I am a disease ecologist and veterinarian at Stanford University's Hopkins Marine Station and an Associate Fellow at Stanford's Center for Innovation in Global Health. I am interested in environmental drivers of infectious disease and creative solutions to protect the health of people and the planet.
Current projects include:
Dams and disease: win-win ecological solutions to reduce human schistosomiasis burdens and restore fisheries
Environmentally mediated disease transmission: novel technologies for environmental diagnostics and ecological interventions to achieve disease control
Interlinkages among human health and ecosystem integrity: Sustainable Development Goal (SDG) 3 'human health and wellbeing,' and SDGs 14 and 15 'Life on land and below water.'
As Executive Director of Stanford's new Program for Disease Ecology, Health and the Environment, I am helping to build a growing interdisciplinary community at Stanford and beyond interested in discovering and promoting ecological solutions to disease that lead to improved human health and a more sustainable use of the natural environment. As part of this new research program, I founded The Upstream Alliance: a research initiative joining partners across the globe for ecological solutions to reduce the parasitic disease: schistosomiasis, which affects more than 250 million people worldwide.
Senior Research Scientist, Stanford Woods Institute for the Environment
Associate Fellow, Center for Innovation in Global Health (2015 - Present)
PhD, University of California Davis, Disease ecology (2008)
DVM, University of California Davis, Clinical veterinary medicine (2003)
Cost-effectiveness of combining drug and environmental treatments for environmentally transmitted diseases.
Proceedings. Biological sciences
2020; 287 (1933): 20200966
Control of neglected tropical diseases (NTDs) via mass drug administration (MDA) has increased considerably over the past decade, but strategies focused exclusively on human treatment show limited efficacy. This paper investigated trade-offs between drug and environmental treatments in the fight against NTDs by using schistosomiasis as a case study. We use optimal control techniques where the planner's objective is to treat the disease over a time horizon at the lowest possible total cost, where the total costs include treatment, transportation and damages (reduction in human health). We show that combining environmental treatments and drug treatments reduces the dependency on MDAs and that this reduction increases when the planners take a longer-run perspective on the fight to reduce NTDs. Our results suggest that NTDs with environmental reservoirs require moving away from a reliance solely on MDA to integrated treatment involving investment in both drug and environmental controls.
View details for DOI 10.1098/rspb.2020.0966
View details for PubMedID 32842925
Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis.
PLoS neglected tropical diseases
2020; 14 (7): e0008417
BACKGROUND: Schistosomiasis is responsible for the second highest burden of disease among neglected tropical diseases globally, with over 90 percent of cases occurring in African regions where drugs to treat the disease are only sporadically available. Additionally, human re-infection after treatment can be a problem where there are high numbers of infected snails in the environment. Recent experiments indicate that aquatic factors, including plants, nutrients, or predators, can influence snail abundance and parasite production within infected snails, both components of human risk. This study investigated how snail host abundance and release of cercariae (the free swimming stage infective to humans) varies at water access sites in an endemic region in Senegal, a setting where human schistosomiasis prevalence is among the highest globally.METHODS/PRINCIPAL FINDINGS: We collected snail intermediate hosts at 15 random points stratified by three habitat types at 36 water access sites, and counted cercarial production by each snail after transfer to the laboratory on the same day. We found that aquatic vegetation was positively associated with per-capita cercarial release by snails, probably because macrophytes harbor periphyton resources that snails feed upon, and well-fed snails tend to produce more parasites. In contrast, the abundance of aquatic macroinvertebrate snail predators was negatively associated with per-capita cercarial release by snails, probably because of several potential sublethal effects on snails or snail infection, despite a positive association between snail predators and total snail numbers at a site, possibly due to shared habitat usage or prey tracking by the predators. Thus, complex bottom-up and top-down ecological effects in this region plausibly influence the snail shedding rate and thus, total local density of schistosome cercariae.CONCLUSIONS/SIGNIFICANCE: Our study suggests that aquatic macrophytes and snail predators can influence per-capita cercarial production and total abundance of snails. Thus, snail control efforts might benefit by targeting specific snail habitats where parasite production is greatest. In conclusion, a better understanding of top-down and bottom-up ecological factors that regulate densities of cercarial release by snails, rather than solely snail densities or snail infection prevalence, might facilitate improved schistosomiasis control.
View details for DOI 10.1371/journal.pntd.0008417
View details for PubMedID 32628666
Effects of agrochemical pollution on schistosomiasis transmission: a systematic review and modelling analysis.
The Lancet. Planetary health
2020; 4 (7): e280–e291
BACKGROUND: Agrochemical pollution of surface waters is a growing global environmental challenge, especially in areas where agriculture is rapidly expanding and intensifying. Agrochemicals might affect schistosomiasis transmission through direct and indirect effects on Schistosoma parasites, their intermediate snail hosts, snail predators, and snail algal resources. We aimed to review and summarise the effects of these agrochemicals on schistosomiasis transmission dynamics.METHODS: We did a systematic review of agrochemical effects on the lifecycle of Schistosoma spp and fitted dose-response models to data regarding the association between components of the lifecycle and agrochemical concentrations. We incorporated these dose-response functions and environmentally relevant concentrations of agrochemicals into a mathematical model to estimate agrochemical effects on schistosomiasis transmission. Dose-response functions were used to estimate individual agrochemical effects on estimates of the agrochemically influenced basic reproduction number, R0, for Schistosoma haematobium. We incorporated time series of environmentally relevant agrochemical concentrations into the model and simulated mass drug administration control efforts in the presence of agrochemicals.FINDINGS: We derived 120 dose-response functions describing the effects of agrochemicals on schistosome lifecycle components. The median estimate of the basic reproduction number under agrochemical-free conditions, was 1·65 (IQR 1·47-1·79). Agrochemical effects on estimates of R0 for S haematobium ranged from a median three-times increase (R0 5·05, IQR 4·06-5·97) to transmission elimination (R0 0). Simulations of transmission dynamics subject to interacting annual mass drug administration and agrochemical pollution yielded a median estimate of 64·82 disability-adjusted life-years (DALYs) lost per 100 000 people per year (IQR 62·52-67·68) attributable to atrazine use. In areas where aquatic arthropod predators of intermediate host snails suppress transmission, the insecticides chlorpyrifos (6·82 DALYs lost per 100 000 people per year, IQR 4·13-8·69) and profenofos (103·06 DALYs lost per 100 000 people per year, IQR 89·63-104·90) might also increase the disability burden through their toxic effects on arthropods.INTERPRETATION: Expected environmental concentrations of agrochemicals alter schistosomiasis transmission through direct and indirect effects on intermediate host and parasite densities. As industrial agricultural practices expand in areas where schistosomiasis is endemic, strategies to prevent increases in transmission due to agrochemical pollution should be developed and pursued.FUNDING: National Science Foundation, National Institutes of Health.
