Navigating parasite webs and parasite flow: emerging and re-emerging parasitic zoonoses of wildlife origin

Wildlife are now recognised as an important source of emerging human pathogens, including parasites. This paper discusses the linkages between wildlife, people, zoonotic parasites and the ecosystems in which they co-exist, revisits definitions for 'emerging' and 're-emerging', and lists zoonotic parasites that can be acquired from wildlife including, for some, estimates of the associated global human health burdens. The paper also introduces the concepts of 'parasite webs' and 'parasite flow', provides a context for parasites, relative to other infectious agents, as causes of emerging human disease, and discusses drivers of disease emergence and re-emergence, especially changes in biodiversity and climate. Angiostrongylus cantonensis in the Caribbean and the southern United States, Baylisascaris procyonis in California and Georgia, Plasmodium knowlesi in Sarawak, Malaysia, Human African Trypanosomiasis, Sarcoptes scabiei in carnivores, and Cryptosporidium, Giardia and Toxoplasma in marine ecosystems are presented as examples of wildlife-derived zoonotic parasites of particular recent interest. An ecological approach to disease is promoted, as is a need for an increased profile for this approach in undergraduate and graduate education in the health sciences. Synergy among scientists and disciplines is identified as critical for the study of parasites and parasitic disease in wildlife populations. Recent advances in techniques for the investigation of parasite fauna of wildlife are presented and monitoring and surveillance systems for wildlife disease are discussed. Some of the limitations inherent in predictions for the emergence and re-emergence of infection and disease associated with zoonotic parasites of wildlife are identified. The importance of public awareness and public education in the prevention and control of emerging and re-emerging zoonotic infection and disease are emphasised. Finally, some thoughts for the future are presented.     

Emerging and Reemerging Infectious Diseases: Biocomplexity as an Interdisciplinary Paradigm

Understanding factors responsible for reemergence of diseases believed to have been controlled and outbreaks of previously unknown infectious diseases is one of the most difficult scientific problems facing society today. Significant knowledge gaps exist for even the most studied emerging infectious diseases. Coupled with failures in the response to the resurgence of infectious diseases, this lack of information is embedded in a simplistic view of pathogens and disconnected from a social and ecological context, and assumes a linear response of pathogens to environmental change. In fact, the natural reservoirs and transmission rates of most emerging infectious diseases primarily are affected by environmental factors, such as seasonality or meteorological events, typically producing nonlinear responses that are inherently unpredictable. A more realistic view of emerging infectious diseases requires a holistic perspective that incorporates social as well as physical, chemical, and biological dimensions of our planet’s systems. The notion of biocomplexity captures this depth and richness, and most importantly, the interactions of human and natural systems. This article provides a brief review and a synthesis of interdisciplinary approaches and insights employing the biocomplexity paradigm and offers a social–ecological approach for addressing and garnering an improved understanding of emerging infectious diseases. Drawing on findings from studies of cholera and other examples of emerging waterborne, zoonotic, and vectorborne diseases, a “blueprint” for the proposed interdisciplinary research framework is offered which integrates biological processes from the molecular level to that of communities and regional systems, incorporating public health infrastructure and climate aspects.     

Industrial Food Animal Production and Global Health Risks: Exploring the Ecosystems and Economics of Avian Influenza

Many emerging infectious diseases in human populations are associated with zoonotic origins. Attention has often focused on wild animal reservoirs, but most zoonotic pathogens of recent concern to human health either originate in, or are transferred to, human populations from domesticated animals raised for human consumption. Thus, the ecological context of emerging infectious disease comprises two overlapping ecosystems: the natural habitats and populations of wild animals, and the anthropogenically controlled habitats and populations of domesticated species. Intensive food animal production systems and their associated value chains dominate in developed countries and are increasingly important in developing countries. These systems are characterized by large numbers of animals being raised in confinement with high throughput and rapid turnover. Although not typically recognized as such, industrial food animal production generates unique ecosystems—environments that may facilitate the evolution of zoonotic pathogens and their transmission to human populations. It is often assumed that confined food animal production reduces risks of emerging zoonotic diseases. This article provides evidence suggesting that these industrial systems may increase animal and public health risks unless there is recognition of the specific biosecurity and biocontainment challenges of the industrial model. Moreover, the economic drivers and constraints faced by the industry and its participants must be fully understood in order to inform preventative policy. In order to more effectively reduce zoonotic disease risk from industrial food animal production, private incentives for the implementation of biosecurity must align with public health interests.     

