Testing the Generality of a Trophic-cascade Model for Plague

Climate may affect the dynamics of infectious diseases by shifting pathogen, vector, or host species abundance, population dynamics, or community interactions. Black-tailed prairie dogs (Cynomys ludovicianus) are highly susceptible to plague, yet little is known about factors that influence the dynamics of plague epizootics in prairie dogs. We investigated temporal patterns of plague occurrence in black-tailed prairie dogs to assess the generality of links between climate and plague occurrence found in previous analyses of human plague cases. We examined long-term data on climate and plague occurrence in prairie dog colonies within two study areas. Multiple regression analyses revealed that plague occurrence in prairie dogs was not associated with climatic variables in our Colorado study area. In contrast, plague occurrence was strongly associated with climatic variables in our Montana study area. The models with most support included a positive association with precipitation in April–July of the previous year, in addition to a positive association with the number of “warm” days and a negative association with the number of “hot” days in the same year as reported plague events. We conclude that the timing and magnitude of precipitation and temperature may affect plague occurrence in some geographic areas. The best climatic predictors of plague occurrence in prairie dogs within our Montana study area are quite similar to the best climatic predictors of human plague cases in the southwestern United States. This correspondence across regions and species suggests support for a (temperature-modulated) trophic-cascade model for plague, including climatic effects on rodent abundance, flea abundance, and pathogen transmission, at least in regions that experience strong climatic signals.     

A Non-Stationary Relationship between Global Climate Phenomena and Human Plague Incidence in Madagascar

Background

Plague, a zoonosis caused by Yersinia pestis, is found in Asia and the Americas, but predominantly in Africa, with the island of Madagascar reporting almost one third of human cases worldwide. Plague''s occurrence is affected by local climate factors which in turn are influenced by large-scale climate phenomena such as the El Niño Southern Oscillation (ENSO). The effects of ENSO on regional climate are often enhanced or reduced by a second large-scale climate phenomenon, the Indian Ocean Dipole (IOD). It is known that ENSO and the IOD interact as drivers of disease. Yet the impacts of these phenomena in driving plague dynamics via their effect on regional climate, and specifically contributing to the foci of transmission on Madagascar, are unknown. Here we present the first analysis of the effects of ENSO and IOD on plague in Madagascar.

Methodology/principal findings

We use a forty-eight year monthly time-series of reported human plague cases from 1960 to 2008. Using wavelet analysis, we show that over the last fifty years there have been complex non-stationary associations between ENSO/IOD and the dynamics of plague in Madagascar. We demonstrate that ENSO and IOD influence temperature in Madagascar and that temperature and plague cycles are associated. The effects on plague appear to be mediated more by temperature, but precipitation also undoubtedly influences plague in Madagascar. Our results confirm a relationship between plague anomalies and an increase in the intensity of ENSO events and precipitation.

Conclusions/significance

This work widens the understanding of how climate factors acting over different temporal scales can combine to drive local disease dynamics. Given the association of increasing ENSO strength and plague anomalies in Madagascar it may in future be possible to forecast plague outbreaks in Madagascar. The study gives insight into the complex and changing relationship between climate factors and plague in Madagascar.     

Flea-Associated Bacterial Communities across an Environmental Transect in a Plague-Endemic Region of Uganda

The vast majority of human plague cases currently occur in sub-Saharan Africa. The primary route of transmission of Yersinia pestis, the causative agent of plague, is via flea bites. Non-pathogenic flea-associated bacteria may interact with Y. pestis within fleas and it is important to understand what factors govern flea-associated bacterial assemblages. Six species of fleas were collected from nine rodent species from ten Ugandan villages between October 2010 and March 2011. A total of 660,345 16S rRNA gene DNA sequences were used to characterize bacterial communities of 332 individual fleas. The DNA sequences were binned into 421 Operational Taxonomic Units (OTUs) based on 97% sequence similarity. We used beta diversity metrics to assess the effects of flea species, flea sex, rodent host species, site (i.e. village), collection date, elevation, mean annual precipitation, average monthly precipitation, and average monthly temperature on bacterial community structure. Flea species had the greatest effect on bacterial community structure with each flea species harboring unique bacterial lineages. The site (i.e. village), rodent host, flea sex, elevation, precipitation, and temperature also significantly affected bacterial community composition. Some bacterial lineages were widespread among flea species (e.g. Bartonella spp. and Wolbachia spp.), but each flea species also harbored unique bacterial lineages. Some of these lineages are not closely related to known bacterial diversity and likely represent newly discovered lineages of insect symbionts. Our finding that flea species has the greatest effect on bacterial community composition may help future investigations between Yersinia pestis and non-pathogenic flea-associated bacteria. Characterizing bacterial communities of fleas during a plague epizootic event in the future would be helpful.     