View details for DOI 10.1016/S2542-5196(20)30105-4
View details for PubMedID 32681899
Models with environmental drivers offer a plausible mechanism for the rapid spread of infectious disease outbreaks in marine organisms.
2020; 10 (1): 5975
The first signs of sea star wasting disease (SSWD) epidemic occurred in just few months in 2013 along the entire North American Pacific coast. Disease dynamics did not manifest as the typical travelling wave of reaction-diffusion epidemiological model, suggesting that other environmental factors might have played some role. To help explore how external factors might trigger disease, we built a coupled oceanographic-epidemiological model and contrasted three hypotheses on the influence of temperature on disease transmission and pathogenicity. Models that linked mortality to sea surface temperature gave patterns more consistent with observed data on sea star wasting disease, which suggests that environmental stress could explain why some marine diseases seem to spread so fast and have region-wide impacts on host populations.
View details for DOI 10.1038/s41598-020-62118-4
View details for PubMedID 32249775
Concomitant Immunity and Worm Senescence May Drive Schistosomiasis Epidemiological Patterns: An Eco-Evolutionary Perspective.
Frontiers in immunology
2020; 11: 160
In areas where human schistosomiasis is endemic, infection prevalence and egg output are known to rise rapidly through childhood, reach a peak at 8-15 years of age, and decline thereafter. A similar peak ("overshoot") followed by return to equilibrium infection levels sometimes occurs a year or less after mass drug administration. These patterns are usually assumed to be due to acquired immunity, which is induced by exposure, directed by the host's immune system, and develops slowly over the lifetime of the host. Other explanations that have been advanced previously include differential exposure of hosts, differential mortality of hosts, and progressive pathology. Here we review these explanations and offer a novel (but not mutually exclusive) explanation, namely that adult worms protect the host against larval stages for their own benefit ("concomitant immunity") and that worm fecundity declines with worm age ("reproductive senescence"). This explanation approaches schistosomiasis from an eco-evolutionary perspective, as concomitant immunity maximizes the fitness of adult worms by reducing intraspecific competition within the host. If correct, our hypothesis could have profound implications for treatment and control of human schistosomiasis. Specifically, if immunity is worm-directed, then treatment of long-standing infections comprised of old senescent worms could enable infection with new, highly fecund worms. Furthermore, our hypothesis suggests revisiting research on therapeutics that mimic the concomitant immunity-modulating activity of adult worms, while minimizing pathological consequences of their eggs. We emphasize the value of an eco-evolutionary perspective on host-parasite interactions.
View details for DOI 10.3389/fimmu.2020.00160
View details for PubMedID 32161583
View details for PubMedCentralID PMC7053360
Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission.
Proceedings of the National Academy of Sciences of the United States of America
Recently, the World Health Organization recognized that efforts to interrupt schistosomiasis transmission through mass drug administration have been ineffective in some regions; one of their new recommended strategies for global schistosomiasis control emphasizes targeting the freshwater snails that transmit schistosome parasites. We sought to identify robust indicators that would enable precision targeting of these snails. At the site of the world's largest recorded schistosomiasis epidemic-the Lower Senegal River Basin in Senegal-intensive sampling revealed positive relationships between intermediate host snails (abundance, density, and prevalence) and human urogenital schistosomiasis reinfection (prevalence and intensity in schoolchildren after drug administration). However, we also found that snail distributions were so patchy in space and time that obtaining useful data required effort that exceeds what is feasible in standard monitoring and control campaigns. Instead, we identified several environmental proxies that were more effective than snail variables for predicting human infection: the area covered by suitable snail habitat (i.e., floating, nonemergent vegetation), the percent cover by suitable snail habitat, and size of the water contact area. Unlike snail surveys, which require hundreds of person-hours per site to conduct, habitat coverage and site area can be quickly estimated with drone or satellite imagery. This, in turn, makes possible large-scale, high-resolution estimation of human urogenital schistosomiasis risk to support targeting of both mass drug administration and snail control efforts.
View details for DOI 10.1073/pnas.1903698116
View details for PubMedID 31659025
Ecological interventions to prevent and manage zoonotic pathogen spillover.
Philosophical transactions of the Royal Society of London. Series B, Biological sciences
2019; 374 (1782): 20180342
Spillover of a pathogen from a wildlife reservoir into a human or livestock host requires the pathogen to overcome a hierarchical series of barriers. Interventions aimed at one or more of these barriers may be able to prevent the occurrence of spillover. Here, we demonstrate how interventions that target the ecological context in which spillover occurs (i.e. ecological interventions) can complement conventional approaches like vaccination, treatment, disinfection and chemical control. Accelerating spillover owing to environmental change requires effective, affordable, durable and scalable solutions that fully harness the complex processes involved in cross-species pathogen spillover. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.
View details for DOI 10.1098/rstb.2018.0342
View details for PubMedID 31401951
Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory.
