 7 ( 9 8 ) 0 0 1 3 7 - X
radiometer (AVHRR) sensor on board the NOAA polar-orbiting satellites. For use in Fasciola
control programs, results indicate that monthly forecast parameters, developed in a GIS with digital
agroecologic zone databases and monthly climate databases, can be used to define the distribution
range of the two Fasciola species, regional variations in intensity and seasonal transmission patterns
at different sites. Results further indicate that many of the methods used for crop productivity
models can also be used to define the potential distribution and abundance of parasites. # 1998
Elsevier Science B.V.
Keywords: Geographic information systems; Climate; Distribution; Fasciola hepatica; Fasciola gigantica; East
Africa; Food and Agriculture Organization
1. Introduction
Geographic information systems (GIS) provide a way to use computers to create,
archive and analyze traditional map data on the epidemiology of disease and to combine
these with global environmental data derived from sensors on board earth observing
satellites. A GIS is created by linking standard computer database `attributes' to map
features represented as layered point, line or polygon `vector' data or to map features
represented as digital `raster' image data pixels (picture elements). Using a new
generation of commercially available digital geographic databases and hand held
geographic positioning systems (GPS) linked to a constellation of satellites, precise point
location and maps can be created for disease applications. Common software/hardware
and commercial data sources for personal computers (PCs) are available to provide
laboratory GIS capability suited for disease investigations at costs affordable by most
academic and government disease control units. These capabilities make it possible to use
computer mapping, remote sensing and GIS to create `health maps' that can be used in
routine disease control programs.
Literature reports on GIS medical and veterinary applications include malaria (Beck et
al., 1994), Rift Valley fever (Linthicum et al., 1987), filariosis (Thompson et al., 1996),
African trypanosomosis (Rogers and Randolph, 1993), theileriosis (Lessard et al., 1990),
Onchocerca (Richards, 1993), Leishmania (Cross et al., 1996), Amblyomma variegatum
(Hugh-Jones et al., 1992), Lyme disease (Kitron et al., 1992), Fasciola (Zukowski et al.,
1991; Malone et al., 1992; Malone and Zukowski, 1992; Malone, 1997), and Schistosoma
(Cross and Bailey, 1984; Malone et al., 1994, 1997).
According to the concepts of landscape epidemiology and the doctrine of nidality
(Pavlovsky, 1966), diseases have natural habitats in the same way as a species: they are
found in focal areas where the spatial distribution of the parasite, host, vector and
required environmental conditions coincide. Inside the distribution range, there are
favorable zones where a high level of abundance is maintained. Near the limits of
distribution there is often a patchy marginal zone of low abundance and epidemiologic
instability. The boundaries of distributions are not strictly fixed and may fluctuate with
climate and other components of the environment. The latter zones would be expected to
change most with relatively small changes in the environment, such as annual weather
variation or long term changes projected by recent studies on global warming.
88 J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101
Crop models are well known that describe the suitability of different environments for
cultivation and recommended times for planting, fertilizer and pest control (Van
Velthuizen et al., 1995). It is proposed that similar methods can be developed, with GIS
agroclimatic databases and satellite sensor technology, to describe the distribution range
and suitability of different areas for propagation and transmission of disease, and that this
information can then be used to design control programs and optimize interventions. In
the current study, a previously developed climate forecast system (Malone et al., 1987)
and digital agroecologic database resources available from FAO for developing countries
were used, in a GIS, to develop a control model for fasciolosis in East Africa, a region
where both F. hepatica and F. gigantica occur as a cause of major economic losses in
livestock.
2. Methods and materials
2.1. GIS data resources
The Climate Based Parasite Forecast System developed at Louisiana State University
for mapping the geographic distribution, relative risk of economic losses and annual
variation in transmission intensity of Fasciola hepatica in the Southcentral USA (Malone
et al., 1987) was further developed for use in East Africa using Atlas GIS software (ESRI,
Redlands, CA) and a modification of the forecast system that utilized monthly rather than
daily climate values. The original forecast utilizes daily minimum and maximum
temperature and rainfall data for a given site to calculate F. hepatica risk indices based on
the local Thornthwaite water budget and the growing degree day concept. Growing
degree days (GDD�degrees over 108C minimum for development) are accumulated if
water is present in the top 2.5 cm of soil or multiplied times surplus water (cm) if soil
moisture exceeds field capacity. Thirty-year-average data can be used to calculate the
`Normal' risk for a site; annual variation in risk is calculated using current climate data
and compared to 30-year-average values or prior years (Malone and Zukowski, 1994). A
Fasciola GIS forecast system was developed for the Intergovernmental Authority on
Drought and Development (IGADD) sub-region of East Africa using the forecast and the
following Food and Agriculture Organization (FAO) resources.