Prevalence and abundance of fleas in black-tailed prairie dog burrows: implications for the transmission of plague (Yersinia pestis)

Plague, the disease caused by the bacterium Yersinia pestis, can have devastating impacts on North American wildlife. Epizootics, or die-offs, in prairie dogs (Cynomys ludovicianus) occur sporadically and fleas (Siphonaptera) are probably important in the disease's transmission and possibly as maintenance hosts of Y. pestis between epizootics. We monitored changes in flea abundance in prairie dog burrows in response to precipitation, temperature, and plague activity in shortgrass steppe in northern Colorado. Oropsylla hirsuta was the most commonly found flea, and it increased in abundance with temperature. In contrast, Oropsylla tuberculata cynomuris declined with rising temperature. During plague epizootics, flea abundance in burrows increased and then subsequently declined after the extirpation of their prairie dog hosts.     

Modeling the epidemiological history of plague in Central Asia: Palaeoclimatic forcing on a disease system over the past millennium

Background

Human cases of plague (Yersinia pestis) infection originate, ultimately, in the bacterium's wildlife host populations. The epidemiological dynamics of the wildlife reservoir therefore determine the abundance, distribution and evolution of the pathogen, which in turn shape the frequency, distribution and virulence of human cases. Earlier studies have shown clear evidence of climatic forcing on contemporary plague abundance in rodents and humans.

Results

We find that high-resolution palaeoclimatic indices correlate with plague prevalence and population density in a major plague host species, the great gerbil (Rhombomys opimus), over 1949-1995. Climate-driven models trained on these data predict independent data on human plague cases in early 20th-century Kazakhstan from 1904-1948, suggesting a consistent impact of climate on large-scale wildlife reservoir dynamics influencing human epidemics. Extending the models further back in time, we also find correspondence between their predictions and qualitative records of plague epidemics over the past 1500 years.

Conclusions

Central Asian climate fluctuations appear to have had significant influences on regional human plague frequency in the first part of the 20th century, and probably over the past 1500 years. This first attempt at ecoepidemiological reconstruction of historical disease activity may shed some light on how long-term plague epidemiology interacts with human activity. As plague activity in Central Asia seems to have followed climate fluctuations over the past centuries, we may expect global warming to have an impact upon future plague epidemiology, probably sustaining or increasing plague activity in the region, at least in the rodent reservoirs, in the coming decades. See commentary: http://www.biomedcentral.com/1741-7007/8/108     

The role of the female Syrian hamster protein on the interaction between serum lipoproteins and heparin

We have previously shown the effect of phosphorylcholine-binding proteins from rat (PCBP) and rabbit (CRP) on the precipitation of serum lipoproteins by heparin in presence of Ca2+. The present paper describes the effect of a phosphorylcholine-binding protein from the female Syrian hamster (FP) on the lipoprotein precipitation reaction. The precipitation of lipoproteins by heparin was lower in assays using female hamster serum in which FP is a prominent protein, compared with assays with male serum in which FP is present in very low concentration. Depletion of FP from female serum resulted in increased lipoprotein precipitation. The addition of purified FP to assays using human very low density lipoprotein (VLDL) inhibited the precipitation reaction. The precipitation of lipoproteins was also examined using serum from male hamsters treated with diethylstilbestrol and female hamsters treated with testosterone, treatments known to modulate the levels of FP. Results indicate an inverse relationship between serum FP levels from normal and hormone-treated hamsters and the precipitation of lipoproteins from their serum. The partially desialylated FP when added to precipitation assays using human VLDL resulted in reduced inhibition of VLDL precipitation.     

