Cholera Outbreak in Senegal in 2005: Was Climate a Factor?

Cholera is an acute diarrheal illness caused by Vibrio cholerae and occurs as widespread epidemics in Africa. In 2005, there were 31,719 cholera cases, with 458 deaths in the Republic of Senegal. We retrospectively investigated the climate origin of the devastating floods in mid-August 2005, in the Dakar Region of Senegal and the subsequent outbreak of cholera along with the pattern of cholera outbreaks in three other regions of that country. We compared rainfall patterns between 2002 and 2005 and the relationship between the sea surface temperature (SST) gradient in the tropical Atlantic Ocean and precipitation over Senegal for 2005. Results showed a specific pattern of rainfall throughout the Dakar region during August, 2005, and the associated rainfall anomaly coincided with an exacerbation of the cholera epidemic. Comparison of rainfall and epidemiological patterns revealed that the temporal dynamics of precipitation, which was abrupt and heavy, was presumably the determining factor. Analysis of the SST gradient showed that the Atlantic Ocean SST variability in 2005 differed from that of 2002 to 2004, a result of a prominent Atlantic meridional mode. The influence of this intense precipitation on cholera transmission over a densely populated and crowded region was detectable for both Dakar and Thiès, Senegal. Thus, high resolution rainfall forecasts at subseasonal time scales should provide a way forward for an early warning system in Africa for cholera and, thereby, trigger epidemic preparedness. Clearly, attention must be paid to both natural and human induced environmental factors to devise appropriate action to prevent cholera and other waterborne disease epidemics in the region.     

Cholera and climate: revisiting the quantitative evidence

Cholera dynamics in endemic regions display regular seasonal cycles and pronounced interannual variability. We review here the current quantitative evidence for the influence of climate on cholera dynamics with reference to the early literature on the subject. We also briefly review the incipient status of mathematical models for cholera and argue that these models are important for understanding climatic influences in the context of the population dynamics of the disease. A better understanding of disease risk related to the environment should further underscore the need for changing the socioeconomic conditions conducive to cholera.     

Cholera and Shigellosis: Different Epidemiology but Similar Responses to Climate Variability

Background

Comparative studies of the associations between different infectious diseases and climate variability, such as the El Niño-Southern Oscillation, are lacking. Diarrheal illnesses, particularly cholera and shigellosis, provide an important opportunity to apply a comparative approach. Cholera and shigellosis have significant global mortality and morbidity burden, pronounced differences in transmission pathways and pathogen ecologies, and there is an established climate link with cholera. In particular, the specific ecology of Vibrio cholerae is often invoked to explain the sensitivity of that disease to climate.

Methods and Findings

The extensive surveillance data of the International Center for Diarrheal Disease Research, Bangladesh are used here to revisit the known associations between cholera and climate, and to address their similarity to previously unexplored patterns for shigellosis. Monthly case data for both the city of Dhaka and a rural area known as Matlab are analyzed with respect to their association with El Niño and flooding. Linear correlations are examined between flooding and cumulative cases, as well as for flooding and El Niño. Rank-correlation maps are also computed between disease cases in the post-monsoon epidemic season and sea surface temperatures in the Pacific. Similar climate associations are found for both diseases and both locations. Increased cases follow increased monsoon flooding and increased sea surface temperatures in the preceding winter corresponding to an El Niño event.

Conclusions

The similarity in association patterns suggests a systemic breakdown in population health with changing environmental conditions, in which climate variability acts primarily through increasing the exposure risk of the human population. We discuss these results in the context of the on-going debate on the relative importance of the environmental reservoir vs. secondary transmission, as well as the implications for the use of El Niño as an early indicator of flooding and enteric disease risk.     

