Kinetics of viral shedding provide insights into the epidemiology of viral hemorrhagic septicemia in Pacific herring

Abstract

Losses from infectious diseases are an important component of natural mortality among marine fish species, but factors controlling the ecology of these diseases and their potential responses to anthropogenic changes are poorly understood. We used viral hemorrhagic septicemia virus (VHSV) and a laboratory stock of Pacific herring Clupea pallasii to investigate the kinetics of viral shedding and its effect on disease transmission and host mortality. Outbreaks of acute disease, accompanied by mortality and viral shedding, were initiated after waterborne exposure of herring to concentrations of VHSV as low as 10 1 plaque-forming units (pfu) ml -1 . Shed virus in flow-through tanks was first detected 4 to 5 d post-exposure, peaked after 6 to 10 d, and was no longer detected after 16 d. Shedding rates, calculated from density, flow and waterborne virus titer reached 1.8 to 5.0 × 10 8 pfu fish -1 d -1. Onset of viral shedding was dose-dependent and preceded initial mortality by 2 d. At 21 d, cumulative mortality in treatment groups ranged from 81 to 100% and was dependent not on challenge dose, but on the kinetics and level of viral shedding by infected fish in the tank. Possible consequences of the viral shedding and disease kinetics are discussed in the context of epizootic initiation and perpetuation among populations of wild Pacific herring. KEY WORDS: Viral shedding · VHSV · Pacific herring · Clupea pallasii · Disease ecology Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 400: [187][188][189][190][191][192][193] 2010 herring populations in Prince William Sound, Alaska, involves excess mortality from disease (Marty et al. 1998(Marty et al. , 2003, although the precise role of VHS remains controversial (Elston & Meyers 2009).Factors contributing to the onset of VHS epizootics in populations of wild marine fishes are not well understood, but initial infection occurs following direct contact with exogenous waterborne virus (Kocan et al. 2001a). Laboratory studies show that epizootics are readily initiated in naïve stocks of Pacific herring after a 1 h waterborne exposure to moderate levels (10 3 plaque-forming units [pfu] ml -1 ) or greater of VHSV (Kocan et al. 1997). However, field surveys have detected only low titers of virus (5 to 15 pfu ml -1 ) in samples of marine water collected in the vicinity of free-ranging schools of herring (Hershberger et al. 1999).The objectives of this study were to determine the minimum exposure thresholds required to initiate epizootics of VHS in Pacific herring and to quantify the kinetics of viral shedding from infected fish. These empirically deduced infection thresholds and virus shedding rates are discussed in the context of disease initiation and perpetuation in wild marine fishes. MATERIALS AND METHODSMinimum exposure levels required to initiate VHS epizootics in groups of 1+ yr old (mean length = 100 mm, SD = 7.2 mm), specific pathogen-free (SPF) Pacific herring (Hershberger et al. 2007) were determined by immer...

Chronic and persistent viral hemorrhagic septicemia virus infections in Pacific herring

“…In addition to acute manifestations of VHS in Pacific herring which are well-documented (Kocan et al 1997, Hershberger et al 2006, 2007, 2010a, we found that the disease can also manifest in this species as a chronic form that is characterized by viral persistence within infected hosts for extended periods with nearbackground levels of VHS-specific host mortality (Fig. 1, Table 1).…”

“…An apparent paradox exists when considering the persistence of VHSV in natural populations of Pacific herring where it is thought that high VHSV shedding rates from infected individuals contribute to virus perpetuation through a process of continuous transmission from infected to uninfected individuals (Kocan et al 2001, Hershberger et al 2010a). This means of perpetuation can only persist within a narrow range of the basic reproduction number (R 0 ), the average number of infected individuals resulting from a single infected host (Ostfeld 2009).…”

“…Once exposed, laboratory stocks of Pacific herring typically experience acute disease followed by rapid mortality (Kocan et al 1997), and epizootics in the wild are likely initiated as a result of a combination of environmental stressors and concentration or amplification mechanisms associated with viral shedding from infected individuals within a school (Hershberger et al 2010a). Individuals that survive these epizootics become refractory to disease, indicating the involvement of a protective adaptive immune response (Kocan et al 2001, Hershberger et al 2007, 2010b).…”

Complementary approaches to diagnosing marine diseases: a union of the modern and the classic

“…Molecular tools led to a better understanding of the differences among different VHSV strains, including virulence and host susceptibilities. The combined tools of the epidemiologist and the molecular virologist have clarified transmission dynamics of this pathogen and its rhabdovirus cousins, infectious haematopoietic necrosis virus and spring viraemia of carp virus [12][13][14]. Risk-based surveillance has controlled disease in aquaculture settings, resulting in the elimination of VHSV from Denmark's rainbow trout O. mykiss farms [15].…”

Principles underlying the epizootiology of viral hemorrhagic septicemia in Pacific herring and other fishes throughout the North Pacific Ocean

“…After exposure to the virus and successful establishment of infection, Pacific herring and other species shed copious amounts of VHSV into the water (Kocan et al 1997;Hershberger et al 2010a;Kim and Faisal 2012). Shed VHSV can be detected in the water as early as 4-5 days postexposure (PE), prior to the onset of host mortality from the resulting disease.…”