Andres Garchitorena

Mycobacterium ulcerans Ecological Dynamics and Its Association with Freshwater Ecosystems and Aquatic Communities: Results from a 12-Month Environmental Survey in Cameroon

Background Mycobacterium ulcerans (MU) is the agent responsible for Buruli Ulcer (BU), an emerging skin disease with dramatic socioeconomic and health outcomes, especially in rural settings. BU emergence and distribution is linked to aquatic ecosystems in tropical and subtropical countries, especially to swampy and flooded areas. Aquatic animal organisms are likely to play a role either as host reservoirs or vectors of the bacilli. However, information on MU ecological dynamics, both in space and time, is dramatically lacking. As a result, the ecology of the disease agent, and consequently its mode of transmission, remains largely unknown, which jeopardizes public health attempts for its control. The objective of this study was to gain insight on MU environmental distribution and colonization of aquatic organisms through time. Methodology/Principal Findings Longitudinal sampling of 32 communities of aquatic macro-invertebrates and vertebrates was conducted from different environments in two BU endemic regions in Cameroon during 12 months. As a result, 238,496 individuals were classified and MU presence was assessed by qPCR in 3,084 sample-pools containing these aquatic organisms. Our study showed a broad distribution of MU in all ecosystems and taxonomic groups, with important regional differences in its occurrence. Colonization dynamics fluctuated along the year, with the highest peaks in August and October. The large variations observed in the colonization dynamics of different taxonomic groups and aquatic ecosystems suggest that the trends shown here are the result of complex ecological processes that need further investigation. Conclusion/Perspectives This is the largest field study on MU ecology to date, providing the first detailed description of its spatio-temporal dynamics in different aquatic ecosystems within BU endemic regions. We argue that coupling this data with fine-scale epidemiological data through statistical and mathematical models will provide a major step forward in the understanding of MU ecology and mode of transmission.

Ecological niche modelling of Hemipteran insects in Cameroon; the paradox of a vector-borne transmission for Mycobacterium ulcerans, the causative agent of Buruli ulcer

BackgroundThe mode of transmission of the emerging neglected disease Buruli ulcer is unknown. Several potential transmission pathways have been proposed, such as amoebae, or transmission through food webs. Several lines of evidence have suggested that biting aquatic insects, Naucoridae and Belostomatidae, may act as vectors, however this proposal remains controversial.Materials and methodsHerein, based on sampling in Cameroon, we construct an ecological niche model of these insects to describe their spatial distribution. We predict their distribution across West Africa, describe important environmental drivers of their abundance, and examine the correlation between their abundance and Buruli ulcer prevalence in the context of the Bradford-Hill guidelines.ResultsWe find a significant positive correlation between the abundance of the insects and the prevalence of Buruli ulcer. This correlation changes in space and time, it is significant in one Camerounese study region in (Akonolinga) and not other (Bankim). We discuss notable environmental differences between these regions.ConclusionWe interpret the presence of, and change in, this correlation as evidence (though not proof) that these insects may be locally important in the environmental persistence, or transmission, of Mycobacterium. ulcerans. This is consistent with the idea of M. ulcerans as a pathogen transmitted by multiple modes of infection, the importance of any one pathway changing from region to region, depending on the local environmental conditions.

Seasonal Patterns of Buruli Ulcer Incidence, Central Africa, 2002-2012.

To determine when risk for Buruli ulcer is highest, we examined seasonal patterns in a highly disease-endemic area of Cameroon during 2002–2012. Cases peaked in March, suggesting that risk is highest during the high rainy season. During and after this season, populations should increase protective behaviors, and case detection efforts should be intensified.

Topography and land cover of watersheds predicts the distribution of the environmental pathogen Mycobacterium ulcerans in aquatic insects.

Background An understanding of the factors driving the distribution of pathogens is useful in preventing disease. Often we achieve this understanding at a local microhabitat scale; however the larger scale processes are often neglected. This can result in misleading inferences about the distribution of the pathogen, inhibiting our ability to manage the disease. One such disease is Buruli ulcer, an emerging neglected tropical disease afflicting many thousands in Africa, caused by the environmental pathogen Mycobacterium ulcerans. Herein, we aim to describe the larger scale landscape process describing the distribution of M. ulcerans. Methodology Following extensive sampling of the community of aquatic macroinvertebrates in Cameroon, we select the 5 dominant insect Orders, and conduct an ecological niche model to describe how the distribution of M. ulcerans positive insects changes according to land cover and topography. We then explore the generalizability of the results by testing them against an independent dataset collected in a second endemic region, French Guiana. Principal Findings We find that the distribution of the bacterium in Cameroon is accurately described by the land cover and topography of the watershed, that there are notable seasonal differences in distribution, and that the Cameroon model does not predict the distribution of M. ulcerans in French Guiana. Conclusions/Significance Future studies of M. ulcerans would benefit from consideration of local structure of the local stream network in future sampling, and further work is needed on the reasons for notable differences in the distribution of this species from one region to another. This work represents a first step in the identification of large-scale environmental drivers of this species, for the purposes of disease risk mapping.

Environmental transmission of Mycobacterium ulcerans drives dynamics of Buruli ulcer in endemic regions of Cameroon

Buruli Ulcer is a devastating skin disease caused by the pathogen Mycobacterium ulcerans. Emergence and distribution of Buruli ulcer cases is clearly linked to aquatic ecosystems, but the specific route of transmission of M. ulcerans to humans remains unclear. Relying on the most detailed field data in space and time on M. ulcerans and Buruli ulcer available today, we assess the relative contribution of two potential transmission routes –environmental and water bug transmission– to the dynamics of Buruli ulcer in two endemic regions of Cameroon. The temporal dynamics of Buruli ulcer incidence are explained by estimating rates of different routes of transmission in mathematical models. Independently, we also estimate statistical models of the different transmission pathways on the spatial distribution of Buruli ulcer. The results of these two independent approaches are corroborative and suggest that environmental transmission pathways explain the temporal and spatial patterns of Buruli ulcer in our endemic areas better than the water bug transmission.