Pathogen adaptation to seasonal forcing and climate change

Many diverse infectious diseases exhibit seasonal dynamics. Seasonality in disease incidence has been attributed to seasonal changes in pathogen transmission rates, resulting from fluctuations in extrinsic climate factors. Multi-strain infectious diseases with strain-specific seasonal signatures, such as cholera, indicate that a range of seasonal patterns in transmission rates is possible in identical environments. We therefore consider pathogens capable of evolving their 'seasonal phenotype', a trait that determines the sensitivity of their transmission rates to environmental variability. We introduce a theoretical framework, based on adaptive dynamics, for predicting the evolution of disease dynamics in seasonal environments. Changes in the seasonality of environmental factors are one important avenue for the effects of climate change on disease. This model also provides a framework for examining these effects on pathogen evolution and associated disease dynamics. An application of this approach gives an explanation for the recent cholera strain replacement in Bangladesh, based on changes in monsoon rainfall patterns.     

Fossil mammals and paleoenvironments in the Omo-Turkana Basin

Although best known for its fossil hominins, the Omo-Turkana Basin of Kenya and Ethiopia is the source of one of the best records of vertebrate evolution from the Late Cenozoic of Africa. Located near the heart of the East African Rift Valley, the basin serves as an important frame of reference for the continent. The fossil record from this region plays a key role in our efforts to understand the environmental and ecological context of human evolution in Africa. The Omo-Turkana faunal data shed light on key questions of human evolution: What kinds of environments did early humans inhabit? How did these environments change over time? What is the relationship between faunal change in East Africa and broader patterns of climatic change?     

Predicting the current and future potential distributions of lymphatic filariasis in Africa using maximum entropy ecological niche modelling

Modelling the spatial distributions of human parasite species is crucial to understanding the environmental determinants of infection as well as for guiding the planning of control programmes. Here, we use ecological niche modelling to map the current potential distribution of the macroparasitic disease, lymphatic filariasis (LF), in Africa, and to estimate how future changes in climate and population could affect its spread and burden across the continent. We used 508 community-specific infection presence data collated from the published literature in conjunction with five predictive environmental/climatic and demographic variables, and a maximum entropy niche modelling method to construct the first ecological niche maps describing potential distribution and burden of LF in Africa. We also ran the best-fit model against climate projections made by the HADCM3 and CCCMA models for 2050 under A2a and B2a scenarios to simulate the likely distribution of LF under future climate and population changes. We predict a broad geographic distribution of LF in Africa extending from the west to the east across the middle region of the continent, with high probabilities of occurrence in the Western Africa compared to large areas of medium probability interspersed with smaller areas of high probability in Central and Eastern Africa and in Madagascar. We uncovered complex relationships between predictor ecological niche variables and the probability of LF occurrence. We show for the first time that predicted climate change and population growth will expand both the range and risk of LF infection (and ultimately disease) in an endemic region. We estimate that populations at risk to LF may range from 543 and 804 million currently, and that this could rise to between 1.65 to 1.86 billion in the future depending on the climate scenario used and thresholds applied to signify infection presence.     

Satellite Based Assessment of Hydroclimatic Conditions Related to Cholera in Zimbabwe

Introduction

Cholera, an infectious diarrheal disease, has been shown to be associated with large scale hydroclimatic processes. The sudden and sporadic occurrence of epidemic cholera is linked with high mortality rates, in part, due to uncertainty in timing and location of outbreaks. Improved understanding of the relationship between pathogenic abundance and climatic processes allows prediction of disease outbreak to be an achievable goal. In this study, we show association of large scale hydroclimatic processes with the cholera epidemic in Zimbabwe reported to have begun in Chitungwiza, a city in Mashonaland East province, in August, 2008.

Principal Findings

Climatic factors in the region were found to be associated with triggering cholera outbreak and are shown to be related to anomalies of temperature and precipitation, validating the hypothesis that poor conditions of sanitation, coupled with elevated temperatures, and followed by heavy rainfall can initiate outbreaks of cholera. Spatial estimation by satellite of precipitation and global gridded air temperature captured sensitivities in hydroclimatic conditions that permitted identification of the location in the region where the disease outbreak began.

