Review
Molecules to modeling: Toxoplasma gondii oocysts at the human–animal–environment interface

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Abstract

Environmental transmission of extremely resistant Toxoplasma gondii oocysts has resulted in infection of diverse species around the world, leading to severe disease and deaths in human and animal populations. This review explores T. gondii oocyst shedding, survival, and transmission, emphasizing the importance of linking laboratory and landscape from molecular characterization of oocysts to watershed-level models of oocyst loading and transport in terrestrial and aquatic systems. Building on discipline-specific studies, a One Health approach incorporating tools and perspectives from diverse fields and stakeholders has contributed to an advanced understanding of T. gondii and is addressing transmission at the rapidly changing human–animal–environment interface.

Introduction

Understanding the ecology and epidemiology of disease in the context of ecosystems is critical for preserving human and animal population health. Over 7 billion people now depend upon the earth's resources [1], and global environmental change has made disease migration to new hosts and landscapes a reality rather than a potential threat [2], [3]. Anthropogenic activities, in particular, reshape landscapes, climate, and species distributions and interactions across the globe, with significant potential to alter patterns of pathogen emergence and spread [4], [5], [6], [7]. Habitat conversion, introduction of non-native species, and increased contact between human, domestic animal, and wildlife populations have been linked to emerging viral, bacterial, and parasitic diseases [8]. Climate change also has the potential to alter cycles of disease transmission by influencing vector and host ranges, pathogen survival, and dynamics of water-borne transmission [8], [9]. Of the 1415 organisms documented as human pathogens, over 60% are believed to have come from domestic or wild animal reservoirs [10]. Examining animal, human, or environmental health alone ignores the vital links between these components.

Historical biological and geographic boundaries of disease transmission will likely continue to shift significantly with changing environmental conditions, making a more holistic, One Health approach to pathogen research and management essential. By linking diverse non-academic stakeholder communities and researchers from different disciplines, the One Health approach builds a synergistic base from which to study and address the unique health challenges emerging at the human–animal–environment interface in a changing global environment [11], [12].

Toxoplasma gondii, a globally distributed, zoonotic, protozoan parasite capable of infecting a wide range of warm-blooded animals [13], provides a broadly applicable example of the complexity of pathogen transmission among diverse hosts and environments and illustrates the need for a One Health approach to better understand disease ecology and epidemiology. Although long-studied in terrestrial landscapes, T. gondii has also emerged as a significant aquatic pathogen linked to marine mammal infection and water-borne outbreaks of disease in humans around the world [14]. Oocysts, the exceptionally hardy free-living environmental stage of the parasite, play a key role in transmission of T. gondii to newly recognized hosts and ecosystems. As wild and domestic felids are the only known hosts capable of shedding T. gondii oocysts in their feces [15], [16], [17], infection of people and animals through contaminated terrestrial and aquatic sources emphasizes the need to jointly examine human, domestic animal, and wildlife populations. While parasitologists, physicians, veterinarians, ecologists, and molecular biologists have studied T. gondii independently, understanding how a traditionally terrestrial pathogen is emerging in new environments requires more integrated knowledge. For T. gondii and other pathogens, creating a more collaborative approach to research and management from molecular to landscape levels has enhanced our understanding of health at the human–animal–environment interface.

Section snippets

Importance of oocysts in transmission of T. gondii infections

Warm-blooded animals, including humans, are typically infected with T. gondii through one of three pathways: ingesting oocysts from the environment (through contaminated water, soil, or food), eating an infected intermediate host with T. gondii cysts in its tissues, or congenital transmission from infected mothers to offspring [13], [18]. Additional potential routes of transmission, including T. gondii tachyzoite-contaminated sperm and unpasteurized milk, have been demonstrated, but are thought

Keys to oocyst success

Oocysts pose a serious threat to susceptible hosts because of their robust environmental resistance, low infectious dose for some species, and the lack of methods to reliably detect oocysts in water and other environmental substrates to identify sources of exposure. Multiple experiments evaluating the survival of oocysts in soils showed that they may remain viable for at least 1 year when covered and in cool temperatures (4 °C) [38], [62], [63], [64]. Under warm climate conditions in dry soils

How molecular characteristics contribute to oocyst success

Molecular description of the oocyst has been extremely limited for several reasons: (1) no method exists for maintaining or expanding oocysts in vitro, therefore, infection of the definitive felid host is required to produce oocysts; (2) oocysts are refractory to routine protocols used to isolate nucleic acids and proteins, thus requiring special equipment and procedures; and (3) live oocysts pose a biohazard risk as they are not readily killed by laboratory disinfectants [75], [76], [77].

Oocysts at the animal–human–environment interface

Evaluating the role of oocysts in T. gondii transmission cycles requires a broad understanding that encompasses: the ecology of felids, aquatic mammals, and terrestrial and marine prey species; chemical and physical properties that determine oocyst resistance; human influences on domestic animal and wildlife populations; and the impact of environmental factors, such as land use, climate, and freshwater runoff. Considering the diverse factors that contribute to T. gondii oocyst loading,

Land use and climate change – anthropogenic influences on oocyst transmission

Oocyst-borne infections with T. gondii may increase in animals and humans as climate and habitat changes reshape environments worldwide. As most of the human population and their domesticated animals are distributed along waterways, there has been an associated increase in the amount of fecal deposition within watersheds that drain into collecting freshwater bodies, estuaries, and coastlines. The physical forces that drive overland runoff events and mobilize transport of fecal matter are likely

Why a One Health modeling approach enhances understanding of T. gondii oocyst transmission

Currently, there is a notable lack of literature on the relationship between T. gondii oocyst properties, felid shedding patterns, oocyst transport from terrestrial to aquatic systems, and climate and habitat change. This knowledge gap illustrates the vital need for a more integrative method to examine the impacts of environmental change on oocyst-based infection in human and animal populations. Uniting ecologists, veterinarians, physicians, epidemiologists, molecular biologists, and physical

Conflict of interest

None.

Role of funding sources

Funders did not have any involvement in the writing of or decision to submit this manuscript.

Acknowledgements

Funding sources supporting the authors included NSF-Ecology of Infectious Disease Grants (0525765, 1065990), a National Institutes of Health K01 award (5K01RR031487) to H. Fritz, and a fellowship from the National Oceanic and Atmospheric Administration Oceans and Human Health Initiative (S08-67884) to K. Shapiro. The authors thank Alison Kent, UC Davis Wildlife Health Center, for assistance in developing the transmission graphic.

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    These authors contributed equally to this review.

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