The Burden of Livestock Parasites on the Poor

Parasitic diseases of humans and livestock are ubiquitous in the developing world and have substantial impacts on human wellbeing. For the estimated one billion people living in poverty who rely on livestock for their livelihoods, parasites steal valuable nutritional resources through multiple pathways. This diversion of nutrients ultimately contributes to chronic malnutrition, greater human disease burdens, and decreased productivity of both humans and livestock.

Disease ecology, health and the environment: A framework to account for ecological and socio-economic drivers in the control of neglected tropical diseases

Reducing the burden of neglected tropical diseases (NTDs) is one of the key strategic targets advanced by the Sustainable Development Goals. Despite the unprecedented effort deployed for NTD elimination in the past decade, their control, mainly through drug administration, remains particularly challenging: persistent poverty and repeated exposure to pathogens embedded in the environment limit the efficacy of strategies focused exclusively on human treatment or medical care. Here, we present a simple modelling framework to illustrate the relative role of ecological and socio-economic drivers of environmentally transmitted parasites and pathogens. Through the analysis of system dynamics, we show that periodic drug treatments that lead to the elimination of directly transmitted diseases may fail to do so in the case of human pathogens with an environmental reservoir. Control of environmentally transmitted diseases can be more effective when human treatment is complemented with interventions targeting the environmental reservoir of the pathogen. We present mechanisms through which the environment can influence the dynamics of poverty via disease feedbacks. For illustration, we present the case studies of Buruli ulcer and schistosomiasis, two devastating waterborne NTDs for which control is particularly challenging. This article is part of the themed issue ‘Conservation, biodiversity and infectious disease: scientific evidence and policy implications’.

Baseline population health conditions ahead of a health system strengthening program in rural Madagascar

ABSTRACT Background: A model health district was initiated through a program of health system strengthening (HSS) in Ifanadiana District of southeastern Madagascar in 2014. We report population health indicators prior to initiation of the program. Methods: A representative household survey based on the Demographic Health Survey was conducted using a two-stage cluster sampling design in two strata – the initial program catchment area and the future catchment area. Chi-squared and t-tests were used to compare data by stratum, using appropriate sampling weights. Madagascar data for comparison were taken from a 2013 national study. Results: 1522 households were surveyed, representing 8310 individuals including 1635 women ages 15–49, 1685 men ages 15–59 and 1251 children under age 5. Maternal mortality rates in the district are 1044/100,000. 81% of women’s last childbirth deliveries were in the home; only 20% of deliveries were attended by a doctor or nurse/midwife (not different by stratum). 9.3% of women had their first birth by age 15, and 29.5% by age 18. Under-5 mortality rate is high: 145/1000 live births vs. 62/1000 nationally. 34.6% of children received all recommended vaccines by age 12 months (compared to 51.5% in Madagascar overall). In the 2 weeks prior to interview, approximately 28% of children under age 5 had acute respiratory infections of whom 34.7% were taken for care, and 14% of children had diarrhea of whom 56.6% were taken for care. Under-5 mortality, illness, care-seeking and vaccination rates were not significantly different between strata. Conclusions: Indicators of population health and health care-seeking reveal low use of the formal health system, which could benefit from HSS. Data from this survey and from a longitudinal follow-up study will be used to target needed interventions, to assess change in the district and the impact of HSS on individual households and the population of the district.

Economic inequality caused by feedbacks between poverty and the dynamics of a rare tropical disease: the case of Buruli ulcer in sub-Saharan Africa

Neglected tropical diseases (NTDs) have received increasing attention in recent years by the global heath community, as they cumulatively constitute substantial burdens of disease as well as barriers for economic development. A number of common tropical diseases such as malaria, hookworm or schistosomiasis have well-documented economic impacts. However, much less is known about the population-level impacts of diseases that are rare but associated with high disability burden, which represent a great number of tropical diseases. Using an individual-based model of Buruli ulcer (BU), we demonstrate that, through feedbacks between health and economic status, such NTDs can have a significant impact on the economic structure of human populations even at low incidence levels. While average wealth is only marginally affected by BU, the economic conditions of certain subpopulations are impacted sufficiently to create changes in measurable population-level inequality. A reduction of the disability burden caused by BU can thus maximize the economic growth of the poorest subpopulations and reduce significantly the economic inequalities introduced by the disease in endemic regions.

Modeling the burden of poultry disease on the rural poor in Madagascar

Livestock represent a fundamental economic and nutritional resource for many households in the developing world; however, a high burden of infectious disease limits their production potential. Here we present an ecological framework for estimating the burden of poultry disease based on coupled models of infectious disease and economics. The framework is novel, as it values humans and livestock as co-contributors to household wellbeing, incorporating feedbacks between poultry production and human capital in disease burden estimates. We parameterize this coupled ecological–economic model with household-level data to provide an estimate of the overall burden of poultry disease for the Ifanadiana District in Madagascar, where over 72% of households rely on poultry for economic and food security. Our models indicate that households may lose 10–25% of their monthly income under current disease conditions. Results suggest that advancements in poultry health may serve to support income generation through improvements in both human and animal health.