Discussion

Satellite derived hydroclimatic processes can be used to capture environmental conditions related to epidemic cholera, as occurred in Zimbabwe, thereby providing an early warning system. Since cholera cannot be eradicated because the causative agent, Vibrio cholerae, is autochthonous to the aquatic environment, prediction of conditions favorable for its growth and estimation of risks of triggering the disease in a given population can be used to alert responders, potentially decreasing infection and saving lives.     

Global microbial ecology: biogeography and diversity of Vibrios as a model

An environmental source of cholera was hypothesized as early as the late nineteenth century by Robert Koch, but not proven because of the ability of Vibrio cholera, the causative agent of cholera, to enter a dormant phase between epidemics. Standard bacteriological procedures for isolation of the vibrios from the environmental samples, including water, between epidemics generally were unsuccessful. Vibrio cholera, a marine vibrio requiring salt for growth, enters into a dormant 'viable but non-culturable' stage when conditions are unfavourable for growth and reproduction. The association of V. cholera with plankton, notably copepods, provides evidence for the environmental origin of cholera, as well as an explanation for the sporadic and erratic nature of cholera epidemics. Thus, the association of V. cholera with plankton was established only recently, allowing analysis of epidemic patterns of cholera, especially in those countries where cholera is endemic. The sporadic and erratic nature of cholera epidemics can now be related to climate and climate events, such as El Ni?o. Since zooplankton have been shown to harbour the bacterium and zooplankton blooms follow phytoplankton blooms, remote sensing can be employed to determine the relationship of cases of cholera with chlorophyll, as well as sea surface temperature (SST), ocean height, and turbidity. Cholera occurs seasonally in Bangladesh with two annual peaks in the number of cases occurring each year. From the data obtained and analysed to date, when the height of the ocean is high and sea surface temperature is also elevated, cholera cases are numerous. When the height is low and sea surface temperature is also low, little or no cholera is recorded. From the examination of data for the 1992-1993 cholera epidemic in India, preliminary comparisons of cholera data for Calcutta show a similar relationship between cholera cases, ocean height and SST. In conclusion, from results of studies of SST, phytoplankton and zooplankton, and their relationships to incidence of cholera, correlation of selected climatological factors and incidence of V. cholera appears to be significant, bringing the potential of predicting conditions conducive to cholera outbreaks closer to reality.     

Impact of Climate Variability on Infectious Disease in West Africa

The importance of infectious disease as a determinant (as well as an outcome) of poverty has recently become a prominent argument for international and national investment in the control of infectious disease, as can be seen in the recently articulated United Nations (UN) Millennium Development Goals (MDGs). Climate variability and land use change have an enormous impact on health in West Africa, and may yet undermine the potential for achieving the MDGs, in certain economic-ecological zones. However, their underlying role in determining the burden of disease in the region on a yearly or decadal basis has never been systematically studied. In order to improve our understanding of the future impacts of climate change, it may be more effective to start by investigating the impact of inter-annual climate variability, and short-term shifts in climate (e.g., decadal), on disease transmission dynamics. This information may inform both current and future policy decisions with regard to prediction, prevention, and management of adverse climate-related health outcomes. This article reviews current knowledge of changes in the epidemiology of infectious diseases associated with climate variability in West Africa over the last 40 years. Selected examples are considered from bacterial (meningococcal meningitis), protozoan (malaria), and filarial (onchocerciasis and lymphatic filariasis) infections where spatial and temporal disease patterns have been directly influenced by seasonal, inter-annual, or decadal changes in climate.The views expressed herein are those of the authors and do not necessarily reflect the views of the National Oceanic and Atmospheric Administration (NOAA) or any of its sub-agencies.     