2.1.1. CVIEW: IGADD crop production system zones (CPSZ)
CVIEW is an FAO software product used to map over 500 database variables for 1220
agroecologic/administrative zones in Ethiopia, Eritrea, Sudan, Somalia, Kenya, Uganda
and Djibouti. It is designed to view, select and export relevant environmental and crop
production datasets to commercial GIS software systems for specific applications (Van
Velthuizen et al., 1995). Atlas GIS (ESRI, Redlands, Ca) software was selected for use
because of its import compatibility with CPSZ databases.
2.1.2. FAOCLIM world climate databases
FOACLIM is available on a CDROM with worldwide monthly climate data and FAO
agroclimatic data analysis software programs (FAO, 1995).
J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101 89
2.1.3. FAO-ARTEMIS/NASA-GSFC satellite image archive
Normalized difference vegetation index (NDVI) derived from the AVHRR of the
national oceanic and atmospheric administration (NOAA) environmental satellite series
for 1981±1991 is accessible on a CDROM. NDVI and estimates of rainfall based on
cold cloud duration (CCD) are used for real-time famine early warning and other
applications using a roof-top data receiver at the Rome headquarters of FAO with
Addapix (Griguolo, 1996) and image display and analysis (IDA) software (Hoefsloot,
1996) developed by FAO. Mean monthly NDVI values derived from the entire 1981±
1991 database (based on 7 km2 pixel size spatial resolution at earth surface) were
interpolated to provide a mean value for the area covered by each CPSZ in the CVIEW
database.
2.1.4. FAO soil type databases (1:1,000,000 scale) for the IGADD sub-region
(Nachtergaele, 1996)
Map file were extracted from this database on potentially waterlogged soils of neutral
or alkaline pH and acid soils of <5.5 pH.
2.2. Prevalence data
Prevalence data for Fasciola was entered for corresponding CPSZ mapunits from
available literature reports for Kenya, Sudan and Ethiopia (Gemechu and Mamo, 1979;
Graber et al., 1978; Karib, 1962). Reported prevalence was assigned to all CPSZ included
in the survey area described by authors.
2.3. Creation of atlas GIS project files
Excel files containing CPSZ data, results of climate forecast calculations and
prevalence data were exported as DBase IV files (.dbf), each column of which was used
by Atlas GIS as values for each of the 1220 CPSZ mapunits for display on the computer
monitor as separate layers (or as products of analysis of several layers/values). CPSZ
boundaries for the 1220 mapunits (polygon files), river/water bodies, railroads, roads
(line files) and capitals±towns±villages (point files) were exported as longitude and
latitude, comma delimited (.bna) files, then imported into Atlas GIS as (.agf) map files.
Map files were linked to database (.dbf) attribute data according to name (identical to
names of the 1220 mapunits) and then analyzed within Atlas GIS. An IGAAD soil
database (.bna) file on potentially waterlogged soils of neutral or alkaline pH and soils
with pH <5.5 were also imported into Atlas GIS as a separate (.agf) file. Fasciola
prevalence data was entered as a column in Excel and exported, with data from the CPSZ
database and forecast calculations, to Atlas GIS.
Regional F. hepatica and F. gigantica forecast index maps were created. Results were
compared to environmental data parameters and to available prevalence survey data and
distribution patterns reported in the literature (Bergeron and Laurent, 1970) for each
species (ie. F. hepatica above 1200 m elevation, F. gigantica below 1800 m, both species
at 1200±1800 m). Statistical analysis was done using the Spearman rank-order correlation
test and linear regression analysis (Bruning and Klintz, 1977).
90 J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101
3. Results
3.1. Monthly forecast adaptation
Initially, the FAOCLIM database was used to create a `typical year' for 27 representa-
tive sites using monthly 30-year-average data on minimum and maximum temperature
and number and intensity of rainfall events per month (Landsberg, 1972) using the
original daily forecast system. This proved too time intensive for estimating daily
baseline values for comparison to daily forecast indices. The climate forecast formula
was, therefore, adapted for large scale regional use using monthly climate data and
average annual mean temperature for each of the 1220 mapunits in the CPSZ database.
�GDD�days in month; IF �Rÿ �PET� 0:8� > 0����GDD� 6���Rÿ PET�=25��; IF Rÿ PET > 0� � Index
where R�rainfall, PET�potential evapotranspiration (calculated by the modified Penman
method) and GDD�average annual mean temperature ± base development temperature
for F. hepatica or F. gigantica.