Colorado animal‐based plague surveillance systems: relationships between targeted animal species and prediction efficacy of areas at risk for humans

Human plague risks (Yersinia pestis infection) are greatest when epizootics cause high mortality among this bacterium's natural rodent hosts. Therefore, health departments in plague‐endemic areas commonly establish animal‐based surveillance programs to monitor Y. pestis infection among plague hosts and vectors. The primary objectives of our study were to determine whether passive animal‐based plague surveillance samples collected in Colorado from 1991 to 2005 were sampled from high human plague risk areas and whether these samples provided information useful for predicting human plague case locations. By comparing locations of plague‐positive animal samples with a previously constructed GIS‐based plague risk model, we determined that the majority of plague‐positive Gunnison's prairie dogs (100%) and non‐prairie dog sciurids (85.82%), and moderately high percentages of sigmodontine rodents (71.4%), domestic cats (69.3%), coyotes (62.9%), and domestic dogs (62.5%) were recovered within 1 km of the nearest area posing high peridomestic risk to humans. In contrast, the majority of white‐tailed prairie dog (66.7%), leporid (cottontailed and jack rabbits) (71.4%), and black‐tailed prairie dog (93.0%) samples originated more than 1 km from the nearest human risk habitat. Plague‐positive animals or their fleas were rarely (one of 19 cases) collected within 2 km of a case exposure site during the 24 months preceding the dates of illness onset for these cases. Low spatial accuracy for identifying epizootic activity prior to human plague cases suggested that other mammalian species or their fleas are likely more important sources of human infection in high plague risk areas. To address this issue, epidemiological observations and multi‐locus variable number tandem repeat analyses (MLVA) were used to preliminarily identify chipmunks as an under‐sampled, but potentially important, species for human plague risk in Colorado.     

Ecology and geography of plague transmission areas in northeastern Brazil

Plague in Brazil is poorly known and now rarely seen, so studies of its ecology are difficult. We used ecological niche models of historical (1966-present) records of human plague cases across northeastern Brazil to assess hypotheses regarding environmental correlates of plague occurrences across the region. Results indicate that the apparently focal distribution of plague in northeastern Brazil is indeed discontinuous, and that the causes of the discontinuity are not necessarily only related to elevation-rather, a diversity of environmental dimensions correlate to presence of plague foci in the region. Perhaps most interesting is that suitable areas for plague show marked seasonal variation in photosynthetic mass, with peaks in April and May, suggesting links to particular land cover types. Next steps in this line of research will require more detailed and specific examination of reservoir ecology and natural history.     

The trophic responses of two different rodent–vector–plague systems to climate change

Plague, the causative agent of three devastating pandemics in history, is currently a re-emerging disease, probably due to climate change and other anthropogenic changes. Without understanding the response of plague systems to anthropogenic or climate changes in their trophic web, it is unfeasible to effectively predict years with high risks of plague outbreak, hampering our ability for effective prevention and control of the disease. Here, by using surveillance data, we apply structural equation modelling to reveal the drivers of plague prevalence in two very different rodent systems: those of the solitary Daurian ground squirrel and the social Mongolian gerbil. We show that plague prevalence in the Daurian ground squirrel is not detectably related to its trophic web, and that therefore surveillance efforts should focus on detecting plague directly in this ecosystem. On the other hand, plague in the Mongolian gerbil is strongly embedded in a complex, yet understandable trophic web of climate, vegetation, and rodent and flea densities, making the ecosystem suitable for more sophisticated low-cost surveillance practices, such as remote sensing. As for the trophic webs of the two rodent species, we find that increased vegetation is positively associated with higher temperatures and precipitation for both ecosystems. We furthermore find a positive association between vegetation and ground squirrel density, yet a negative association between vegetation and gerbil density. Our study thus shows how past surveillance records can be used to design and improve existing plague prevention and control measures, by tailoring them to individual plague foci. Such measures are indeed highly needed under present conditions with prevailing climate change.     