Malaria epidemic expected in Mozambique

Health experts fear epidemics of several infectious diseases in Mozambique as floods recede and mosquitoes begin breeding. According to Pierre Kahozi of WHO, malaria is already endemic in the region but there are fears that a much greater outbreak might occur. Scores of suspected cases of cholera were reported and more are expected, along with cases of other diarrheal conditions. Neil Cameron, chief director of communicable diseases at the health department in South Africa, said that more cases are expected within a month when the breeding cycle of mosquitoes is renewed. He reported that the number of malaria cases in South Africa increased from 12,000 in 1995 to 50,000 in 1999, and a number of people had been dying from this disease. The increase could be attributed partly to climatic changes and resistance to certain drugs. DDT had been used in the past to control mosquitoes, and it?s possible that it will be used again in Mozambique. The issues involved in tackling malaria are now being considered as part of a special development initiative on infectious diseases that is being undertaken jointly by the health departments of three countries: South Africa, Mozambique, and Swaziland.     

Occurrence of Vibrio cholerae in Municipal and Natural Waters and Incidence of Cholera in Azerbaijan

Cholera, a waterborne disease caused by Vibrio cholerae, is an autochthonous member of the aquatic environment and predominantly reported from developing countries. Technical reports and proceedings were reviewed to determine the relationship between occurrence of V. cholerae in natural waters, including sources of municipal water, and cases of cholera in Azerbaijan. Water samples collected from different environmental sources from 1970 to 1998 were tested for V. cholerae and 0.73% (864/117,893) were positive. The results showed that in April of each year, when the air temperature rose by approximately 5°C, V. cholerae could be isolated. With each increase in air temperature, 6-8 weeks after, impact on cases of cholera was recorded. The incidence of cholera peaked when the air temperature reached >25°C during the month of September. It is concluded that a distinct seasonality in cholera incidence exists in Azerbaijan, with increased occurrence during warmer months.     

Relationship between Distinct African Cholera Epidemics Revealed via MLVA Haplotyping of 337 Vibrio cholerae Isolates

BackgroundSince cholera appeared in Africa during the 1970s, cases have been reported on the continent every year. In Sub-Saharan Africa, cholera outbreaks primarily cluster at certain hotspots including the African Great Lakes Region and West Africa.Conclusions/SignificanceTo effectively combat the disease, it is critical to understand the mechanisms of cholera emergence and diffusion in a region-specific manner. Overall, these findings demonstrate the relationship between distinct epidemics in West Africa and the African Great Lakes Region. This study also highlights the importance of monitoring and analyzing Vibrio cholerae isolates.     

Eltor cholera in Latin America

Cholera epidemics in South and Central America in the period 1991-1999 are characterized. The mechanisms of existence of Vibrio eltor in environmental objects have been substantiated. The causes and conditions of endemic foci formation which determine the infection spread not only within the countries of the subcontinent, but also far beyond its borders are shown. The effectiveness of cholera control interventions is evaluated.     

Astronomically forced climate change in the Kenyan Rift Valley 2.7-2.55 Ma: implications for the evolution of early hominin ecosystems

Global climate change, linked to astronomical forcing factors, has been implicated in faunal evolutionary change in equatorial Africa, including the origin and diversification of hominin lineages. Empirical terrestrial data demonstrating that orbital forcing has a significant effect, or is detectable, at early hominin sites in equatorial continental interiors during the Pliocene, however, remain limited. Sedimentation patterns in the Baringo Basin within the Central Kenyan Rift Valley between ca. 2.7 and 2.55 Ma, controlled by climatic factors, provide a detailed paleoenvironmental record spanning 35 fossil vertebrate localities, including three hominin sites. The succession includes a sequence of diatomites that record rhythmic cycling of major freshwater lake systems consistent with approximately 23-kyr Milankovitch precessional periodicity. The temporal framework of shifting precipitation patterns, relative to Pliocene insolation curves, implicate African monsoonal climatic control and indicate that climatic fluctuations in Rift Valley ecosystems were paced by global climatic change documented in marine cores. These data provide direct evidence of orbitally mediated environmental change at Pliocene Rift Valley hominin fossil localities, providing a unique opportunity to assess the evolutionary effect of short-term climatic flux on late Pliocene East African terrestrial communities.     