Philosophical transactions of the Royal Society of London. Series B, Biological sciences
2019; 374 (1782): 20180344
Pathogen spillover between different host species is the trigger for many infectious disease outbreaks and emergence events, and ecosystem boundary areas have been suggested as spatial hotspots of spillover. This hypothesis is largely based on suspected higher rates of zoonotic disease spillover and emergence in fragmented landscapes and other areas where humans live in close vicinity to wildlife. For example, Ebola virus outbreaks have been linked to contacts between humans and infected wildlife at the rural-forest border, and spillover of yellow fever via mosquito vectors happens at the interface between forest and human settlements. Because spillover involves complex interactions between multiple species and is difficult to observe directly, empirical studies are scarce, particularly those that quantify underlying mechanisms. In this review, we identify and explore potential ecological mechanisms affecting spillover of pathogens (and parasites in general) at ecosystem boundaries. We borrow the concept of 'permeability' from animal movement ecology as a measure of the likelihood that hosts and parasites are present in an ecosystem boundary region. We then discuss how different mechanisms operating at the levels of organisms and ecosystems might affect permeability and spillover. This review is a step towards developing a general theory of cross-species parasite spillover across ecosystem boundaries with the eventual aim of improving predictions of spillover risk in heterogeneous landscapes. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.
View details for DOI 10.1098/rstb.2018.0344
View details for PubMedID 31401953
Unavoidable Risks: Local Perspectives on Water Contact Behavior and Implications for Schistosomiasis Control in an Agricultural Region of Northern Senegal.
The American journal of tropical medicine and hygiene
Human schistosomiasis is a snail-borne parasitic disease affecting more than 200 million people worldwide. Direct contact with snail-infested freshwater is the primary route of exposure. Water management infrastructure, including dams and irrigation schemes, expands snail habitat, increasing the risk across the landscape. The Diama Dam, built on the lower basin of the Senegal River to prevent saltwater intrusion and promote year-round agriculture in the drought-prone Sahel, is a paradigmatic case. Since dam completion in 1986, the rural population-whose livelihoods rely mostly on agriculture-has suffered high rates of schistosome infection. The region remains one of the most hyperendemic regions in the world. Because of the convergence between livelihoods and environmental conditions favorable to transmission, schistosomiasis is considered an illustrative case of a disease-driven poverty trap (DDPT). The literature to date on the topic, however, remains largely theoretical. With qualitative data generated from 12 focus groups in four villages, we conducted team-based theme analysis to investigate how perception of schistosomiasis risk and reported preventive behaviors may suggest the presence of a DDPT. Our analysis reveals three key findings: 1) rural villagers understand schistosomiasis risk (i.e., where and when infections occur), 2) accordingly, they adopt some preventive behaviors, but ultimately, 3) exposure persists, because of circumstances characteristic of rural livelihoods. These findings highlight the capacity of local populations to participate actively in schistosomiasis control programs and the limitations of widespread drug treatment campaigns. Interventions that target the environmental reservoir of disease may provide opportunities to reduce exposure while maintaining resource-dependent livelihoods.
View details for DOI 10.4269/ajtmh.19-0099
View details for PubMedID 31452497
- Modelled effects of prawn aquaculture on poverty alleviation and schistosomiasis control NATURE SUSTAINABILITY 2019; 2 (7): 611–20
- Emerging human infectious diseases and the links to global food production NATURE SUSTAINABILITY 2019; 2 (6): 445–56
Gene drives for schistosomiasis transmission control.
PLoS neglected tropical diseases
2019; 13 (12): e0007833
Schistosomiasis is one of the most important and widespread neglected tropical diseases (NTD), with over 200 million people infected in more than 70 countries; the disease has nearly 800 million people at risk in endemic areas. Although mass drug administration is a cost-effective approach to reduce occurrence, extent, and severity of the disease, it does not provide protection to subsequent reinfection. Interventions that target the parasites' intermediate snail hosts are a crucial part of the integrated strategy required to move toward disease elimination. The recent revolution in gene drive technology naturally leads to questions about whether gene drives could be used to efficiently spread schistosome resistance traits in a population of snails and whether gene drives have the potential to contribute to reduced disease transmission in the long run. Responsible implementation of gene drives will require solutions to complex challenges spanning multiple disciplines, from biology to policy. This Review Article presents collected perspectives from practitioners of global health, genome engineering, epidemiology, and snail/schistosome biology and outlines strategies for responsible gene drive technology development, impact measurements of gene drives for schistosomiasis control, and gene drive governance. Success in this arena is a function of many factors, including gene-editing specificity and efficiency, the level of resistance conferred by the gene drive, how fast gene drives may spread in a metapopulation over a complex landscape, ecological sustainability, social equity, and, ultimately, the reduction of infection prevalence in humans. With combined efforts from across the broad global health community, gene drives for schistosomiasis control could fortify our defenses against this devastating disease in the future.
View details for DOI 10.1371/journal.pntd.0007833
View details for PubMedID 31856157
Emerging human infectious diseases and the links to global food production.
2019; 2 (6): 445–56
Infectious diseases are emerging globally at an unprecedented rate while global food demand is projected to increase sharply by 2100. Here, we synthesize the pathways by which projected agricultural expansion and intensification will influence human infectious diseases and how human infectious diseases might likewise affect food production and distribution. Feeding 11 billion people will require substantial increases in crop and animal production that will expand agricultural use of antibiotics, water, pesticides and fertilizer, and contact rates between humans and both wild and domestic animals, all with consequences for the emergence and spread of infectious agents. Indeed, our synthesis of the literature suggests that, since 1940, agricultural drivers were associated with >25% of all - and >50% of zoonotic - infectious diseases that emerged in humans, proportions that will likely increase as agriculture expands and intensifies. We identify agricultural and disease management and policy actions, and additional research, needed to address the public health challenge posed by feeding 11 billion people.
View details for DOI 10.1038/s41893-019-0293-3
View details for PubMedID 32219187
View details for PubMedCentralID PMC7091874
THE ROLE OF IRRIGATED AGRICULTURE IN SCHISTOSOMIASIS RISK IN A DAMMED LANDSCAPE IN WEST AFRICA
AMER SOC TROP MED & HYGIENE. 2019: 11
View details for Web of Science ID 000507364502035
Potential Biological Control of Schistosomiasis by Fishes in the Lower Senegal River Basin.