Structural validation of an individual-based model for plague epidemics simulation

Plague remains endemic in many countries in the world and Madagascar is currently the country where the highest number of human plague cases is reported every year. The investigation of causal factors, which command the disease dynamics in rodent populations, is a crucial step to forecast, control and anticipate the infection extension to humans. This paper presents simulation results obtained from an epidemic model, SIMPEST, designed to simulate bubonic plague in a rodent population at a high level of spatial and temporal resolution. We developed a structurally realistic individual-based model, mobilizing knowledge about fleas and rats behaviour, inter-individual plague transmission, and disease evolution in individual organisms, so that the model reflects the way the real system operates and to generate spatial and temporal patterns of disease spread. To assess the structural validity of our simulations, we perform sensitivity analyses on the initial population size and spatial distribution, and compare our results with theoretical statements, garnered from both previous modelling experiences and repeated field observations. We show our results are consistent with referents about population size conditions for a disease to invade and persist and the effect of the contact network on disease dynamics.     

Enzymatic inactivation of levomycetin and penicillin by cells of the plague and pseudotuberculosis microbes that contain R plasmid depending on cultivation conditions]

The activity of enzymes, inactivating levomycetin and penicillin in the cells of plague and pseudotuberculosis microbes bearing extrachromosomal determinants resistant to a number of antibiotics was studied as dependent on some cultivation parameters: population age, aeration rate and temperature. It was shown that the highest capacity for levomycetin acetylation was characteristic of the cells in the late logarithmic and early stationary growth phages. Accumulation of levomycetin O-acetothers in the incubation medium markedly increased, when the cells were grown under the conditions of intensive aeration. An increase in the cultivation temperature up to 37 degrees C was accompanied by a reliable decrease in the activity of levomycetin acetylase in the transconjugant plague and pseudotuberculosis microbes though no correlation with the resistance levels in the same strains to the above antibiotics was observed. Optimal conditions for penicillinase production were determined. The maximum levels of penicillinase were found in the cells of Y. pestis 556/106 Rn with the episotic resistance type in the early exponential developmental phase under the aeration conditions and the temperature of 28 degrees C.     

Climate-driven spatial dynamics of plague among prairie dog colonies

We present a Bayesian hierarchical model for the joint spatial dynamics of a host-parasite system. The model was fitted to long-term data on regional plague dynamics and metapopulation dynamics of the black-tailed prairie dog, a declining keystone species of North American prairies. The rate of plague transmission between colonies increases with increasing precipitation, while the rate of infection from unknown sources decreases in response to hot weather. The mean annual dispersal distance of plague is about 10 km, and topographic relief reduces the transmission rate. Larger colonies are more likely to become infected, but colony area does not affect the infectiousness of colonies. The results suggest that prairie dog movements do not drive the spread of plague through the landscape. Instead, prairie dogs are useful sentinels of plague epizootics. Simulations suggest that this model can be used for predicting long-term colony and plague dynamics as well as for identifying which colonies are most likely to become infected in a specific year.     

Effect of subinhibitory concentrations of antibiotics on catalase activity of plague microbes]

It was shown that the presence of subinhibitory concentrations of ampicillin, cefotaxime or gentamicin in the cultivation medium had a marked inhibitory effect on the catalase activity of plague microbe. The effect depended on the characteristic features of plague microbe strains and the incubation temperature. When the cells of a virulent strain of the plague microbe Y. pestis 1300 were cultivated at a temperature of 37 degrees C on a medium containing the subinhibitory concentrations of ampicillin or cefotaxime, the pathogen virulence for albino mice significantly decreased.     

Where Does Human Plague Still Persist in Latin America?

Background

Plague is an epidemic-prone disease with a potential impact on public health, international trade, and tourism. It may emerge and re-emerge after decades of epidemiological silence. Today, in Latin America, human cases and foci are present in Bolivia, Brazil, Ecuador, and Peru.

Aims

The objective of this study is to identify where cases of human plague still persist in Latin America and map areas that may be at risk for emergence or re-emergence. This analysis will provide evidence-based information for countries to prioritize areas for intervention.

