Effects of Environmental Change on the Interactions between Pathogens and Humans

Kawabata Zen’ichiro RIHN

Asano Kota Graduate School of Human and Environmental Sciences, Kyoto University Itayama Tomoaki RIHN 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 human actions that may create or eliminate ‘fertile’ disease environments – is necessary for prediction and prevention of new disease outbreaks. This project intensively examines the ecological and social causes and effects of Koi Herpes Virus disease in Japan and China in order to develop a model of pathogen-human interactions. Based on our experiments and observations of interactions between pathogen, environments and humans, we will suggest ways to prevent or minimize the emergence and spread of infectious diseases.

Objectives

Infectious disease has become a significant global environmental problem. This study investigates the emergence and spread of Koi Herpes Virus (KHV) in Lake Biwa, Japan. 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).

This study has three main objectives: (1) To describe Koi Herpes Virus disease ecology, including: the specific links between anthropogenic 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 adaptation (Fig. 1); (2) To describe a general model of linkage between environments, pathogens and humans (Fig. 3); (3) To suggest how interactions between pathogen and humans may be modified in order to mitigate the human and environmental damages associated with infectious diseases.

Research methods and organization

Fields surveys are conducted at Lake Biwa, Japan, and Lake Erhai, China. 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 inv

estigates the effects of anthropogenic environmental alteration on the emergence and spread of KHV and the behavior of its host Cyprinus carpio carpio.

The Pathogen and Host Ecology Group defines the biology and ecology of KHV and carp, 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 material cycling.

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

The Feedback Group examines the human response to losses caused by KHV disease, and the environmental change associated with this response.

The Executive Group coordinates the activities of each group and develops the model of pathogen-human interactions.

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 water temperature on gentle gradient lakeshores is more spatially and temporally variable than on steep banks constructed by humans. This result suggests that gentle shores can provide a wider range of thermal conditions that allows fish to finetune their (everyday) thermoregulatory behavior, acclimate efficiently to (longer-term) changes in water temperature, and generally alleviate stresses associated with unfavorable water temperatures and so reduce susceptibility to KHV (Yamanaka et al. 2010).

2) We established a method to measure KHV presence in natural water (Minamoto et al., 2009a; Honjo et al., 2010) and found that in the five years since its presence was first documented, KHV has spread throughout Lake Biwa (Fig. 2) (Minamoto et al., 2009b).

3) Telemetry tracking of carp behavior revealed that carp favor warmer water temperatures. This finding was incorporated into our mathematical model predicting KHV disease outbreaks.

4) We found no evidence of KHV antibodies in carp smaller than 30cm, while 54% of carp larger than 30cm were KHV positive. Of antibody-positive individuals, 44% contracted KHV by polymerase chain reaction (PCR), strongly suggesting that those surviving carp become KHV carriers. A few individuals were positive by PCR but negative for antibodies, indicating recent infection. These results suggest that transmission of KHV is still occurring within the native common carp population in Lake Biwa (Uchii, et al., 2009).

5) We developed a non-invasive method (i.e. a method that does not require handling fish) to quantify how water conditions stress carp. This method indicates that changes in water temperature do stress carp.

6) In Lake Erhai we found gradient and water temperature conditions similar to those of Lake Biwa, indicating that KHV may find an advantageous habitat there.

7) At national and international conferences, we have presented our findings on the linkages between environment, pathogen and humans, and emphasized their importance to the prevention and control of infectious disease.

Scheduled research objectives in 2010

1) Develop a method to quantitatively detect KHV in sediment, organisms and other elements in aquatic ecosystems.

2) Clarify the distribution of infectious KHV in Lake Biwa.

3) Develop a micro-device to measure the quantity and infectivity of KHV in situ.

4) Determine the environmental factors involved in KHV dynamics and infectivity.

5) Use outdoor experimental tanks to define optimum water temperature for carp.

6) Describe the environmental characteristics of the places where KHV and carp interact, and clarify the behavior of the KHV-infected carp in order to reveal the locations where infection likely occurs (Fig. 4).

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

8) Demonstrate the ecological effects of carp on species composition in experimental ponds.

9) Evaluate the cultural and nutritional value of carp as a human food.

10) Assess the economic and cultural impact of carp die-offs.

11) Create a preliminary model of the interactions between environmental change, KHV and humans.

12) Survey the spatial and temporal distribution of water temperature in Lake Erhai in order to establish the applicability of Lake Biwa findings to Lake Erhai (Photo 3).

13) Describe the common parameters of KHV and other infectious diseases.

14) Promote collaboration with the DIVERSITAS program of international biodiversity science.

15) Develop a set of recommendations to prevent or minimize the emergence and spread of infectious diseases.