The American journal of tropical medicine and hygiene
More than 200 million people in sub-Saharan Africa are infected with schistosome parasites. Transmission of schistosomiasis occurs when people come into contact with larval schistosomes emitted from freshwater snails in the aquatic environment. Thus, controlling snails through augmenting or restoring their natural enemies, such as native predators and competitors, could offer sustainable control for this human disease. Fishes may reduce schistosomiasis transmission directly, by preying on snails or parasites, or indirectly, by competing with snails for food or by reducing availability of macrophyte habitat (i.e., aquatic plants) where snails feed and reproduce. To identify fishes that might serve as native biological control agents for schistosomiasis in the lower Senegal River basin-one of the highest transmission areas for human schistosomiasis globally-we surveyed the freshwater fish that inhabit shallow, nearshore habitats and conducted multivariate analyses with quantitative diet data for each of the fish species encountered. Ten of the 16 fish species we encountered exhibited diets that may result in direct (predation) and/or indirect (food competition and habitat removal) control of snails. Fish abundance was low, suggesting limited effects on schistosomiasis transmission by the contemporary fish community in the lower Senegal River basin in the wild. Here, we highlight some native species-such as tilapia, West African lungfish, and freshwater prawns-that could be aquacultured for local-scale biological control of schistosomiasis transmission.
View details for PubMedID 30479247
Estimating the elimination feasibility in the 'end game' of control efforts for parasites subjected to regular mass drug administration: Methods and their application to schistosomiasis.
PLoS neglected tropical diseases
2018; 12 (11): e0006794
Progress towards controlling and eliminating parasitic worms, including schistosomiasis, onchocerciasis, and lymphatic filariasis, is advancing rapidly as national governments, multinational NGOs, and pharmaceutical companies launch collaborative chemotherapeutic control campaigns. Critical questions remain regarding the potential for achieving elimination of these infections, and analytical methods can help to quickly estimate progress towards-and the probability of achieving-elimination over specific timeframes. Here, we propose the effective reproduction number, Reff, as a proxy of elimination potential for sexually reproducing worms that are subject to poor mating success at very low abundance (positive density dependence, or Allee effects). Reff is the number of parasites produced by a single reproductive parasite at a given stage in the transmission cycle, over the parasite's lifetime-it is the generalized form of the more familiar basic reproduction number, R0, which only applies at the beginning of an epidemic-and it can be estimated in a 'model-free' manner by an estimator ('epsilon'). We introduce epsilon, demonstrate its estimation using simulated data, and discuss how it may be used in planning and evaluation of ongoing elimination efforts for a range of parasitic diseases.
View details for PubMedID 30418968
Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts
2018; 9: 837
Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Increased prevalence and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife and a projected 2- to 5-fold increase in global agrochemical use by 2050. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat and decreasing densities of snail predators. Epidemiological models indicate that these agrochemical effects can increase transmission of schistosomes. Identifying agricultural practices or agrochemicals that minimize disease risk will be critical to meeting growing food demands while improving human wellbeing.
View details for PubMedID 29483531
To Reduce the Global Burden of Human Schistosomiasis, Use 'Old Fashioned' Snail Control
TRENDS IN PARASITOLOGY
2018; 34 (1): 23–40
Control strategies to reduce human schistosomiasis have evolved from 'snail picking' campaigns, a century ago, to modern wide-scale human treatment campaigns, or preventive chemotherapy. Unfortunately, despite the rise in preventive chemotherapy campaigns, just as many people suffer from schistosomiasis today as they did 50 years ago. Snail control can complement preventive chemotherapy by reducing the risk of transmission from snails to humans. Here, we present ideas for modernizing and scaling up snail control, including spatiotemporal targeting, environmental diagnostics, better molluscicides, new technologies (e.g., gene drive), and 'outside the box' strategies such as natural enemies, traps, and repellants. We conclude that, to achieve the World Health Assembly's stated goal to eliminate schistosomiasis, it is time to give snail control another look.
View details for PubMedID 29126819
View details for PubMedCentralID PMC5819334
- Ecological control of schistosomiasis in Sub-Saharan Africa: restoration of predator-prey dynamics to reduce transmission ECOLOGY AND EVOLUTION OF INFECTIOUS DISEASES: PATHOGEN CONTROL AND PUBLIC HEALTH MANAGEMENT IN LOW-INCOME COUNTRIES 2018: 236–51
OU SONT LES ESCARGOTS - WHERE ARE THE SNAILS? USING REMOTE SENSING METHODS TO COMBAT SCHISTOSOMIASIS IN NORTHERN SENEGAL
AMER SOC TROP MED & HYGIENE. 2018: 19
View details for Web of Science ID 000461386602058
AN ECO-EVOLUTIONARY PERSPECTIVE ON SCHISTOSOMIASIS
AMER SOC TROP MED & HYGIENE. 2018: 418
View details for Web of Science ID 000461386604028
LOCAL PERCEPTIONS OF SEASONALITY AND REPORTED WATER CONTACT BEHAVIOR IN THE SAHEL: IMPLICATIONS FOR SCHISTOSOMIASIS TRANSMISSION
AMER SOC TROP MED & HYGIENE. 2018: 418–19
View details for Web of Science ID 000461386604031
COMPUTER VISION AND MACHINE LEARNING ENABLE ENVIRONMENTAL DIAGNOSTICS FOR TARGETING SCHISTOSOMIASIS CONTROL
AMER SOC TROP MED & HYGIENE. 2018: 418
View details for Web of Science ID 000461386604029
Heterogeneity in schistosomiasis transmission dynamics
JOURNAL OF THEORETICAL BIOLOGY
2017; 432: 87–99
Simple models of disease propagation often disregard the effects of transmission heterogeneity on the ecological and epidemiological dynamics associated with host-parasite interactions. However, for some diseases like schistosomiasis, a widespread parasitic infection caused by Schistosoma worms, accounting for heterogeneity is crucial to both characterize long-term dynamics and evaluate opportunities for disease control. Elaborating on the classic Macdonald model for macroparasite transmission, we analyze families of models including explicit descriptions of heterogeneity related to differential transmission risk within a community, water contact patterns, the distribution of the snail host population, human mobility, and the seasonal fluctuations of the environment. Through simple numerical examples, we show that heterogeneous multigroup communities may be more prone to schistosomiasis than homogeneous ones, that the availability of multiple water sources can hinder parasite transmission, and that both spatial and temporal heterogeneities may have nontrivial implications for disease endemicity. Finally, we discuss the implications of heterogeneity for disease control. Although focused on schistosomiasis, results from this study may apply as well to other parasitic infections with complex transmission cycles, such as cysticercosis, dracunculiasis and fasciolosis.