Focus: Zoonotic Disease: Health System Contact and Awareness of Zoonotic Diseases: Can it Serve as One Health Entry Point in the Urban Community of Ahmedabad, India?

One Health (OH) is emphasized globally to tackle the (re)emerging issues at the human-animal-ecosystem interface. However, the low awareness about zoonoses remain a challenge in global south, thus this study documented the health system contact and its effect on the awareness level of zoonoses in the urban community of Ahmedabad, India. A community-based household survey was conducted between October 2018 and July 2019. A total of 460 households (HHs) were surveyed from two zones and 23 wards of the city through cluster sampling. A structured, pilot-tested, and researcher-administered questionnaire in the vernacular language was used to collect the information on demographic details, socio-economic details, health-seeking behavior for both the humans and their animals, human and animal health system contact details and the participants’ awareness on selected zoonotic diseases based on the prioritization (rabies, brucellosis, swine flu, and bird flu). Out of 460 surveyed households, 69% of HHs and 59% of HHs had a health system contact to the human and animal health system respectively at the community level. There are multiple health workers active on the community level that could potentially serve as One Health liaisons. The investigation of the knowledge and awareness level of selected zoonotic diseases revealed that 58.5%, 47.6%, and 4.6% know about rabies, swine and/or bird flu, and brucellosis, respectively. The mixed-effect linear regression model indicates that there is no significant effect on the zoonotic disease awareness score with the human health system contact; however, a minimal positive effect with the animal health system contact was evident.     

Beyond Disciplinary Boundaries: Leptospirosis as a Model of Incorporating Transdisciplinary Approaches to Understand Infectious Disease Emergence

Leptospirosis is a zoonotic infectious disease of global significance. Political, economic, demographic, ecologic, and other anthropogenically driven environmental changes have fueled the reemergence of this disease in industrialized and developing countries, and in both urban and rural settings. We argue that conventional disciplinary, even interdisciplinary, research methods are not sufficient to elucidate the complex mechanisms and causal relationships among the myriad factors responsible for infectious disease emergence. To address the significant gaps in the field of leptospirosis, an integrated research agenda is needed to guide successful public health remediation of the disease. Based on both working group analysis of literature and newly obtained information, we describe cross-disciplinary collaborative approaches that allow a novel approach to understand leptospirosis emergence with regard to mountain-to-sea ecosystems in Hawai‘i and other region-specific ecosystems. Leptospirosis research is a model for how complementary disciplines in the social, cultural, ecological, and biomedical sciences can optimally interact towards a higher understanding of emerging infectious diseases.     

Evolution of virulence,environmental change,and the threat posed by emerging and chronic diseases

Assessments of future threats posed by infection have focused largely on zoonotic, acute disease, under the rubric “emerging diseases.” Evolutionary and epidemiological studies indicate, however, that particular aspects of infrastructure, such as protected water supplies, vector-proof housing, and health care facilities, protect against the emergence of zoonotic, acute infectious diseases. While attention in the global health community has focused on emerging diseases, there has been a concurrent, growing recognition that important chronic diseases, such as cancer, are often caused by infectious agents that are already widespread in human populations. For economically prosperous countries, the immediacy of this threat contrasts with their infrastructural protection from severe acute infectious disease. This reasoning leads to the conclusion that chronic infectious diseases pose a more significant threat to economically prosperous countries than zoonotic, acute infectious diseases. Research efforts directed at threats posed by infection may therefore be more effective overall if increased efforts are directed toward understanding and preventing infectious causes of chronic diseases across the spectrum of economic prosperity, as well as toward specific infrastructural improvements in less prosperous countries to protect against virulent, acute infectious diseases.     