The Role of Socioeconomic Status in Longitudinal Trends of Cholera in Matlab,Bangladesh, 1993–2007

There has been little evidence of a decline in the global burden of cholera in recent years as the number of cholera cases reported to WHO continues to rise. Cholera remains a global threat to public health and a key indicator of lack of socioeconomic development. Overall socioeconomic development is the ultimate solution for control of cholera as evidenced in developed countries. However, most research has focused on cross-county comparisons so that the role of individual- or small area-level socioeconomic status (SES) in cholera dynamics has not been carefully studied. Reported cases of cholera in Matlab, Bangladesh have fluctuated greatly over time and epidemic outbreaks of cholera continue, most recently with the introduction of a new serotype into the region. The wealth of longitudinal data on the population of Matlab provides a unique opportunity to explore the impact of socioeconomic status and other demographic characteristics on the long-term temporal dynamics of cholera in the region. In this population-based study we examine which factors impact the initial number of cholera cases in a bari at the beginning of the 0139 epidemic and the factors impacting the number of cases over time. Cholera data were derived from the ICDDR,B health records and linked to socioeconomic and geographic data collected as part of the Matlab Health and Demographic Surveillance System. Longitudinal zero-inflated Poisson (ZIP) multilevel regression models are used to examine the impact of environmental and socio-demographic factors on cholera counts across baris. Results indicate that baris with a high socioeconomic status had lower initial rates of cholera at the beginning of the 0139 epidemic (γ₀₁ = −0.147, p = 0.041) and a higher probability of reporting no cholera cases (α₀₁ = 0.156, p = 0.061). Populations in baris characterized by low SES are more likely to experience higher cholera morbidity at the beginning of an epidemic than populations in high SES baris.     

Rapoport effect and biomic specialization in African mammals: revisiting the climatic variability hypothesis

Aim One of the mechanisms proposed to explain the tendency for geographical range size to increase from the equator to the poles, known as the Rapoport effect, is the climatic variability hypothesis. It states that, towards higher latitudes, greater seasonal climatic variability is the most important pressure that selectively promotes greater general climatic tolerance of species, and therefore also more extensive species ranges. In order to test this hypothesis, we explore the influence of climate, area and biome diversity on the latitudinal gradient of climatic specialization. Location The study used the large mammal assemblage from Africa. Methods The degree of climatic specialization of African large mammals (Primates, Carnivora, Proboscidea, Perissodactyla, Hyracoidea, Tubulidentata, Artiodactyla and Pholidota) is investigated using the biomic specialization index (BSI) for each mammal species, based on the number of biomes it inhabits. We studied the influence of 11 climatic and biogeographical predictors in the latitudinal pattern of biomic specialization. Stepwise multiple regressions were used to identify the strongest predictors of biomic specialization in Africa and, separately, in both continental hemispheres. We also studied differences among taxonomical groups (primates, carnivores and artiodactyls). We used correlograms generated using Moran's I coefficients to control for spatial autocorrelation in all these analyses. Results Average BSI values for successive 1°‐latitude bands generally decline towards the equator and temperature variability emerged as the most predictive factor in the regression model for the whole continent, thus supporting the climatic variability hypothesis. Nevertheless, there are differences between hemispheres and among taxa. While temperature variability is the most important predictor of latitudinal variability in biomic specialization in most of the regression models for the northern hemisphere, continental area for each latitudinal band is the best predictor in all the regression models in the southern hemisphere. Main conclusions It appears that similar patterns in latitudinal variation in average BSI may be caused by different factors in the two hemispheres. We suggest that the strong north–south geographical asymmetry of Africa, which influences its biogeographical structure, and the presence of land connections with Eurasia in the northern hemisphere are responsible for the observed patterns. Our data illustrate the influence of continental biogeographical structure and history on macroecological patterns.     