View details for PubMedID 28823529
View details for PubMedCentralID PMC5595357
The spatial spread of schistosomiasis: A multidimensional network model applied to Saint-Louis region, Senegal
ADVANCES IN WATER RESOURCES
2017; 108: 406–15
Schistosomiasis is a parasitic, water-related disease that is prevalent in tropical and subtropical areas of the world, causing severe and chronic consequences especially among children. Here we study the spatial spread of this disease within a network of connected villages in the endemic region of the Lower Basin of the Senegal River, in Senegal. The analysis is performed by means of a spatially explicit metapopulation model that couples local-scale eco-epidemiological dynamics with spatial mechanisms related to human mobility (estimated from anonymized mobile phone records), snail dispersal and hydrological transport of schistosome larvae along the main water bodies of the region. Results show that the model produces epidemiological patterns consistent with field observations, and point out the key role of spatial connectivity on the spread of the disease. These findings underline the importance of considering different transport pathways in order to elaborate disease control strategies that can be effective within a network of connected populations.
View details for PubMedID 29056816
View details for PubMedCentralID PMC5637889
Nearly 400 million people are at higher risk of schistosomiasis because dams block the migration of snail-eating river prawns
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2017; 372 (1722)
Dams have long been associated with elevated burdens of human schistosomiasis, but how dams increase disease is not always clear, in part because dams have many ecological and socio-economic effects. A recent hypothesis argues that dams block reproduction of the migratory river prawns that eat the snail hosts of schistosomiasis. In the Senegal River Basin, there is evidence that prawn populations declined and schistosomiasis increased after completion of the Diama Dam. Restoring prawns to a water-access site upstream of the dam reduced snail density and reinfection rates in people. However, whether a similar cascade of effects (from dams to prawns to snails to human schistosomiasis) occurs elsewhere is unknown. Here, we examine large dams worldwide and identify where their catchments intersect with endemic schistosomiasis and the historical habitat ranges of large, migratory Macrobrachium spp. prawns. River prawn habitats are widespread, and we estimate that 277-385 million people live within schistosomiasis-endemic regions where river prawns are or were present (out of the 800 million people who are at risk of schistosomiasis). Using a published repository of schistosomiasis studies in sub-Saharan Africa, we compared infection before and after the construction of 14 large dams for people living in: (i) upstream catchments within historical habitats of native prawns, (ii) comparable undammed watersheds, and (iii) dammed catchments beyond the historical reach of migratory prawns. Damming was followed by greater increases in schistosomiasis within prawn habitats than outside prawn habitats. We estimate that one third to one half of the global population-at-risk of schistosomiasis could benefit from restoration of native prawns. Because dams block prawn migrations, our results suggest that prawn extirpation contributes to the sharp increase of schistosomiasis after damming, and points to prawn restoration as an ecological solution for reducing human disease.This article is part of the themed issue 'Conservation, biodiversity and infectious disease: scientific evidence and policy implications'.
View details for DOI 10.1098/rstb.2016.0127
View details for Web of Science ID 000399956400008
View details for PubMedID 28438916
Disease ecology, health and the environment: a framework to account for ecological and socio-economic drivers in the control of neglected tropical diseases
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES
2017; 372 (1722)
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'.
View details for DOI 10.1098/rstb.2016.0128
View details for PubMedID 28438917
A novel framework to account for ecological drivers in the control and elimination of environmentally transmitted disease: a modelling study
ELSEVIER SCIENCE INC. 2017: 5
View details for Web of Science ID 000406739900006
Big-data-driven modeling unveils country-wide drivers of endemic schistosomiasis
Schistosomiasis is a parasitic infection that is widespread in sub-Saharan Africa, where it represents a major health problem. We study the drivers of its geographical distribution in Senegal via a spatially explicit network model accounting for epidemiological dynamics driven by local socioeconomic and environmental conditions, and human mobility. The model is parameterized by tapping several available geodatabases and a large dataset of mobile phone traces. It reliably reproduces the observed spatial patterns of regional schistosomiasis prevalence throughout the country, provided that spatial heterogeneity and human mobility are suitably accounted for. Specifically, a fine-grained description of the socioeconomic and environmental heterogeneities involved in local disease transmission is crucial to capturing the spatial variability of disease prevalence, while the inclusion of human mobility significantly improves the explanatory power of the model. Concerning human movement, we find that moderate mobility may reduce disease prevalence, whereas either high or low mobility may result in increased prevalence of infection. The effects of control strategies based on exposure and contamination reduction via improved access to safe water or educational campaigns are also analyzed. To our knowledge, this represents the first application of an integrative schistosomiasis transmission model at a whole-country scale.
View details for DOI 10.1038/s41598-017-00493-1
View details for Web of Science ID 000397528600021
View details for PubMedID 28352101
Global Assessment of Schistosomiasis Control Over the Past Century Shows Targeting the Snail Intermediate Host Works Best.
PLoS neglected tropical diseases
2016; 10 (7)
Despite control efforts, human schistosomiasis remains prevalent throughout Africa, Asia, and South America. The global schistosomiasis burden has changed little since the new anthelmintic drug, praziquantel, promised widespread control.We evaluated large-scale schistosomiasis control attempts over the past century and across the globe by identifying factors that predict control program success: snail control (e.g., molluscicides or biological control), mass drug administrations (MDA) with praziquantel, or a combined strategy using both. For data, we compiled historical information on control tactics and their quantitative outcomes for all 83 countries and territories in which: (i) schistosomiasis was allegedly endemic during the 20th century, and (ii) schistosomiasis remains endemic, or (iii) schistosomiasis has been "eliminated," or is "no longer endemic," or transmission has been interrupted.Widespread snail control reduced prevalence by 92 ± 5% (N = 19) vs. 37 ± 7% (N = 29) for programs using little or no snail control. In addition, ecological, economic, and political factors contributed to schistosomiasis elimination. For instance, snail control was most common and widespread in wealthier countries and when control began earlier in the 20th century.Snail control has been the most effective way to reduce schistosomiasis prevalence. Despite evidence that snail control leads to long-term disease reduction and elimination, most current schistosomiasis control efforts emphasize MDA using praziquantel over snail control. Combining drug-based control programs with affordable snail control seems the best strategy for eliminating schistosomiasis.