In the first part of the formula, subtracting the factor (PET*0.8) from rainfall is
equivalent to counting monthly GDD if moisture storage is present in the top 2.5 cm layer
of a soil water budget model. The second part counts GDD if monthly surplus water is
present due to rainfall events; GDD is multiplied by 6 based on monthly records that
indicate that 6 rainydays/month with over 1 mm of rain are typical in areas that have a
rainy season that results in surplus water (i.e. most areas of Ethiopia). For use at specific
sites in the IGADD zone or elsewhere, this value can be adjusted based on 30-year rain
pattern data.
Climate data was selected from the CPSZ database and exported to an Excel 5.0
spreadsheet for monthly rainfall and potential evapotranspiration (PET), average annual
mean temperature, NDVI (mean monthly value based on the 1982±1991 database),
growing season (length, duration, beginning, end), altitude and irrigation status. Excel 5.0
was then used to calculate forecast values and to perform initial statistical analysis.
F. hepatica risk index (a temperate zone species) was calculated using a GDD base
temperature of 108C. For the tropical species F. gigantica, risk index was calculated
similarly but to the reported base temperature of 168C (Dinnik and Dinnik, 1963). The
average annual mean temperature was used since mean temperatures are relatively
constant year-round at IGADD sub-region latitudes; this value is successfully used in
regional crop forecast models in lieu of daily or monthly temperature data (Van
Velthuizen et al., 1995). The forecast revealed indices of over 6000 in Ethiopian highland
areas that receive major rainfall, a value that reflects the relative severity of the fasciolosis
problem in that country; indices in fluke zones or the southern gulf coast of the USA
exceed indices of 3000 only in very high risk years (Malone and Zukowski, 1994).
3.2. GIS model output
Using separate models for F. gigantica and F. hepatica (Figs. 1 and 2), fasciolosis risk
gradients were identified in the IGADD sub-region on the basis of 30-year-average
J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101 91
monthly climate data. For both models, the greatest risk occurred in areas of extended
high annual rainfall associated with high soil moisture and surplus water, with risk
diminishing in areas of shorter `wet' season and/or lower temperatures. Arid areas
were generally unsuitable (except where irrigation, water bodies or floods occur) due to
soil moisture deficit and/or, in the case of F. hepatica, high average annual mean
temperature.
For F. gigantica, regions in the highlands of Ethiopia and Kenya were identified as
unsuitable due to inadequate thermal regime (i.e. below the 600 growing degree days
required for completion of life cycle in a single year); this result is consistent with
literature reports of a dearth of F. gigantica over 1800 m elevation in Ethiopia (Bergeron
and Laurent, 1970).
F. hepatica endemic areas in the highlands of Ethiopia and Kenya could be identified
and characterized as to relative risk and geographic distribution. In initial forecast output,
Fig. 1. Fasciola gigantica potential distribution and abundance in the IGADD sub-region based on a GIS
constructed from FAO CVIEW agroecologic zone map files, 30-year-average monthly climate databases, a
modification of the LSU climate based parasite forecast system, a base life cycle development temperature of
168C and known irrigation zones. Irrigated areas and flood zones, also suitable for F. gigantica, were not
included in the climate forecast analysis.
92 J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101
`false positive' areas were seen in the lowlands of Sudan and Uganda. Further iterative
GIS analysis suggested that soil acidity regime in Southwestern Sudan and Uganda (<5.5
pH) may be unsuitable for lymnaeid snail hosts of F. hepatica and/or that tropical thermal
regimes with average annual mean temperature above 238C are unsuited to this temperate
species. Average annual mean temperature of 238C or above were found to correspond to
areas below the reported 1200 m elevation limit of F. hepatica in Ethiopia.
Statistical analysis revealed the sum of forecast indices (F. hepatica index�F. gigantica
index) was correlated (p<0.05) by the Spearman rank-order correlation test with available
prevalence survey data from 260 CPSZ in Ethiopia, Sudan and Kenya (Gemechu and
Mamo, 1979; Graber et al., 1978; Karib, 1962) and by linear regression analysis with
average monthly 1981±1991 NDVI values from the FAO ARTEMIS satellite data archive
Fig. 2. GIS map of F. hepatica potential distribution and abundance gradients for the IGADD sub-region. A base
temperature of 108C for life cycle progression was used. Zones with average annual mean temperatures of
>238C were excluded (shown as areas with horizontal dotted lines). This temperature corresponds to the reported
1200 m elevation lower limit of F. hepatica distribution in Ethiopia. Additional areas in Uganda, Kenya and
Southern Sudan may be unsuitable for Lymnaea truncatula snail hosts based on the presence of acid ferralsol
soils of <5.5 pH (Nachtergaele, 1996).
