Effects of Environmental Change on the Interactions between Pathogens and Humans

Kawabata Zen’ichiro RIHN

minamoto Toshifumi RIHN

Abe Akira RIHN Asano Kota Graduate School of Human and Environmental Sciences, Kyoto University Itayama Tomoaki Nagasaki University Kakehashi Masayuki Graduate School of Health Sciences, Hiroshima University Kong Hainan School of Environmental Science and Engineering, Shanghai Jiao Tong University, China Matsuoka Masatomi Asahi Fishery Cooperative, Shiga Minamoto Toshifumi RIHN Nasu Masao Environmental Science and Microbiology, Graduate School of Pharmaceutical Sciences, Osaka University Okuda Noboru Center for Ecological Research, Kyoto University Omori Koji Center for Marine Environmental Studies, Ehime University Wu, Deyi School of Environmental Science and Engineering, Shanghai Jiao Tong University, China Yamanaka Hiroki Department of Environmental Solution Technology, Ryukoku University

There is an important environmental component to infectious disease. While pathological studies inform effective disease treatment, study of disease ecology – the interactions between pathogen, host and humans that may create or alleviate ‘fertile’ disease environments – is necessary for prediction and prevention of new disease outbreaks. This project develops a model of environment-pathogen-human interactions based on our intensive examination of the ecological and social causes and effects of Koi Herpes Virus disease in Lake Biwa, Japan. This model will allow us to suggest ways to prevent or minimize the emergence and spread of infectious diseases.

Objectives

The rapid spread of emerging infectious diseases is threatening humans, wildlife, and livestock worldwide. Koi Herpes Virus (KHV) is a pathogen responsible for episodic mass mortality of common carp (Cyprinus carpio carpio) (Photo 1) since the late 1990s. The common carp is the original domesticated aquaculture species, and an important source of protein today (Photo 2). To predict outbreaks of infectious disease and to prevent epidemics, it is essential to conduct pathological studies and to understand the environment-pathogen-human interactions that cause and spread infectious disease.

This study has three main objectives. It first describes KHV disease ecology, including: the specific links between anthropogenically-caused changes to freshwater ecosystems and the emergence and spread of KHV disease; the impacts of KHV disease on local ecosystem services; the social and cultural attempts to address KHV disease; and the environmental changes associated with human mitigation or adaptation (Fig. 1). Based on this description of the human and non-human factors affecting KHV disease ecology, it then describes a general model of environment-pathogen-human interaction (Fig. 2). Finally, it will suggest how these interactions may be modified in order to mitigate the damages associated with infectious diseases.

Research methods and organization

Fields survey is conducted at Lake Biwa, Japan. Laboratory work is undertaken at RIHN. Our project is organized into five research groups, plus executive and advisory groups, as follows:

The Human Alterations Group investigates the effects of anthropogenic environmental alteration on the emergence and spread of KHV and the behavior of its host carp.

The Pathogen and Host Ecology Group defines carp and KHV ecology, and so describes the environmental factors involved in KHV infection and transmission.

The Ecosystem Impacts Group examines the process of infection and the effects of KHV disease on ecosystem functions such as genetic diversity.

The Economics and Culture Group investigates the damages associated with KHV disease, including on ecosystem services and economic and cultural phenomena, and describes the social attempts to redress those losses.

The Feedback Group examines the environmental changes associated with human response to loses caused by KHV disease.

The Executive Group develops the model of pathogen-human interactions by coordinating the activities of each group.

Finally, an Advisory Group composed of recognized experts in relevant fields makes suggestions in order to improve the research.

Main results to date

1) We found that gentle gradient lakeshores provide a wide range of thermal conditions, suggesting that fish can choose tempertures to alleviate stress associated with unfavorable water temperatures, and thus reduce susceptibility to KHV (Yamanaka et al., 2010).

2) We established an innovative method to quantitatively detect KHV in natural environments (Minamoto et al., 2009 (Fig. 3); Honjo et al., 2010). The method revealed that since it was first detected in 2003, KHV is now found throughout the Lake Biwa ecosystem, including in plankton and sediment, lagoons and ponds, and now in almost all the rivers in Japan. We demonstrated that it is impossible to eliminate KHV, but that precautionary environmental management can eliminate “fertile” disease environments.

3) We have developed a preliminary break-through method allowing determination of the number and location of carp in their natural environments.

4) We found that breeding habitats can become hot spots for transmission of infectious diseases if hosts aggregate for mating and pathogen activation occurs during the host breeding season (Uchii et al., 2011) (Photo 3).

5) We developed a non-invasive method (i.e., a method that does not require handling fish) to quantify how water conditions stress carp. Using this method we found that changes in water temperature do induce stress.

6) We applied a Based on our assessment of KHV disease in Lake Biwa, we applied our conceptual model of linked environment-pathogen-human interactions to Lake Erhai, China, schistosomiasis in Kenya, fish diseases in the Pin River at Chaing Mai, Thailand (Photo 4), and Legionella disease (Yamaguchi et al., 2010), MRSA, Norovirus disease, and nontuberculous mycobacteria disease (Ichijo et al., 2010) in Japan. These applications helped us understand how pathogens interact with humans and suggested environmental conditions that might prevent disease outbreaks and spread as well asstrategies for safe coexistence of humans with pathogens.

7) By combining the results from each work group, ranging from molecular biology to environmental sciences to human society, we are providing evidence to support the hypothesis that anthropogenic environmental changes promote disease outbreaks.

8) We have presented our findings at national and international conferences of the linkages between the environment, pathogens and humans, emphsizing their significance to prevention and control of infectious disease.

Scheduled research objectives in 2011

1) Refine a method to quantify carp spatially and temporally and innovative methods to describe our conceptual model of environment-pathogen-human linkages including a development of micro-device capable of in-situ measurment of KHV incidence and infectivity.

2) Determine the environmental factors involved in KHV abundance and its infectivity, and in carp population density and its susceptibility.

3) Conduct controlled experiments to reveal the relationship between water temperature, carp stress and susceptibility to KHV.

4) Assess the economic and cultural impacts of carp die-offs.

5) Apply the conceptual model of environment-pathogen-human linkage to other infectious diseases; KHV disease in Lake Erhai, China, Schistosomiasis in Kenya, fish diseases in the Pin River at Chaing Mai, Thailand, and Legionella disease, MRSA, Norovirus disease, and nontuberculous mycobacteria disease in Japan, and then describe the common parameters of KHV disease and other infectious diseases.

6) Continue to explore evidence that anthropogenic environmental changes can mediate disease outbreaks.

7) Synthesis of results of the work groups in order to develop a set of recommendations designed to minimize the emergence and spread of infectious diseases and facilitate the safe coexistence of humans with pathogens.

8) Publish our results in international journals and books in order to disseminate the concepts and practical measures that can aid the control of “fertile” disease environments.

9) Organize a national and international symposium on environment-pathogen-human linkage to develop a network for this field of study.