Zoonoses

The numbers of microbial species that can infect human beings are shown to be 1415, of which 868 species (61%) are zoonotic. Since most of the emerging pathogens (75%) are originated from other animals, public health sectors should be vigilant against the emergence of new zoonotic diseases. Only 33% of zoonoses can spread from human to human after introduction into human population. Various factors such as human demography, ecological change, global transportation and climate change are responsible for the emergence of zoonoses. Even a slight change in the ecological niche where pathogenic organisms thrive would result in the increase of the incidence of the disease.     

All Hands on Deck: Transdisciplinary Approaches to Emerging Infectious Disease

The increasing burden of emerging infectious diseases worldwide confronts us with numerous challenges, including the imperative to design research and responses that are commensurate to understanding the complex social and ecological contexts in which infectious diseases occur. A diverse group of scientists met in Hawaii in March 2005 to discuss the linked social and ecological contexts in which infectious diseases emerge. A subset of the meeting was a group that focused on “transdisciplinary approaches” to integrating knowledge across and beyond academic disciplines in order to improve prevention and control of emerging infections. This article is based on the discussions of that group. Here, we outline the epidemiological legacy that has dominated infectious disease research and control up until now, and introduce the role of new, transdisciplinary and systems-based approaches to emerging infectious diseases. We describe four cases of transboundary health issues and use them to discuss the potential benefits, as well as the inherent difficulties, in understanding the social–ecological contexts in which infectious diseases occur and of using transdisciplinary approaches to deal with them. The views expressed here by Marian McDonald and Josh Rosenthal are those of the authors and do not represent official views or policies of the U.S. Centers for Disease Control and Prevention or the National Institutes of Health.     

The Role of Ecotones in Emerging Infectious Diseases

Recognition of the significance of the boundary between ecological systems, often referred to as the ecotone, has a long history in the ecological sciences and in zoonotic disease research. More recent research in landscape ecology has produced an expanded view of ecotones and elaboration of their characteristics and functions in ecosystems. Parallel research on emerging infectious diseases (EIDs) and the causes of increased rates of pathogen transmission, spread, and adaptation suggests a correspondence between ecotonal processes and the ecological and evolutionary processes responsible for zoonotic and vector-borne emerging infections. A review of the literature suggests that ecotones play a role in a number of the most important EIDs. Yet these are the only diseases for which specific landscape ecological information exists in the literature or disease reports. However, the similar disease ecologies of these with about half of the approximately 130 zoonotic EIDs suggests ecotones, particularly their anthropogenic origination or modification, may be generally associated with ecotones and the global trend of increasing EIDs.     

Awareness and Practices Relating to Zoonotic Diseases Among Smallholder Farmers in Nepal

Increasing livestock production to meet growing demands has resulted in greater interactions at the livestock–wildlife–human interface and more opportunities for zoonotic disease spread. Zoonoses impose enormous burdens on low-income countries like Nepal, where populations are largely dependent on livestock production and access to shared grazing lands, often near protected areas, due to population pressures. Several livestock-associated zoonoses have been reported in Nepal; however, little is known regarding Nepali farmers’ knowledge of zoonoses and opportunities for disease management. We conducted a cross-sectional study to investigate Nepali farmers’ awareness of zoonoses, assess current health challenges, and evaluate disease prevention and control practices. We found that awareness of zoonotic pathogens was limited, especially in informally educated and illiterate farmers; the majority of which were women. Further, farmers’ preventive herd health, food safety, and sanitation practices were not associated with their awareness. Several farmers reported high-risk practices despite being aware of zoonotic diseases, suggesting a disconnect between the farmers’ awareness and practice. Our study highlights the need for improving Nepali farmers’ knowledge of zoonoses and disease prevention measures. Closing these awareness-practice gaps will require an improved understanding of risk and effective drivers of behavior change, alongside engagement of farmers in development of zoonotic disease prevention programs that encourage participation of both male and female farmers across all levels of education.     