Methods

Evidence of the presence of plague was demonstrated using existing official information from WHO, PAHO, and Ministries of Health. A geo-referenced database was created to map the historical presence of plague by country between the first registered case in 1899 and 2012. Areas where plague still persists were mapped at the second level of the political/administrative divisions (counties). Selected demographic, socioeconomic, and environmental variables were described.

Results

Plague was found to be present for one or more years in 14 out of 25 countries in Latin America (1899–2012). Foci persisted in six countries, two of which have no report of current cases. There is evidence that human cases of plague still persist in 18 counties. Demographic and poverty patterns were observed in 11/18 counties. Four types of biomes are most commonly found. 12/18 have an average altitude higher than 1,300 meters above sea level.

Discussion

Even though human plague cases are very localized, the risk is present, and unexpected outbreaks could occur. Countries need to make the final push to eliminate plague as a public health problem for the Americas. A further disaggregated risk evaluation is recommended, including identification of foci and possible interactions among areas where plague could emerge or re-emerge. A closer geographical approach and environmental characterization are suggested.     

Two Distinct Yersinia pestis Populations Causing Plague among Humans in the West Nile Region of Uganda

Background

Plague is a life-threatening disease caused by the bacterium, Yersinia pestis. Since the 1990s, Africa has accounted for the majority of reported human cases. In Uganda, plague cases occur in the West Nile region, near the border with Democratic Republic of Congo. Despite the ongoing risk of contracting plague in this region, little is known about Y. pestis genotypes causing human disease.

Methodology/Principal Findings

During January 2004–December 2012, 1,092 suspect human plague cases were recorded in the West Nile region of Uganda. Sixty-one cases were culture-confirmed. Recovered Y. pestis isolates were analyzed using three typing methods, single nucleotide polymorphisms (SNPs), pulsed field gel electrophoresis (PFGE), and multiple variable number of tandem repeat analysis (MLVA) and subpopulations analyzed in the context of associated geographic, temporal, and clinical data for source patients. All three methods separated the 61 isolates into two distinct 1.ANT lineages, which persisted throughout the 9 year period and were associated with differences in elevation and geographic distribution.

Conclusions/Significance

We demonstrate that human cases of plague in the West Nile region of Uganda are caused by two distinct 1.ANT genetic subpopulations. Notably, all three typing methods used, SNPs, PFGE, and MLVA, identified the two genetic subpopulations, despite recognizing different mutation types in the Y. pestis genome. The geographic and elevation differences between the two subpopulations is suggestive of their maintenance in highly localized enzootic cycles, potentially with differing vector-host community composition. This improved understanding of Y. pestis subpopulations in the West Nile region will be useful for identifying ecologic and environmental factors associated with elevated plague risk.     

The perils of climate change: In utero exposure to temperature variability and birth outcomes in the Andean region

The discussion on the effects of climate change on human activity has primarily focused on how increasing temperature levels can impair human health. However, less attention has been paid to the effect of increased climate variability on health. We investigate how in utero exposure to temperature variability, measured as the fluctuations relative to the historical local temperature mean, affects birth outcomes in the Andean region. Our results suggest that exposure to a temperate one standard deviation relative to the municipality’s long-term temperature mean during pregnancy reduces birth weight by 20 g. and increases the probability a child is born with low birth weight by a 0.7 percentage point. We also explore potential channels driving our results and find some evidence that increased temperature variability can lead to a decrease in health care and increased food insecurity during pregnancy.     