View details for DOI 10.1371/journal.pntd.0004794
View details for PubMedID 27441556
View details for PubMedCentralID PMC4956325
Infection with schistosome parasites in snails leads to increased predation by prawns: implications for human schistosomiasis control
JOURNAL OF EXPERIMENTAL BIOLOGY
2015; 218 (24): 3962-3967
Schistosomiasis - a parasitic disease that affects over 200 million people across the globe - is primarily transmitted between human definitive hosts and snail intermediate hosts. To reduce schistosomiasis transmission, some have advocated disrupting the schistosome life cycle through biological control of snails, achieved by boosting the abundance of snails' natural predators. But little is known about the effect of parasitic infection on predator-prey interactions, especially in the case of schistosomiasis. Here, we present the results of laboratory experiments performed on Bulinus truncatus and Biomphalaria glabrata snails to investigate: (i) rates of predation on schistosome-infected versus uninfected snails by a sympatric native river prawn, Macrobrachium vollenhovenii, and (ii) differences in snail behavior (including movement, refuge-seeking and anti-predator behavior) between infected and uninfected snails. In predation trials, prawns showed a preference for consuming snails infected with schistosome larvae. In behavioral trials, infected snails moved less quickly and less often than uninfected snails, and were less likely to avoid predation by exiting the water or hiding under substrate. Although the mechanism by which the parasite alters snail behavior remains unknown, these results provide insight into the effects of parasitic infection on predator-prey dynamics and suggest that boosting natural rates of predation on snails may be a useful strategy for reducing transmission in schistosomiasis hotspots.
View details for DOI 10.1242/jeb.129221
View details for Web of Science ID 000366645500015
View details for PubMedID 26677260
A Theoretical Analysis of the Geography of Schistosomiasis in Burkina Faso Highlights the Roles of Human Mobility and Water Resources Development in Disease Transmission
PLOS NEGLECTED TROPICAL DISEASES
2015; 9 (10)
We study the geography of schistosomiasis across Burkina Faso by means of a spatially explicit model of water-based disease dynamics. The model quantitatively addresses the geographic stratification of disease burden in a novel framework by explicitly accounting for drivers and controls of the disease, including spatial information on the distributions of population and infrastructure, jointly with a general description of human mobility and climatic/ecological drivers. Spatial patterns of disease are analysed by the extraction and the mapping of suitable eigenvectors of the Jacobian matrix subsuming the stability of the disease-free equilibrium. The relevance of the work lies in the novel mapping of disease burden, a byproduct of the parametrization induced by regional upscaling, by model-guided field validations and in the predictive scenarios allowed by exploiting the range of possible parameters and processes. Human mobility is found to be a primary control at regional scales both for pathogen invasion success and the overall distribution of disease burden. The effects of water resources development highlighted by systematic reviews are accounted for by the average distances of human settlements from water bodies that are habitats for the parasite's intermediate host. Our results confirm the empirical findings about the role of water resources development on disease spread into regions previously nearly disease-free also by inspection of empirical prevalence patterns. We conclude that while the model still needs refinements based on field and epidemiological evidence, the proposed framework provides a powerful tool for large-scale public health planning and schistosomiasis management.
View details for DOI 10.1371/journal.pntd.0004127
View details for Web of Science ID 000364459600033
View details for PubMedID 26513655
View details for PubMedCentralID PMC4625963
Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2015; 112 (31): 9650-9655
Eliminating human parasitic disease often requires interrupting complex transmission pathways. Even when drugs to treat people are available, disease control can be difficult if the parasite can persist in nonhuman hosts. Here, we show that restoration of a natural predator of a parasite's intermediate hosts may enhance drug-based schistosomiasis control. Our study site was the Senegal River Basin, where villagers suffered a massive outbreak and persistent epidemic after the 1986 completion of the Diama Dam. The dam blocked the annual migration of native river prawns (Macrobrachium vollenhoveni) that are voracious predators of the snail intermediate hosts for schistosomiasis. We tested schistosomiasis control by reintroduced river prawns in a before-after-control-impact field experiment that tracked parasitism in snails and people at two matched villages after prawns were stocked at one village's river access point. The abundance of infected snails was 80% lower at that village, presumably because prawn predation reduced the abundance and average life span of latently infected snails. As expected from a reduction in infected snails, human schistosomiasis prevalence was 18 ± 5% lower and egg burden was 50 ± 8% lower at the prawn-stocking village compared with the control village. In a mathematical model of the system, stocking prawns, coupled with infrequent mass drug treatment, eliminates schistosomiasis from high-transmission sites. We conclude that restoring river prawns could be a novel contribution to controlling, or eliminating, schistosomiasis.
View details for DOI 10.1073/pnas.1502651112
View details for Web of Science ID 000358930600060
View details for PubMedID 26195752
View details for PubMedCentralID PMC4534245
- Pathogenesis of Human Schistosomiasis Emerging and Re-emerging Human Infections Wiley and Sons Publishers. 2015
ROUTLEDGE HANDBOOK OF OCEAN RESOURCES AND MANAGEMENT
View details for Web of Science ID 000383152900008
- Ocean Health Handbook of Ocean Resources and Management Earthscan (UK). 2015
The Prawn Macrobrachium vollenhovenii in the Senegal River Basin: Towards Sustainable Restocking of All-Male Populations for Biological Control of Schistosomiasis.