Toward Holistic Evaluation and Assessment: Linking Ecosystems and Human Well-Being for the Three Gorges Dam

A significant challenge exists in assessing the social and ecological impacts of development projects in a holistic and comprehensive manner. Our objective is to elucidate the linkages between ecological change and human well-being, and its importance in integrated assessment policy for development projects, using the Three Gorges Dam (China) as a case study. A collaborative research initiative was undertaken to review and synthesize published information on the ecological and human health effects of the Three Gorges Dam. Our synthesis suggests that the Three Gorges Dam has altered social–ecological dynamics of human health and ecosystem function in the Yangtze River basin with significant consequences for human well-being. Direct impacts to human well-being were grouped into four primary categories, including: (1) toxicological impacts; (2) shifting infectious disease dynamics; (3) natural hazards; and (4) social health. Social–ecological relationships were altered in complex ways, with both direct and indirect effects, positive and negative interactions, and chronic and acute impacts on human well-being. Our synthesis supports a comprehensive evaluation of development projects via integrated assessments of human and environmental consequences. This is probably best achieved through a coupled social–environmental impact assessment to ensure holistic and comprehensive analyses of expected costs and benefits. The role of research can thereby be to elucidate the linkages between ecosystems and human health to better inform the assessment process. A synthesis of the existing information on the Three Gorges suggests that this is best achieved through institutional collaboration and transdisciplinary integration of expertise.     

Introducing One Health to the Ethical Debate About Zoonotic Diseases in Southeast Asia

Pandemic plans recommend phases of response to an emergent infectious disease (EID) outbreak, and are primarily aimed at preventing and mitigating human‐to‐human transmission. These plans carry presumptive weight and are increasingly being operationalized at the national, regional and international level with the support of the World Health Organization (WHO). The conventional focus of pandemic preparedness for EIDs of zoonotic origin has been on public health and human welfare. However, this focus on human populations has resulted in strategically important disciplinary silos. As the risks of zoonotic diseases have implications that reach across many domains outside traditional public health, including anthropological, environmental, and veterinary fora, a more inclusive ecological perspective is paramount for an effective response to future outbreaks.     

Eco-cultural health,global health,and sustainability

Anthropogenic stress on the earth’s ecosystems has resulted in widespread prevalence of ecosystem distress syndrome, a quantifiable set of signs of ecosystem degradation. At the same time, the planet is witnessing rapid declines in global cultural diversity and in the vitality of the world’s cultures, which closely mirror, and are interrelated with, ecological degradation. As a consequence of this converging crisis of loss of ecosystem and cultural health, global health and sustainability are increasingly under threat. An eco-cultural health perspective based on understanding the linkages between human activities, ecological and cultural disruption, and public health is essential for addressing these threats and achieving global sustainability.     

Ecosystem Approach to Human Health in Two Villages of the North Jordan Valley: Scoping the Problems

North Jordan Valley (NJV) is a narrow rift valley that extends from lake Tiberius in the north to the Dead Sea in the south. It follows the River Jordan and contains the most fertile lands in Jordan. With a population around 140,000, primarily working in agriculture, NJV is Jordan’s premier agricultural production area. NJV is an ecosystem that is stressed both naturally and by human activities. Limited precipitation and very hot summer seasons are stresses that are inherent parts of the ecosystem itself. However, human activities like agriculture, poor sanitation, and tourism produce health risks to the people through the pollution and degradation of natural resources. The area also faces several socioeconomic problems such as poverty, large family size, and unemployment. In NJV, women typically work at home as housewives taking care of large families and are engaged in agricultural activities through which they are exposed, along with men and children, to high temperature and high concentration of pesticides. This article presents the findings of a Participatory Rapid Appraisal (PRA) study that focused on assessing local communities’ perception and awareness of the linkages between disruption of the ecosystem and prevailing public health problems. From an academic point of view, one of the key challenges of implementing ecosystem approaches to human health is the incorporation of various stakeholders as full partners throughout the research process rather than as contributors to a research designed from the sole perspective and interests of the academic research team. This study was conceptualized as a preliminary study to guide and inform the design of a larger research study on health and environment linkages in the NJV. The process was considered key for ensuring that research questions would reflect and build upon the priorities of multiple stakeholders, including community members, and would involve them in the design of the research. In addition to the successful involvement of local communities and other stakeholders in the identification of primary health problems and community priorities in the study area, the research played a key role in introducing various stakeholders to the basics of the Ecosystem Approaches to Human Health (Ecohealth) concept. The study took place in two small villages in NJV (Tal Al-Arbaeen and Tal Al-Menteh). The first village is located upstream of the junction point where King Abdullah Canal’s fresh water mixes with marginal quality water of King Talal Reservoir (KTR) while the second one is situated downstream. Results of this study showed that local communities are generally aware of the linkages between the health of the ecosystem and human health and well-being. According to the results of the study, key stressors to the environment (socioeconomic and institutional) include the use/abuse of agrochemicals and household insecticides, spread of flies (associated to organic agriculture), mismanagement of organic fertilizers, lack of sanitation services, unsanitary household conditions, and a serious problem of stray dogs and rodents. Problems associated with poverty and large family size were also commonly mentioned. Diarrhea, respiratory diseases, and infectious and parasitic diseases were believed to be the most common health problems in both villages. Local communities showed great interest and concern for the various health problems to which they are confronted and expressed eagerness to contribute to potential mitigation/intervention measures.     

Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases

Studies have demonstrated that ~60%–80% of emerging infectious diseases (EIDs) in humans originated from wild life. Bats are natural reservoirs of a large variety of viruses, including many important zoonotic viruses that cause severe diseases in humans and domestic animals. However, the understanding of the viral population and the ecological diversity residing in bat populations is unclear, which complicates the determination of the origins of certain EIDs. Here, using bats as a typical wildlife reservoir model, virome analysis was conducted based on pharyngeal and anal swab samples of 4440 bat individuals of 40 major bat species throughout China. The purpose of this study was to survey the ecological and biological diversities of viruses residing in these bat species, to investigate the presence of potential bat-borne zoonotic viruses and to evaluate the impacts of these viruses on public health. The data obtained in this study revealed an overview of the viral community present in these bat samples. Many novel bat viruses were reported for the first time and some bat viruses closely related to known human or animal pathogens were identified. This genetic evidence provides new clues in the search for the origin or evolution pattern of certain viruses, such as coronaviruses and noroviruses. These data offer meaningful ecological information for predicting and tracing wildlife-originated EIDs.     

Human vs. Animal Outbreaks of the 2009 Swine-Origin H1N1 Influenza A epidemic

The majority of emerging infectious diseases are zoonotic in origin, including recently emerging influenza viruses such as the 2009 swine-origin H1N1 influenza A epidemic. The epidemic that year affected both human and animal populations as it spread globally. In fact, before the end of 2009, 14 different countries reported H1N1 infected swine. In order to better understand the zoonotic nature of the epidemic and the relationship between human and animal disease surveillance data streams, we compared 2009 reports of H1N1 infection to define the temporal relationship between reported cases in animals and humans. Generally, human cases preceded animal cases at a country-level, supporting the potential of H1N1 infection to be a “reverse zoonosis”, and the value of integrating human and animal disease report data.     

Wildlife Trade and Human Health in Lao PDR: An Assessment of the Zoonotic Disease Risk in Markets

Although the majority of emerging infectious diseases can be linked to wildlife sources, most pathogen spillover events to people could likely be avoided if transmission was better understood and practices adjusted to mitigate risk. Wildlife trade can facilitate zoonotic disease transmission and represents a threat to human health and economies in Asia, highlighted by the 2003 SARS coronavirus outbreak, where a Chinese wildlife market facilitated pathogen transmission. Additionally, wildlife trade poses a serious threat to biodiversity. Therefore, the combined impacts of Asian wildlife trade, sometimes termed bush meat trade, on public health and biodiversity need assessing. From 2010 to 2013, observational data were collected in Lao PDR from markets selling wildlife, including information on volume, form, species and price of wildlife; market biosafety and visitor origin. The potential for traded wildlife to host zoonotic diseases that pose a serious threat to human health was then evaluated at seven markets identified as having high volumes of trade. At the seven markets, during 21 observational surveys, 1,937 alive or fresh dead mammals (approximately 1,009 kg) were observed for sale, including mammals from 12 taxonomic families previously documented to be capable of hosting 36 zoonotic pathogens. In these seven markets, the combination of high wildlife volumes, high risk taxa for zoonoses and poor biosafety increases the potential for pathogen presence and transmission. To examine the potential conservation impact of trade in markets, we assessed the status of 33,752 animals observed during 375 visits to 93 markets, under the Lao PDR Wildlife and Aquatic Law. We observed 6,452 animals listed by Lao PDR as near extinct or threatened with extinction. The combined risks of wildlife trade in Lao PDR to human health and biodiversity highlight the need for a multi-sector approach to effectively protect public health, economic interests and biodiversity.     

