Integrated parasite management: path to sustainable control of fishborne trematodes in aquaculture Jesper H. Clausen 1 , Henry Madsen 1 , Phan Thi Van 2 , Anders Dalsgaard 1 , and K. Darwin Murrell 1 1 Faculty of Health and Medical Sciences, Department of Veterinary Disease Biology, University of Copenhagen, Denmark 2 Research Institute for Aquaculture Number 1 (RIA1), Bac Ninh, Viet Nam Fishborne zoonotic trematodes (FZT) are an emerging problem and there is now a consensus that, in addition to wild-caught fish, fish produced in aquaculture present a major food safety risk, especially in Southeast Asia where aquaculture is important economically. Current control programs target communities at risk through mass drug administration. However, we argue that treat- ment alone will not reduce the risk from eating infected fish and that sustainable effective control must adopt an integrated FZT control approach based on education, infrastructure improvements, and management prac- tices that target critical control points in the aquaculture production cycle identified from a thorough understand- ing of FZT and host biology and epidemiology. We present recommendations for an integrated parasite management (IPM) program for aquaculture farms. The problem of fishborne parasites in aquaculture Recent global health assessments have identified FZT (see Glossary) as among the most important (and neglected) parasitic zoonotic diseases [1–7]. Along with bacteria and viruses, FZT can be important causes of illnesses in humans, ranging from mild gastroenteritis to life-threat- ening disease [8]. These infections occur in humans and other reservoir hosts as a result of ingesting raw or im- properly cooked fish that are infected with the metacercar- ia stage of the zoonotic trematodes (or flukes). The liver flukes Opisthorchis viverrini, O. felineus, and Clonorchis sinensis are notable for causing chronic inflammation of the hepatobiliary system, which in chronic infections may lead to cholangiocarcinoma [9]. Infections with intestinal FZT (mainly species of Heterophyidae such as Haplorchis spp.) and Echinostomatidae (e.g., Echinochasmus spp.) may cause intestinal inflammation, diarrhea, and invasion of the heart, brain, and spinal cord by parasite eggs [10,11]. Other important intestinal flukes are Metagoni- mus spp., Centrocestus spp., Stellantchasmus falcatus, and Procerovum varium [11]. In many countries, wild-caught fish are important sources of FZT, and the increase in aquaculture production in Asia has been proposed as increasing the risk for human cases of fishborne trematodiasis in that region [1,2,4,12,13]; research is needed to clarify the relative risk from these sources of fish. The growth in aquaculture has been remarkable over the past few decades, especially in the People’s Republic of China, India, and several countries in Southeast Asia. The increase in production is driven by growing demands in both national and global markets, as well as by technological advances and improved efficiency in the aquaculture sector [14,15]. Fish cultured in Asia now account for 85% of world aquaculture production, and Opinion Glossary Catchment area: the area from which rainfall flows into a single basin (e.g., pond, reservoir, lake, or river). Cercaria: a larval trematode that develops in a molluscan host from a redia or sporocyst and emerges as a tailed swimming form that seeks out a host (e.g., fish) in which it invades and develops to the metacercaria stage (usually encysted). Cholangiocarcinoma: a cancer of the biliary system of humans, which has been associated with chronic infections of the liver flukes Opisthorchis spp and Clonorchis sinensis. Fish fry: fish larvae that have developed to the age that they are capable of feeding themselves. Fishborne zoonotic trematodes (FZT): these are transmitted to humans as metacercariae that have encysted in fish. Host: most trematodes have a life cycle requiring at least two hosts: the definitive or primary host (a vertebrate) in which the flukes sexually reproduce, and an intermediate host (a mollusk), in which asexual reproduction occurs, producing a cercaria, the agent of transmission to other hosts. Integrated parasite management (IPM): the inclusion of prevention and control actions that are identified through HACCP analysis as critical points for risk of infection, and may include education, management and infrastructure changes, and use of drug treatment of definitive hosts when appropriate. Juvenile fish: fish fry that morphologically resemble the adult (e.g., possess scales and working fins) but are sexually immature and are not full-grown. Metacercaria: a tailless encysted (e.g., in the tissues of a fish) late larva of a trematode that is usually the stage that is infective for the definitive host. Semi-intensive aquaculture systems: semi-intensive culture systems which depend at least partially on natural food that can be increased over baseline levels by fertilization (often in the form of human and animal fecal waste) and/ or use of supplementary feed to complement natural food. Reservoir host: definitive host (for a parasite to reproduce sexually) that can serve as a source of infection for other hosts, independently of human hosts in the case of zoonotic trematodes. Trematoda: trematodes (flukes) represent a class of mostly hermaphroditic, dorso-ventrally flattened worms in the phylum Platyhelminthes that internally parasitize molluscs and vertebrates. VAC system: a semi-intensive fish culture system named after the Vietnamese words for garden (Vuon), pond (Ao), and livestock housing (Chuong, pigsty). 1471-4922/ ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.pt.2014.10.005 Corresponding author: Murrell, K.D. (kdmurrell@comcast.net). Keywords: fishborne; parasites; aquaculture; fish; prevention; control. 8 Trends in Parasitology, January 2015, Vol. 31, No. 1