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. A sampling of my current research interests include: 1) biological control of schistosomiasis by restoring a native river prawn that preys on the snail intermediate host, 2) network models of schistosomiasis transmission and control, and 3) discovery of ecological solutions for mutually beneficial outcomes for human health and the environment.
As Executive Director of Stanford's new Program for Disease Ecology, Health and the Environment, I am interested in discovering and promoting ecological solutions that benefit human health and a healthy environment. As part of my research program, I founded The Upstream Alliance: a research initiative joining partners across the globe for reduction of the parasitic disease: schistosomiasis.
Basic Life Science Research Associate, Biology
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)
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
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
- Ocean Health Handbook of Ocean Resources and Management Earthscan (UK). 2015
- Pathogenesis of Human Schistosomiasis Emerging and Re-emerging Human Infections Wiley and Sons Publishers. 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 Web of Science ID 000341574700031
View details for PubMedID 25166746
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 Web of Science ID 000334001100009
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