Network Approach for Analyzing and Promoting Equity in Participatory Ecohealth Research

Effective involvement and equity in participation between men and women and the various community groups are likely to influence the equity in the sharing of the development outcomes of any participatory research project. The CARUSO project, a participatory research based on the ecosystem approach to human health, showed that the inhabitants from Brasília Legal, a small village located on the river banks of the Tapajós river in the Brazilian Amazon, are exposed to mercury through fish consumption; a subsequent participatory intervention based on dietary changes was effective in reducing mercury exposure of the population. In the present study, we focus on equity in participation and analyze the discussion network about mercury and health to measure individual and group involvement in the community. Participation in the discussion network is associated with the awareness of the critical information necessary to allow the individual to change dietary habits toward the preferential consumption of the less contaminated fish species. Our network analysis shows that gender, age, religion, education, subsistence activities, and spatial distribution of the houses are key elements affecting the involvement of the population in discussions about mercury and health. Based on these results, we propose strategies for integrating the research results and the knowledge of the villagers in a new cycle of participatory research in order to address the lack of involvement of some groups and to promote equitable participation and benefit sharing.     

Public Health Risk Assessment Linked to Climatic and Ecological Change

Disturbances of climatic and ecological systems can present risks to human health, which are becoming more evident from health studies linked to climate variability, landuse change and global climate change. Waterborne disease agents, such as Giardia cysts and Cryposporidium oocysts have been positively correlated with rainfall. El Niño-related extreme weather conditions can have a significant impact on vector- and water-borne diseases. The linkages between weather, terrestrial ecology and human health have been discovered for some diseases, such as rodent-borne hantavirus. Marine ecology also plays a role in determining human health risks, such as from cholera, and other enteric pathogens. Deforestation and ensuing changes in landuse, human settlement, commercial development, road construction, and water control systems singly, and in combination have been accompanied by increases in or emergence of diseases like malaria and schistosomiasis in some regions of the world. Long-term climate change may increase the frequency of heat waves and potentially air pollution episodes, increase the number of extreme weather events, cause coastal flooding and salination of fresh water aquifers, and displace coastal settlements. Ultimately, a two-pronged approach (empirical and modeling studies) is required to better understand these linkages between climato-logical and ecological change as determinants of disease.     

Development of Transdisciplinarity Among Students Placed with a Sustainability for Health Research Project

Transdisciplinary education on sustainability for health has been primarily developed in high-income countries, yet the need in countries with limited research and human resource investments remains urgent. Little empiric documentation of the facilitators and barriers to transdisciplinary learning in such countries has been described. We assessed transdisciplinary learning among students of different disciplines collaborating with an Ecuadorian sustainability for health research project. Six undergraduate students from four different disciplinary backgrounds were incorporated through work–study agreements with provincial university academic supervisors. Learning was fostered and monitored through participant observations by a field supervisor. Students’ learning was evaluated through subsequent in-depth interviews and visualization methods. Academic supervisor key informant and co-investigator observations aided triangulation. Qualitative data were analyzed using indicators of transdisciplinary thinking. Principal factors facilitating transdisciplinary learning were interaction with social actors, the integration of work with other disciplines, the use of alternative research techniques and methods, and the constant support of the field supervisor. Inhibiting factors included the existence of rigid academic rules, lack of training of the academic supervisors in diverse research methods, and social pressures to implement unidisciplinary foci. At the end of their link with the project, students had developed both cognitive outcomes and attitudinal values relevant to sustainable development for health. In countries with limited investments in research and human resources development, transdisciplinary approaches with social actors and engaged researchers can sensitize new professionals training in traditional academic contexts to the ecological–social–health problems faced by poor majorities and encourage their subsequent work on sustainability for human health.