中国大中型陆栖哺乳动物地理区边界探测及其驱动因素

地理隔离是驱动物种空间分布格局形成的主要原因之一。利用我国大中型陆栖哺乳动物的地理分布数据,基于信息地图生物区(Infomap Bioregions)方法探测生物地理区域,提取对大中型陆栖哺乳动物类群的分布扩散产生阻隔效应的主要界线。从温度、降水和地形的梯度变化角度入手,应用空间自回归模型确定与生物地理区边界相关的主要驱动因子,构建地理加权逻辑回归(GWLR)模型分析各驱动因子重要性的空间非平稳性特征。结果表明,研究区域划分为3个主要的生物地理区,除年降水量变异系数与边界联系不明显外,其余变量均在10%及以下的显著性水平与生物地理区边界呈正相关,反映出生物地理区边界与气候突变、地形障碍和人类活动的协同作用有关。生物地理区1与生物地理区3的边界线的主导影响因子是人类足迹指数,生物地理区1和生物地理区2的边界线的主导影响因子是气温季节性变动系数变异系数,生物地理区2和生物地理区3边界线在祁连山脉一带的主导影响因子主要是气温季节性变动系数变异系数,其余地区为地形障碍。多类群物种对隔离屏障的响应模式难以统一,研究从大中型动物入手,通过识别以不同物种组合为特征的生物地理区域,揭示物种在空间上的分组方式,为探讨各动物类群的隔离机制提供空间模式和框架。     

Expected future plague levels in a wildlife host under different scenarios of climate change

We predicted future plague and black-tailed prairie dog dynamics in the North American prairies under different scenarios of climate change. A climate-driven model for the joint dynamic of the host–parasite system was used. Projections for the regional climate were obtained through empirical–statistical downscaling of global climate scenarios generated by an ensemble of global climate models for the recent Fourth Assessment Report by the IPCC. The study shows the uncertainties involved in predicting future regional climate and climate-driven population dynamics, but reveals that unchanged or lower levels of plague, leading to increased black-tailed prairie dog colonies, can be expected. Less plague is particularly expected for scenarios that assume the highest emission of greenhouse gases associated with the greatest projected future warming. Moreover, under high-emission scenarios, decreased probabilities of extremely high numbers of infected colonies are expected, along with decreased probabilities of extremely low total numbers of colonies. The assumed main underlying mechanism is an inhibiting effect of high temperatures on fleas (dispersal vector) and on flea-mediated transmission of the disease-causing bacterium. Our study highlights the importance of using dynamic ecological (here host–parasite) models together with ensembles of climate projections to investigate the responses of populations and parasites to a changed climate.     

Species richness,vegetation structure,and floristic composition of woody plants along the elevation gradient of Mt. Meru,Tanzania

Understanding the change in vegetation composition along elevational gradients is critical for species conservation in a changing world. We studied the species richness, tree height, and floristic composition of woody plants along an elevation gradient of protected habitats on the eastern slope of Mount Meru and analyzed how these vegetation variables are influenced by the interplay of temperature and precipitation. Vegetation data were collected on 44 plots systematically placed along five transects spanning an elevational gradient of 1600 to 3400 m a.s.l. We used ordinary linear models and multivariate analyses to test the effect of mean annual temperature and precipitation on woody plant species richness, tree height, and floristic composition. We found that species richness, mean tree height, and maximum tree height declined monotonically with elevation. Models that included only mean annual temperature as an explanatory variable were generally best supported to predict changes in species richness and tree height along the elevation gradient. We found significant changes in woody plant floristic composition with elevation, which were shaped by an interaction of mean annual temperature and precipitation. While plant communities consistently changed with temperature along the elevation gradient, levels of precipitation were more important for plant communities at lower than for those at higher elevations. Our study suggests that changes in temperature and precipitation regimes in the course of climate change will reshape elevational gradients of diversity, tree height, and correlated carbon storage in ecosystems, and the sequence of tree communities on East African mountains.     

古尔班通古特沙漠旱生植物时空分布特征

根据2000—2016年MODIS NDVI数据提取旱生植物的时空格局,并结合MODIS地表温度数据和TRMM降水数据,我们分析了古尔班通古特沙漠旱生植物的空间分布和变化特征。结果表明:(1) 2000—2016年间,古尔班通古特沙漠旱生植物覆盖的年际波动明显,但整体呈现缓慢上升趋势;(2)沙漠中旱生植物覆盖空间分布具有明显的地区差异性,位于南部靠近农田地区的覆盖最高,中东部地区次之,西北部最少;(3)古尔班通古特沙漠反映旱生植物长势的NDVI值与温度及降水呈现正相关,降水对NDVI的影响大于温度,并且NDVI与温度或降水之间存在明显的滞后效应,降水与NDVI之间的滞后效应更强。