PLoS neglected tropical diseases
2014; 8 (8)
Early malacological literature suggests that the outbreak of schistosomiasis, a parasitic disease transmitted by aquatic snails, in the Senegal River basin occurred due to ecological changes resulting from the construction of the Diama dam. The common treatment, the drug praziquantel, does not protect from the high risk of re-infection due to human contact with infested water on a daily basis. The construction of the dam interfered with the life cycle of the prawn Macrobrachium vollenhovenii by blocking its access to breeding grounds in the estuary. These prawns were demonstrated to be potential biological control agents, being effective predators of Schistosoma-susceptible snails. Here, we propose a responsible restocking strategy using all-male prawn populations which could provide sustainable disease control. Male prawns reach a larger size and have a lower tendency to migrate than females. We, therefore, expect that periodic restocking of all-male juveniles will decrease the prevalence of schistosomiasis and increase villagers' welfare. In this interdisciplinary study, we examined current prawn abundance along the river basin, complemented with a retrospective questionnaire completed by local fishermen. We revealed the current absence of prawns upriver and thus demonstrated the need for restocking. Since male prawns are suggested to be preferable for bio-control, we laid the molecular foundation for production of all-male M. vollenhovenii through a complete sequencing of the insulin-like androgenic gland-encoding gene (IAG), which is responsible for sexual differentiation in crustaceans. We also conducted bioinformatics and immunohistochemistry analyses to demonstrate the similarity of this sequence to the IAG of another Macrobrachium species in which neo-females are produced and their progeny are 100% males. At least 100 million people at risk of schistosomiasis are residents of areas that experienced water management manipulations. Our suggested non-breeding sustainable model of control-if proven successful-could prevent re-infections and thus prove useful throughout the world.
View details for DOI 10.1371/journal.pntd.0003060
View details for PubMedID 25166746
View details for PubMedCentralID PMC4148216
Sapronosis: a distinctive type of infectious agent.
Trends in parasitology
2014; 30 (8): 386-393
Sapronotic disease agents have evolutionary and epidemiological properties unlike other infectious organisms. Their essential saprophagic existence prevents coevolution, and no host-parasite virulence trade-off can evolve. However, the host may evolve defenses. Models of pathogens show that sapronoses, lacking a threshold of transmission, cannot regulate host populations, although they can reduce host abundance and even extirpate their hosts. Immunocompromised hosts are relatively susceptible to sapronoses. Some particularly important sapronoses, such as cholera and anthrax, can sustain an epidemic in a host population. However, these microbes ultimately persist as saprophages. One-third of human infectious disease agents are sapronotic, including nearly all fungal diseases. Recognition that an infectious disease is sapronotic illuminates a need for effective environmental control strategies.
View details for DOI 10.1016/j.pt.2014.06.006
View details for PubMedID 25028088
Regulation of laboratory populations of snails (Biomphalaria and Bulinus spp.) by river prawns, Macrobrachium spp. (Decapoda, Palaemonidae): Implications for control of schistosomiasis.
2014; 132: 64-74
Human schistosomiasis is a common parasitic disease endemic in many tropical and subtropical countries. One barrier to achieving long-term control of this disease has been re-infection of treated patients when they swim, bathe, or wade in surface fresh water infested with snails that harbor and release larval parasites. Because some snail species are obligate intermediate hosts of schistosome parasites, removing snails may reduce parasitic larvae in the water, reducing re-infection risk. Here, we evaluate the potential for snail control by predatory freshwater prawns, Macrobrachium rosenbergii and M. vollenhovenii, native to Asia and Africa, respectively. Both prawn species are high value, protein-rich human food commodities, suggesting their cultivation may be beneficial in resource-poor settings where few other disease control options exist. In a series of predation trials in laboratory aquaria, we found both species to be voracious predators of schistosome-susceptible snails, hatchlings, and eggs, even in the presence of alternative food, with sustained average consumption rates of 12% of their body weight per day. Prawns showed a weak preference for Bulinus truncatus over Biomphalaria glabrata snails. Consumption rates were highly predictable based on the ratio of prawn: snail body mass, suggesting satiation-limited predation. Even the smallest prawns tested (0.5-2g) caused snail recruitment failure, despite high snail fecundity. With the World Health Organization turning attention toward schistosomiasis elimination, native prawn cultivation may be a viable snail control strategy that offers a win-win for public health and economic development.
View details for DOI 10.1016/j.actatropica.2013.12.013
View details for PubMedID 24388955
Predictive Power of Air Travel and Socio-Economic Data for Early Pandemic Spread
2010; 5 (9)
Controlling the pandemic spread of newly emerging diseases requires rapid, targeted allocation of limited resources among nations. Critical, early control steps would be greatly enhanced if the key risk factors can be identified that accurately predict early disease spread immediately after emergence.Here, we examine the role of travel, trade, and national healthcare resources in predicting the emergence and initial spread of 2009 A/H1N1 influenza. We find that incorporating national healthcare resource data into our analyses allowed a much greater capacity to predict the international spread of this virus. In countries with lower healthcare resources, the reporting of 2009 A/H1N1 cases was significantly delayed, likely reflecting a lower capacity for testing and reporting, as well as other socio-political issues. We also report substantial international trade in live swine and poultry in the decade preceding the pandemic which may have contributed to the emergence and mixed genotype of this pandemic strain. However, the lack of knowledge of recent evolution of each H1N1 viral gene segment precludes the use of this approach to determine viral origins.We conclude that strategies to prevent pandemic influenza virus emergence and spread in the future should include: 1) enhanced surveillance for strains resulting from reassortment in traded livestock; 2) rapid deployment of control measures in the initial spreading phase to countries where travel data predict the pathogen will reach and to countries where lower healthcare resources will likely cause delays in reporting. Our results highlight the benefits, for all parties, when higher income countries provide additional healthcare resources for lower income countries, particularly those that have high air traffic volumes. In particular, international authorities should prioritize aid to those poorest countries where both the risk of emerging infectious diseases and air traffic volume is highest. This strategy will result in earlier detection of pathogens and a reduction in the impact of future pandemics.