J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101 93
(Figs. 3±5). The latter suggests that NDVI threshhold criteria might be further developed
as an additional parameter or surrogate for climate values in the forecast.
4. Discussion
Results indicate that the Climate Based Parasite Forecast System, modified for use in a
GIS with CVIEW map viewer databases and the FAOCLIM worldwide monthly climate
database, can be used to define: (1) the potential distribution range of F. hepatica and
F. gigantica, (2) regional differences in intensity of Fasciola spp. transmission, and (3)
seasonal transmission patterns at divergent sites. This information is essential for design
of control programs and to determine the most cost-effective time(s) for treatment.
Current monthly climate values may also be used to generate forecasts of annual
variation in disease risk, although previous experience with FAO crop models shows that
dekadal (10-day-average) data is more suitable for forecast purposes (FAO, 1995). Where
both Fasciola species overlap, the forecast index for each may be summed. Where
Fig. 3. Average monthly normalized vegetation index (NDVI) values�1000 for CPSZ mapunits interpolated
from the FAO-ARTEMIS NDVI Image Bank, Africa, 1981±1991 decadal time series (FAO, 1993). While
NDVI and Fasciola forecast values are statistically related, probably due to common dependence on thermal-
moisture regime, the spatial relationships of the two Fasciola species and average monthly NDVI are not
the same.
94 J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101
available, daily data may be used in the original forecast model on a site-specific basis
where greater precision is required than is possible with monthly or dekadal climate data.
Results indicate the need for more accurate data on the environmental requirements
and limits of tolerance of Fasciola spp., including minimum, maximum, optimum
temperatures, moisture regime and soil characteristics suited for life cycle propagation.
Such information has in the past been generated by laboratory or field microenvironment
studies that define these factors under varying conditions (Appleton, 1978).
In the future, GIS may provide an alternative way to define the range and optimum
conditions for a parasite species by mapping survey data and then iteratively fitting them
to associated climatic and edaphic conditions. A possible upper limit of 238C for F.
Fig. 4. Relationship between reported fasciolosis prevalence (%) and combined annual forecast indices (F.
hepatica � F. gigantica) in 260 of 1220 agroclimatic crop production system zones in the IGADD sub-region of
East Africa, ranked by forecast indices. The Spearman rank-order correlation test showed a significant direct
relationship (p<0.05). Low prevalence rates (1±20%) were seen in the first 20 CPSZ, where no Fasciola risk was
forecast, were located in warm (>258C), arid to semiarid areas; most of them were associated with rivers or
major±minor irrigation which were not considered in the forecast model but which are expected to be important
enzootic sites for Fasciola.
J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101 95
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96 J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101
hepatica was suggested by the correlation found in the current study with elevations less
than 1200 m in the IGADD zone. While the life cycle may progress with higher
temperatures, continuous or long term temperatures of above 238C over several years
may provide critical limits. This result is consistent with the reported 188C optimum for
this temperate species (Armour, 1975) and suggests the need for further studies on the
limiting effect of higher temperatures on the distribution range of F. hepatica. Similar
conclusions can be derived from the apparent inadequate thermal regime for the tropical
species F. gigantica at cool, high elevation sites. While complete development of this
species requiring two seasons has been reported at high elevations in Kenya where mean
maximum temperatures of 20±308C occur (Preston and Castelino, 1977), such sites are at
the edge of the reported distribution range of F. gigantica; forecast index values, and
prevalence survey data indicate optimum thermal conditions are found at lower elevation,
tropical sites. Dinnik and Dinnik, 1963 reported minimum development temperatures of
168C for F. gigantica in Kenya and found that inhibited cercariae development in infected
snail hosts occurred when mean maximum temperature was below 208C. Schillhorn van
Veen, 1980, however, reported cercariae shedding in the Nigerian savannah in the cool,
dry season (13±188C) and attached less importance to this factor in the total
epidemiology of F. gigantica.
Limited Fasciola prevalence data was available for model development in the present
study. To provide adequate validation data, cooperating scientists in each IGADD country
should be identified for further development and implementation of the Fasciola forecast
GIS and design of integrated parasite control programs. To accomplish this, there is a
need to
� compile published and unpublished prevalence data (eg. thesis, abattoir records, local
meeting reports).
� generate forecast indices to (1) describe a 30-year-average `typical year' in
representative agroecological zones and (2) the range of interannual variation, using
local climate data.
� evaluate efficacy of recommended control programs at selected sites based on seasonal
transmission pattern and current year climate forecasts.