European rabbit survival and recruitment are linked to epidemiological and environmental conditions in their exotic range

The European rabbit, Oryctolagus cuniculus, is threatened within its native range, yet it is a highly successful colonizing pest species across its worldwide introduced range, causing large economic losses and widespread environmental degradation. To date, there has been no long‐term empirical evidence documenting the relative roles of climatic, epidemiological and biological factors in limiting life‐history determinants of rabbit range and abundance. Using 12 years of capture–mark–recapture data from their exotic range in Australia, we constructed candidate Cormack–Jolly–Seber models to test the influence of environmental, competition and disease conditions on rabbit survival and recruitment. Our results show that: (i) population‐level disease infection rate has the largest overall impact on rabbit survival, explaining 80% of variance in survival rates; (ii) environmental as well as epidemiological conditions constrain rabbit survival, especially for younger animals; (iii) temporal variation in rabbit kitten recruitment patterns are best described by a combination of climate, competition and disease settings (accounting for 68% of variance), while temperature alone has a strong negative influence on kitten recruitment; and (iv) recruitment responds positively to rabbit haemorrhagic disease, but negatively to myxomatosis – the former, probably being mediated through a disease driven effect on intraspecific competition for food. A strengthened understanding of climate change impacts on rabbit range and abundance can be achieved by accounting explicitly for potential synergisms between disease dynamics and climate. In this analysis, we provide the first step towards such an attempt for this important mammal species. Integrated approaches of this kind are essential for future forecasts of rabbit range and abundance, offsetting the conservation threat faced by O. cuniculus in its native range, and achieving effective management in exotic habitats.     

The Role of China in the Global Spread of the Current Cholera Pandemic

Epidemics and pandemics of cholera, a severe diarrheal disease, have occurred since the early 19th century and waves of epidemic disease continue today. Cholera epidemics are caused by individual, genetically monomorphic lineages of Vibrio cholerae: the ongoing seventh pandemic, which has spread globally since 1961, is associated with lineage L2 of biotype El Tor. Previous genomic studies of the epidemiology of the seventh pandemic identified three successive sub-lineages within L2, designated waves 1 to 3, which spread globally from the Bay of Bengal on multiple occasions. However, these studies did not include samples from China, which also experienced multiple epidemics of cholera in recent decades. We sequenced the genomes of 71 strains isolated in China between 1961 and 2010, as well as eight from other sources, and compared them with 181 published genomes. The results indicated that outbreaks in China between 1960 and 1990 were associated with wave 1 whereas later outbreaks were associated with wave 2. However, the previously defined waves overlapped temporally, and are an inadequate representation of the shape of the global genealogy. We therefore suggest replacing them by a series of tightly delineated clades. Between 1960 and 1990 multiple such clades were imported into China, underwent further microevolution there and then spread to other countries. China was thus both a sink and source during the pandemic spread of V. cholerae, and needs to be included in reconstructions of the global patterns of spread of cholera.     

Evaluating Spatial Interaction Models for Regional Mobility in Sub-Saharan Africa

Simple spatial interaction models of human mobility based on physical laws have been used extensively in the social, biological, and physical sciences, and in the study of the human dynamics underlying the spread of disease. Recent analyses of commuting patterns and travel behavior in high-income countries have led to the suggestion that these models are highly generalizable, and as a result, gravity and radiation models have become standard tools for describing population mobility dynamics for infectious disease epidemiology. Communities in Sub-Saharan Africa may not conform to these models, however; physical accessibility, availability of transport, and cost of travel between locations may be variable and severely constrained compared to high-income settings, informal labor movements rather than regular commuting patterns are often the norm, and the rise of mega-cities across the continent has important implications for travel between rural and urban areas. Here, we first review how infectious disease frameworks incorporate human mobility on different spatial scales and use anonymous mobile phone data from nearly 15 million individuals to analyze the spatiotemporal dynamics of the Kenyan population. We find that gravity and radiation models fail in systematic ways to capture human mobility measured by mobile phones; both severely overestimate the spatial spread of travel and perform poorly in rural areas, but each exhibits different characteristic patterns of failure with respect to routes and volumes of travel. Thus, infectious disease frameworks that rely on spatial interaction models are likely to misrepresent population dynamics important for the spread of disease in many African populations.