pathogens Review Challenges and Solutions to Viral Diseases of Finfish in Marine Aquaculture Kizito K. Mugimba 1,* , Denis K. Byarugaba 1, Stephen Mutoloki 2 , Øystein Evensen 2 and Hetron M. Munang’andu 3,* 1 Department of Biotechnical and Diagnostic Sciences, College of Veterinary Medicine Animal Resources and Biosecurity, Makerere University, Kampala P.O. Box 7062, Uganda; [email protected] 2 Department of Paraclinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, P.O. Box 369, 0102 Oslo, Norway; [email protected] (S.M.); [email protected] (Ø.E.) 3 Department of Production Animal Clinical Sciences, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, P.O. Box 369, 0102 Oslo, Norway * Correspondence: [email protected] (K.K.M.); [email protected] (H.M.M.); Tel.: +256-772-56-7940 (K.K.M.); +47-98-86-86-83 (H.M.M.) Abstract: Aquaculture is the fastest food-producing sector in the world, accounting for one-third of global food production. As is the case with all intensive farming systems, increase in infectious diseases has adversely impacted the growth of marine fish farming worldwide. Viral diseases cause high economic losses in marine aquaculture. We provide an overview of the major challenges limiting the control and prevention of viral diseases in marine fish farming, as well as highlight potential solutions. The major challenges include increase in the number of emerging viral diseases, wild reservoirs, migratory species, anthropogenic activities, limitations in diagnostic tools and expertise, transportation of virus contaminated ballast water, and international trade. The proposed solutions to these problems include developing biosecurity policies at global and national levels, Citation: Mugimba, K.K.; Byarugaba, implementation of biosecurity measures, vaccine development, use of antiviral drugs and probiotics D.K.; Mutoloki, S.; Evensen, Ø.; to combat viral infections, selective breeding of disease-resistant fish, use of improved diagnostic tools, Munang’andu, H.M. Challenges and disease surveillance, as well as promoting the use of good husbandry and management practices. Solutions to Viral Diseases of Finfish in Marine Aquaculture. Pathogens A multifaceted approach combining several control strategies would provide more effective long- 2021, 10, 673. https://doi.org/ lasting solutions to reduction in viral infections in marine aquaculture than using a single disease 10.3390/pathogens10060673 control approach like vaccination alone. Academic Editor: Frederick Kibenge Keywords: viruses; challenges; solutions; prevention; control; vaccines; biosecurity Received: 9 May 2021 Accepted: 26 May 2021 Published: 30 May 2021 1. Introduction Aquaculture, also referred to as “underwater agriculture”, is the fastest growing Publisher’s Note: MDPI stays neutral food-producing sector in the world. By 2013, it had already overtaken beef and poultry with regard to jurisdictional claims in production [1]. It contributes one-third of global food production, which includes more published maps and institutional affil- than 200 farmed fish species [1]. Similar to other intensive farming systems, the impact of iations. infectious diseases in intensive fish farming has had serious repercussions. Among these are viral diseases, most of which cause high economic losses [2–4]. In addition, viral diseases reduce fish welfare by causing various conditions that adversely affect the wellbeing of fish, such as reduced feed intake, abnormal swimming behavior, predation of diseased Copyright: © 2021 by the authors. fish, and negative social interactions [5–8]. As pointed out by several scientists [9–12], Licensee MDPI, Basel, Switzerland. viruses are the most abundant entity in marine ecosystems. Their abundance in oceans This article is an open access article range from 3 × 106 mL−1 viral particles (VPs) in the deep sea to 1 × 108 mL−1 VPs in distributed under the terms and coastal waters, decreasing in abundance with distance from shore [9,13,14]. However, only conditions of the Creative Commons a few viruses cause diseases in farmed fish linked to high economic losses, rendering these Attribution (CC BY) license (https:// viruses noticeable in most countries. It should be noted, however, that most pathogenic creativecommons.org/licenses/by/ 4.0/). viruses of fish have been detected in areas around Europe, Americas, and Asia. Hence, it Pathogens 2021, 10, 673. https://doi.org/10.3390/pathogens10060673 https://www.mdpi.com/journal/pathogens Pathogens 2021, 10, 673 2 of 22 Pathogens 2021, 10, 673 2 of 21 pathogenic viruses of fish have been detected in areas around Europe, Americas, and Asia. Hence, it is likely that several pathogenic viruses remain unknown due to lack of surveillance.is likely that In several this review, pathogenic we highlight viruses remain some of unknown the major due challenges to lack of associated surveillance. with In viralthis review,diseases we in mariculture highlight some and of suggest the major solutions challenges to these associated problems. with viral diseases in mariculture and suggest solutions to these problems. 