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Horizontal Transmission Dynamics of White Spot Syndrome Virus By Preventive Veterinary Medicine 117 (2014) 286–294 CORE Metadata, citation and similar papers at core.ac.uk Contents lists available at ScienceDirect Provided by Elsevier - Publisher Connector Preventive Veterinary Medicine j ournal homepage: www.elsevier.com/locate/prevetmed Horizontal transmission dynamics of White spot syndrome virus by cohabitation trials in juvenile Penaeus monodon and P. vannamei a,b,∗ c d a N.X. Tuyen , J. Verreth , J.M. Vlak , M.C.M. de Jong a Quantitative Veterinary Epidemiology Group, WU Animal sciences, Wageningen University, Radix Building, Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands b Research Institute for Aquaculture No. 2, 116 Nguyen Dinh Chieu St., HoChiMinh City, Viet Nam c Aquaculture and Fisheries Group, WU Animal Sciences, Wageningen University, 6700AH Wageningen, The Netherlands d Laboratory of Virology, Wageningen University, Wageningen, The Netherlands a r t i c l e i n f o a b s t r a c t Article history: White spot syndrome virus (WSSV), a rod-shaped double-stranded DNA virus, is an infec- Received 17 December 2013 tious agent causing fatal disease in shrimp farming around the globe. Within shrimp Received in revised form 21 July 2014 populations WSSV is transmitted very fast, however, the modes and dynamics of trans- Accepted 14 August 2014 mission of this virus are not well understood. In the current study the dynamics of disease transmission of WSSV were investigated in small, closed populations of Penaeus monodon Keywords: and Penaeus vannamei. Pair cohabitation experiments using PCR as a readout for virus infec- White spot syndrome virus tion were used to estimate transmission parameters for WSSV in these two species. The Penaeus monodon mortality rate of contact-infected shrimp in P. monodon was higher than the rate in P. Penaeus vannamei vannamei. The transmission rate parameters for WSSV were not different between the two Pair cohabitation species. The relative contribution of direct and indirect transmission rates of WSSV differed Transmission rate parameter Basic reproduction ratio between the two species. For P. vannamei the direct contact transmission rate of WSSV was significantly lower than the indirect environmental transmission rate, but for P. monodon, the opposite was found. The reproduction ratio R0 for WSSV for these two species of shrimp was estimated to be above one: 2.07 (95%CI 1.53, 2.79) for P. monodon and 1.51 (95%CI 1.12, 2.03) for P. vannamei. The difference in R0 between the two species is due to a lower host mortality and hence a longer infectious period of WSSV in P. monodon. © 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). 1. Introduction Zhangpu in Fujian Province, China (Lo et al., 2005). Within two years, Taiwan reported that WSSV caused disease in White spot syndrome virus (WSSV) is a serious three cultured shrimp species Penaeus monodon, P. japoni- pathogen of penaeid shrimp. Outbreaks of WSSV were first cus, and P. penicillatus (Chou et al., 1995). Within a decade reported in 1992 for cultured Penaeus japonicus shrimp in from these first observations WSSV had spread very fast and caused losses in fourteen shrimp producing countries of Asia (NACA, 2002). In 1995, WSSV was found in shrimp farms along the coastal area in the Gulf of Mexico (Lightner ∗ Corresponding author at: Quantitative Veterinary Epidemiology et al., 1997). Subsequently WSSV was reported in nine Group, WU Animal sciences, Wageningen University, Radix Building, countries in the Americas (OIE, 2003), most notably in Droevendaalsesteeg 1, 6708PB Wageningen, The Netherlands. Brazil (Cavalli et al., 2008) and Argentina (Martorelli et al., E-mail addresses: [email protected], [email protected] (N.X. Tuyen). 2010). WSSV is now considered a global epidemic, having http://dx.doi.org/10.1016/j.prevetmed.2014.08.007 0167-5877/© 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/3.0/). N.X. Tuyen et al. / Preventive Veterinary Medicine 117 (2014) 286–294 287 also recently been found in Saudi Arabia and off the African cohabitation of infected and susceptible shrimp (Soto and coast in Madagascar (Flegel, 2012). Transmission of WSSV Lotz, 2001). In that paper four experimental groups were between countries is thought to occur mainly through the used starting with one infected shrimp and 12 susceptible transport of both live and frozen uncooked shrimp (Nunan in-contact shrimp. The results showed that contact infec- et al., 1998; Durand et al., 2000), as well as imports of brood tion was only observed in one. It can be concluded that they stock with latent WSSV (Stentiford et al., 2012). only observed a minor outbreak with a reproduction ratio A typical outbreak in cultured shrimp starts one or R0 (the average number of