� disseminate model control recommendations to veterinarians and producers, including
early warning of high risk years.
If successful, this application of GIS may serve as a model for developing strategic
control recommendations in other areas of the world where F. hepatica and/or F.
gigantica occur and 30-year-average climate databases are available. Further, the model
may be adapted to develop similar models for other environmentally sensitive diseases,
including tick-borne diseases, trypanosomosis, and other helminth infections, based on
the requirements for propagation and transmission of respective life cycles.
Work reported here may be applicable to strategies for future development of GIS in
animal production and health by FAO and other agencies and for applications in human
health. Broader implementation of GIS technology in control programs for disease will
likely be most effective if centered on PC-based models that allow interaction at user,
developer and central resource levels. Useful medical GIS applications are possible with
relatively simple software packages that are commercially available for use at the PC
J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101 97
level. Many disease control workers could become interactive users of GIS in routine
control programs if it were possible to invest minimal energy learning to access database
viewers, internet web sites and products of GIS models using standard desktop software
resources. Disease control program officers could contribute to shared GIS/database
resources as applications developers in their specific field of expertise and by interactive
database development with field collaborators and GIS support staff at central resource
facilities. Such a three-tier strategy, already operational in FAO crop programs, can be
applied in development of GIS disease control models.
4.1. GIS user level
Viewer software such as CVIEW produced by FAO can be provided inexpensively to
disease control officers, field collaborators and the public on a single disk for PC
operation, allowing users to view, select and export digital map data on a wide range of
environmental variables, crops±crop diseases-forages and livestock±livestock diseases.
Relevant data can be selected and exported to spreadsheets (eg. Excel) for statistical
analysis or linked to exported map files in a GIS for spatial analysis. Enhancements to
CVIEW software under development at FAO (Verelst, 1997; Gommes, pers. comm.) will
allow map display of FAO AGROSTAT-PC databases, development of new applications
and improved data import/export compatibility with most commercial GIS software
packages, speadsheets and presentation graphics. Databases similar to that for the
IGADD Sub-Region are being developed by FAO for Southern Africa and West Africa so
that similar datasets will be available for all of sub-Saharan Africa. PC viewer software is
suitable for users (medical officers, field workers, and the public) with minimal training
(<2 weeks). Such database viewer data for administrative-agroclimatic zones may
provide the basis of improved animal disease and productivity reporting systems, using
`mirror' software at FAO and agriculture ministries in developing countries.
4.2. GIS developer level
Depending on program needs and interest, medical officers who complete entry level
training on commercial GIS packages (1±4 months) may serve as developers for
interactive creation by field specialists and headquarters staff of early warning-
intervention strategies, agricultural statistics analysis, model development and other
applications. Specific GIS applications can be included in database viewers or used in
PC-based GIS analysis packages, spreadsheets and presentation software. Many
commercial PC GIS packages can be linked to FAO database map viewers, to satellite
imagery analysis software products (eg. ERDAS, Atlanta, GA; Idrisi, Newton, MA; IDA,
Rome, Italy) and to advanced resources available at central GIS facilities operational in
many countries and universities.
4.3. Central resource level
To provide higher level UNIX-based and/or PC GIS central resource software/
hardware, data archives (eg. NDVI Image bank, soils, specialized analysis products),
98 J.B. Malone et al. / Veterinary Parasitology 78 (1998) 87±101
expert assistance, training assistance and project collaboration to support developers
and users. Digital map databases and basemaps are increasingly available worldwide
for purchase (eg. ArcData, Digital Chart of the World) or access over the internet.
Central resource personnel and GIS support staff are needed to create, geographically
transform and link spatial data derived from different GIS software packages.
These advanced systems and applications require large inputs of time and specialized
training.
GIS studies reported here suggest that many of the methods used for crop productivity
models can also be used to define the distribution and abundance of parasites. The
expanding availability of digital databases such as CVIEW, AGROSTAT, FAOCLIM,
internet data sources, improved hardware/software systems for analyzing climate, digital
thematic maps of selected environmental features, and sensor data from earth observing
satellites provide new opportunites for use of GIS models as decision support systems for
disease control programs.
Acknowledgements
This work was partly supported by the FAO Programme of Cooperation with Academic
and Research Institutions during a 4-month sabbatical leave by J.B. Malone at the Animal
Production and Health Division, FAO Headquarters, Rome, Italy. Dr Yilma's
contributions during a 9-month stay at Louisiana State University were supported by
the Fulbright Senior Research Scholar Program of the Council for the International
Exchange of Scholars, United States Information Agency, Department of State,
Washington, D.C.
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