Few studies have focused on environmental and behavioral variables associated with plague infection, especially in the plague-endemic West Nile region of Uganda. Information gleaned from such studies may aid in tailoring evidence-based recommendations for the prevention and control of plague in this region. By coupling a previously published landscape-level statistical model of plague risk12
with this observational survey, we were able to identify potential residence-based variables associated with huts within historic case or control villages (e.g., distance to neighboring homestead and presence of pigs near the home) and huts within areas previously predicted as elevated or low risk (e.g., corn and other annual crops grown near the home, water storage in the home, and processed commercial foods stored in the home).
Although additional studies are required to fully understand why these variables emerged as predictors, we believe that they are consistent with current ecological theories on plague host population dynamics. Plague epizootics, the periods when humans are at greatest risk of being exposed to infected fleas, are dependent on critical thresholds of rodent hosts and vector fleas. That is, as host abundance and flea infestation rates increase, so does the probability of epizootic activity.1,2,19,20,31–36
Human risk of exposure has been associated with behaviors that increase the probability of contact with infectious fleas or practices that increase the availability of food or harborage for rodents.21,25
Rodent movement is often driven by food availability and appropriate habitat.34,37
Therefore, behaviors that attract flea-infested rodents into peridomestic settings may increase the probability of human exposure to plague-infested fleas or rodent hosts.38
In an attempt to identify areas of elevated risk of human exposure to plague bacteria in the West Nile region, a fine-resolution model was recently created based primarily on RS variables.12
As previously mentioned, plague risk was higher at elevations greater than 1,300 m than below,16
and RS variables included in the model implied that risk was elevated in wetter areas with less vegetative growth and more bare soil during the dry month of January when fields of seasonal crops are typically fallow.12
The reasons for why these variables were indicative of elevated risk were not evaluated in the previous study, but it was hypothesized that these spectral signatures were associated with areas of more intensive agriculture.12
Presumably, agricultural crops would increase the food supply for rodents and may result in higher densities of rodents. Our residence-based observations showed that some seasonal crops, such as corn and other grains, were associated with elevated risk areas and may be more attractive to rodents than perennial plantation crops such as bananas or coffee beans, which were either similar between elevated- and low-risk areas or more frequently associated with low-risk areas. Indeed, previous studies rarely observed rodent damage to banana and coffee crops compared with other seasonal crops,37
suggesting that, perhaps, rodents are less attracted to banana and coffee crops. The differentiation between these crop types is consistent with the spectral signatures used to differentiate elevated- and low-risk areas. Specifically, corn and other grain fields are often fallow during the dry month of January and would be expected to yield high brightness values indicative of bare soil and little vegetative growth.
The RS model also identified a positive association between wetness and the probability of an area being classified as elevated risk. Our multivariable model indicated a negative association with availability of water for rodents (e.g., presence of water in containers) within huts situated in pixels classified as elevated risk. We believe that water storage in huts may be more common in drier areas that are more distant from water sources. Finally, storage of processed commercial foods within the hut was more frequently associated with areas of low risk. Again, this variable may relate back to agricultural practices, such that in areas of elevated risk, more subsistence crops such as corn are grown, and thus, there is less need for purchasing commercial foods. Alternatively, it is possible that commercially processed foods are more commonly purchased in areas that engage in growing cash crops, such as coffee, which is found in areas classified as low risk, as stated above. In addition, the packaging of this processed food could be a deterrent for the rodents if enough easily accessible food is available. Because our study did not quantify the abundance of such foods but rather surveyed simple presence or absence of these food types, it is difficult to draw conclusions about this variable.
Our observational survey was conducted before the identification of RS landscape variables associated with elevated plague risk in this region,12
and thus, we did not control for many of these variables in our village selection. Confirming and reemphasizing the importance of these RS variables in assessing the likelihood of human plague case occurrence, our univariate analyses (objective 1) () showed that three of four variables included in the previous model (e.g., elevation, brightness, and Landsat ETM+ band 6) remained significant predictors of case or control designation. The multivariable analyses revealed that huts in case villages typically had lower Landsat ETM+ band 6 values compared with huts in control villages; this is indicative of wetter conditions in case areas compared with control areas and shows consistency with the model predictions.
In addition to these landscape variables, we identified three residence-based variables that were predictive of case or control village designation. Specifically, when huts in case villages were compared with huts in control villages, pigs were more commonly observed in the peridomestic setting, and huts were spaced farther from their neighbors. We speculate that peridomestic pigs were observed more frequently in historic case villages because of a similar dietary pattern between rodent species and pigs. Commensal and sylvatic rodents that are susceptible to plague infection could be attracted to food provided to the pigs. These food sources could serve to increase the local carrying capacity for these rodents. Regarding hut spacing, local observations suggest that the spaces between neighboring homesteads are often occupied either by agricultural plots that could serve as food sources for rodents (e.g., corn and other seasonally grown grains) or brush that could serve as rodent harborage. Land converted to agriculture increases the habitat and food availability for sylvatic rodents and potential interactions with peridomestic rodents.28,38
It is also believed that areas with increased primary production of food crops, which result from elevated precipitation rates and wetter conditions, may increase the carrying capacity of rodents.1,2,28,33,35,39,40
After repeating the analysis using only huts that occurred within pixels recently classified as elevated risk (objective 3) ( and ), the association with pigs in the peridomestic setting and distance to neighbor remained as significant predictors of case or control designation.
In addition to identifying variables that may increase the risk for plague infection, other factors were more commonly found within control villages, suggesting that these behaviors or environmental conditions may be protective against exposure to plague bacteria. Beds made of material other than reed mats (e.g., foam pad or stuffed mattress) were observed more frequently within huts in control villages compared with case villages. We speculate that reed mats may be more likely to be infested with fleas than other bedding, because the organic content or dust media in these mats provides a suitable place for fleas to breed.41
Although our models yielded overall accuracies of 74–78%, several additional studies are required to improve our understanding of plague risk factors. Because case investigations were not conducted to determine the location of exposure, our study was based on randomly selected huts within case and control villages. Within villages, huts are not homogenous with respect to many of the surveyed variables. Focusing future surveys on the residence of laboratory-confirmed plague patients and appropriate controls may improve model accuracy. As suggested before, targeting areas classified as elevated risk that continue to not report plague cases may provide insight into subtle differences in housing, crops, or behaviors that prove protective.12
In addition to focusing future efforts within ecologically conducive areas and in conjunction with laboratory-confirmed plague case investigations, it would be beneficial to conduct the surveys during plague outbreaks or during the wet season, when most plague cases have been reported. Many of the variables that we surveyed related to crop production and storage. These practices change seasonally and may be associated with observed differences over time and space in the distribution of zoonotic hosts and their vectors.12,19,20,37
Future studies could also include making adjustments to the environmental and behavioral questions on the observational survey. Questions should include type and frequency of mud smearing, quantity of seasonal crops growing around huts, quantity of foods being stored in huts, and frequency and type of interactions between peridomestic animals and humans. Lastly, further investigation of the variables that presented as significant in this study should be conducted to test our hypotheses for why they may enhance or diminish plague risk. Understanding the critical link between fleas, their reservoir hosts, and humans is essential to prevention and control of plague within this endemic region of Uganda.23
We believe that this study provides important preliminary information about environmental and behavioral factors that might be contributing to plague risk.