new cases caused by one typical two days after the introduction of virus or virus-infected infected shrimp in a susceptible population) estimated less shrimp and is usually followed by a mass mortality of up to than one (Diekmann et al., 1990; de Jong, 1995). However, 70–100% of the shrimp population in the next five to seven the R0 should be larger than one. Their experiments still days (Chou et al., 1995). P. monodon, infected by WSSV, leave the possibility for R0 > 1, as their results the estimated often show reduced movement and food consumption, dis- R0 = 0.22 with 95% confidence interval (0.0065; 2.15), cal- coloration of the body from pinkish to reddish, occurrence culated as described in van der Goot et al. (2005). However, of white spots of 0.5–2.0 mm in diameter under the surface to obtain an estimate for R0 with narrow confidence inter- of the exoskeleton, and rapid mortality (Lightner, 1996). vals pairwise cohabitation experiments are better suited WSSV is a non-occluded virus (Wang et al., 1995) with (Velthuis et al., 2002). a large double-stranded super-coiled DNA genome that The purpose of this paper was therefore to use pair- varies in size from 292.96 to 305.1 kilobase pairs in size wise cohabitation experiments, (i.e. one infected shrimp (van Hulten et al., 2001; Yang et al., 2001). It was classified cohabitated with one healthy shrimp), to estimate the to belong to the genus Whispovirus of a newly established transmission rate and mortality rate parameters for WSSV virus family Nimaviridae (Lo et al., 2011). in the two shrimp species that are most frequently used As reviewed by Sánchez-Paz (2010), WSSV has a wide in the production of Penaeus vannamei and P. monodon. range of arthropods, particularly of decapods, as hosts In addition we wanted to know which routes of trans- and carriers which have been identified in both challenge mission are responsible for the transmission of WSSV in experiments and in the wild. All cultured marine shrimps these species and whether or not they differ between are susceptible to WSSV (Walker and Mohan, 2009). Other the two species. To that end we compared transmission aquatic and benthic organisms can be virus carriers or between pairs of shrimp where we removed dead shrimp reservoirs and these include polychaete worms (Vijayan as quickly as possible (‘remove’) and pairs where the dead et al., 2005; Desrina et al., 2013), microalgae (Liu et al., shrimps were left (‘keep’). Also we estimated transmission 2007) and rotifer eggs (Yan et al., 2004). rate parameters both for the transmission between in- WSSV can transmit between individuals of the same contact shrimp (direct contact transmission) and spatially host species (Chou et al., 1998) or between different host separated shrimp in the same tank (indirect environment species (Waikhom et al., 2006). Horizontal transmission transmission). of WSSV within a host population is influenced by partic- ular biological factors, including aggressive behavior and 2. Materials and methods predation (Wu et al., 2001; Soto et al., 2001), different ages of shrimp (Lightner et al., 1998; Venegas et al., 2000), 2.1. Virus and inoculum preparation difference in the virulence of WSSV strains (Wang et al., 1999; Marks et al., 2005; Zwart et al., 2010), virus passing The WSSV strain (VN-T) used to prepare the inoculum through different hosts (Lightner et al., 1998; Rajendran was derived from diseased P. monodon collected from a et al., 1999; Waikhom et al., 2006), high densities of hosts farm in the Central region of Vietnam (Dieu et al., 2004). (Wu et al., 2001) and meteorological conditions (Tendencia Virus propagated once through Orconectes limosus cray- et al., 2011). Physiological stressors such as water quality fish (Jiravanichpaisal et al., 2001) was used as an inoculum parameters (temperature, dissolved oxygen, salinity, etc.), for P. vannamei and virus propagated once through juve- outside the optimal ranges for shrimp growth can also nile P. monodon was used as an inoculum for P. monodon. influence transmission (Rahman et al., 2006; Esparza-Leal WSSV was purified from ∼10 g gill tissue homogenized in et al., 2010; Gunalan et al., 2010). Transmission through dif- 500 ml TNE buffer (50 mM Tris–HCl, 400 mM NaCl, 5 mM ferent infection routes (Soto and Lotz, 2001) can affect the EDTA; pH 8.5) as described by Xie et al. (2005). After the rate of horizontal transmission of WSSV, and there is also addition of the protease inhibitors phenylmethylsulfonyl evidence that WSSV can be vertically transmitted to the fluoride, benzamidine, and Na2S2O5 each to a 1 mM final next generation from brooders (Lo et al., 1997; Hsu et al., concentration, the homogenate was centrifuged at 3500 × g ◦ 1999). Observationally epidemiological studies on the risk for 5 min at 4 C.
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