2. Major Challenges Associated with Viral Diseases in Marine Aquaculture 2. Major Challenges Associated with Viral Diseases in Marine Aquaculture 2.1. Emerging Infectious Diseases 2.1. Emerging Infectious Diseases Krkosek [15] defined emerging infectious diseases (EID) as previously unknown Krkosek [15] defined emerging infectious diseases (EID) as previously unknown diseases or spread of an existing disease into a new host or geographic area. As shown in diseases or spread of an existing disease into a new host or geographic area. As shown Figure 1, factors associated with occurrence of EIDs include (i) viral factors such as the in Figure1, factors associated with occurrence of EIDs include (i) viral factors such as the emergence of a new virus in an area or viruses acquiring virulence through mutations, (ii) emergence of a new virus in an area or viruses acquiring virulence through mutations, anthropogenic activities such as the introduction of an exotic susceptible fish species or (ii) anthropogenic activities such as the introduction of an exotic susceptible fish species or virusvirus in in a a new new habitat, habitat, (iii) (iii) host host fa factorsctors such such as as fish fish becoming becoming stressed stressed and and thus thus susceptible susceptible toto viral viral infection infection through through intensive intensive aquaculture, aquaculture, or or (iv) (iv) environmental environmental factors factors such such as as changes in salinity, pH, CO2, and other factors that render fish susceptible to infection changes in salinity, pH, CO2, and other factors that render fish susceptible to infection [16]. [16]Krkosek. Krkosek [15] pointed[15] pointed out thatout freshwaterthat freshwater and marineand marine fish havefish have the highest the highest rates rates of EIDs of EIDsamong among vertebrates vertebrates mainly mainly because because they they are are the the most most speciose speciose group group [ 17[17]].. This could could alsoalso be be attributed attributed to to the the fact fact that that aquatic aquatic environments environments used used for for fish fish farming farming have have a a high high populatipopulationon of of unknown unknown viruses, viruses, some some of of which which could could infect infect and and cause cause disease disease in in fish. fish. DuringDuring the the period period of of 1988 1988 to to 1992, 1992, Hetrick Hetrick and and Hedrick Hedrick [18] [18] identified identified more more than than 35 35 EIDs EIDs thatthat infect infect fish. fish. Among Among these these were were new new infectious infectious agents, agents, while while others others were were isolates isolates of of knknownown agents agents but but infecting infecting new new host host species. species. They They attributed attributed this this increase increase in EIDs in EIDs to an to increasean increase in surveillance in surveillance accompanied accompanied by an by expansion an expansion of aquaculture of aquaculture that included that included new farmednew farmed fish species. fish species. Additionally, Additionally, we wereported reported close close to to20 20 newly newly discovered discovered viral viral ppathogensathogens of of fish fish using using metagenomics metagenomics analysis analysis between between 2010 2010 and and 2016 2016 [19] [19].. Overall, Overall, EIDs EIDs posepose a a challenge challenge to to the the expansion expansion of of aquaculture. aquaculture. FigureFigure 1. DriversDrivers of of emerging emerging infectious infectious diseases diseases in aquaculture. in aquaculture. (A) Virus (A drivers) Virus includedrivers mutations include mutationsleading to leading virulent to strains virulent and strains the ability and to the infect ability different to infect host different species. (Bhost) Fish species host drivers. (B) Fish include host driverssusceptibility include to susceptibility infection due to to infection low immunity. due to (Clow) Anthropogenic immunity. (C) drivers Anthropogenic include farming drivers practicesinclude farmingthat include practices high that stocking include density high stocking and poor density feeding and regimes poor thatfeeding cause regimes fish to that become cause stressed fish to becomeand increase stressed susceptibility and increase to susceptibility infection. (D) to Environmental infection. (D) driversEnvironmental include adversedrivers include