View details for DOI 10.1371/journal.pone.0012763
View details for Web of Science ID 000281815800025
View details for PubMedID 20856678
Allometry and spatial scales of foraging in mammalian herbivores
2010; 13 (3): 311-320
Herbivores forage in spatially complex habitats. Due to allometry and scale-dependent foraging, herbivores are hypothesized to perceive and respond to heterogeneity of resources at scales relative to their body sizes. This hypothesis has not been manipulatively tested for animals with only moderate differences in body size and similar food niches. We compared short-term spatial foraging behavior of two herbivores (sheep and cattle) with similar dietary niche but differing body size. Although intake rates scaled allometrically with body mass (mass(0.75)), spatial foraging strategies substantially differed, with cattle exhibiting a coarser-grained use of the 'foodscape.' Selectivity by cattle (and not sheep) for their preferred food was more restricted when patches were smaller (< 10 m(2)). We conclude that differences in spatial scales of selection offers a plausible mechanism by which species can coexist on shared resources that exhibit multiple scales of spatial heterogeneity.
View details for DOI 10.1111/j.1461-0248.2009.01423.x
View details for Web of Science ID 000274713200005
View details for PubMedID 20100240
Ecology of avian influenza viruses in a changing world
YEAR IN ECOLOGY AND CONSERVATION BIOLOGY 2010
2010; 1195: 113-128
Influenza A virus infections result in approximately 500,000 human deaths per year and many more sublethal infections. Wild birds are recognized as the ancestral host of influenza A viruses, and avian viruses have contributed genetic material to most human viruses, including subtypes H5N1 and H1N1. Thus, influenza virus transmission in wild and domestic animals and humans is intimately connected. Here we review how anthropogenic change, including human population growth, land use, climate change, globalization of trade, agricultural intensification, and changes in vaccine technology may alter the evolution and transmission of influenza viruses. Evidence suggests that viral transmission in domestic poultry, spillover to other domestic animals, wild birds and humans, and the potential for subsequent pandemic spread, are all increasing. We highlight four areas in need of research: drivers of viral subtype dynamics; ecological and evolutionary determinants of transmissibility and virulence in birds and humans; the impact of changing land use and climate on hosts, viruses, and transmission; and the impact of influenza viruses on wild bird hosts, including their ability to migrate while shedding virus.
View details for DOI 10.1111/j.1749-6632.2010.05451.x
View details for Web of Science ID 000282828200007
View details for PubMedID 20536820
Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence
DISEASES OF AQUATIC ORGANISMS
2009; 87 (1-2): 5-18
A close examination of the coral disease literature reveals many hypothesized mechanisms for how coral disease may be linked to climate change. However, evidence has been largely circumstantial, and much uncertainty remains. Here, I review the latest information on both the predicted effects of climate change in coastal marine ecosystems and current research on coral-pathogen dynamics in relation to climate variables. The published evidence supports the hypothesis that coral infectious diseases are emerging and demonstrates that coral disease research has been exponentially expanding over the last few decades. Current research suggests that environmental factors, such as ocean warming, altered rainfall, increased storm frequency, sea level rise, altered circulation, and ocean acidification may play a role in coral disease. These climate variables likely alter coral epidemiology through effects on pathogen growth rates, transmission, virulence, and susceptibility. Despite recent advances, discovering the causes of coral disease emergence at large spatial and temporal scales has been hindered by several factors including (1) the inability to rely on Koch's postulates for diseases with multifactorial etiologies, (2) the paucity of long-term, coordinated, coral disease data, and (3) the difficulty in detecting correlations in inherently non-linear, dynamic disease systems. In a rapidly changing global environment, the consequences of increasing coral disease may be severe, leading to elevated extinction risk and loss of critical reef habitat. Current evidence is still preliminary but is increasingly suggestive that mitigating the effects of climate change may help reduce the emergence of disease and improve the health of coral reef ecosystems.
View details for DOI 10.3354/dao02099
View details for Web of Science ID 000272675600002
View details for PubMedID 20095237
- Editor's choice: Disease dynamics in marine metapopulations: modelling infectious diseases on coral reefs JOURNAL OF APPLIED ECOLOGY 2009; 46 (3): 621-631
- Causal inference in disease ecology: investigating ecological drivers of disease emergence FRONTIERS IN ECOLOGY AND THE ENVIRONMENT 2008; 6 (8): 420-429
- Spatial epidemiology of Caribbean yellow band syndrome in Montastrea spp. coral in the eastern Yucatan, Mexico HYDROBIOLOGIA 2005; 548: 33-40
Epidemiologic evaluation of diarrhea in dogs in an animal shelter
AMERICAN JOURNAL OF VETERINARY RESEARCH
2005; 66 (6): 1018-1024
To determine associations among infectious pathogens and diarrheal disease in dogs in an animal shelter and demonstrate the use of geographic information systems (GISs) for tracking spatial distributions of diarrheal disease within shelters.Feces from 120 dogs.Fresh fecal specimens were screened for bacteria and bacterial toxins via bacteriologic culture and ELISA, parvovirus via ELISA, canine coronavirus via nested polymerase chain reaction assay, protozoal cysts and oocysts via a direct fluorescent antibody technique, and parasite ova and larvae via microscopic examination of direct wet mounts and zinc sulfate centrifugation flotation.Salmonella enterica and Brachyspira spp were not common, whereas other pathogens such as canine coronavirus and Helicobacter spp were common among the dogs that were surveyed. Only intestinal parasites and Campylobacterjejuni infection were significant risk factors for diarrhea by univariate odds ratio analysis. Giardia lamblia was significantly underestimated by fecal flotation, compared with a direct fluorescent antibody technique. Spatial analysis of case specimens by use of GIS indicated that diarrhea was widespread throughout the entire shelter, and spatial statistical analysis revealed no evidence of spatial clustering of case specimens.This study provided an epidemiologic overview of diarrhea and interacting diarrhea-associated pathogens in a densely housed, highly predisposed shelter population of dogs. Several of the approaches used in this study, such as use of a spatial representation of case specimens and considering multiple etiologies simultaneously, were novel and illustrate an integrated approach to epidemiologic investigations in shelter populations.
View details for Web of Science ID 000229404800016
View details for PubMedID 16008226