Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata

Abstract

The aim of the present study was to determine whether Enteromyxum leei, one of the most threatening parasitic diseases in Mediterranean fish culture, could be transmitted by peranal intubation in gilthead sea bream Sparus aurata L. Fish were inoculated either orally or anally with intestinal scrapings of infected fish in 3 trials. Oral transmission failed, but the parasite was efficiently and quickly transmitted peranally. Prevalence of infection was 100% at 60 d post inoculation (p.i.) in Trial 1 under high summer temperature (22 to 25°C; fish weight = 187.1 g), and 85.7% in just 15 d p.i. in Trial 3 using smaller fish (127.5 g) at autumn temperature (19 to 22°C). In Trial 2, prevalence reached 60% at 60 d p.i. in the group reared at constant temperature (18°C), whereas no fish was infected in the group that was kept at low winter temperature (11 to 12°C), although infection appeared (46.1% at 216 d p.i.) when temperature increased in spring. The arrested development at low temperature has important epidemiological consequences, as fish giving false negative results in winter can act as reservoirs of the parasite. Histopathological examination showed a posterior-anterior intestinal gradient in the progression of the infection, in terms of both intensity and parasite maturation. Thus, peranal intubation provides a very uniform, reliable and faster mode of transmission of E. leei than the commonly used transmission methods (cohabitation, exposure to infected effluent and oral inoculation), which require long exposure times or give variable and unpredictable results.

Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei

“…Enteromyxum leei is a myxosporean enteric parasite seriously affecting Mediterranean sparid cultures (Palenzuela, 2006;Sitjà-Bobadilla and Palenzuela, 2011). The parasite has been experimentally transmitted by cohabitation with infected fish, oral intubation with infected intestinal scrapings, exposure to water from infected tanks (effluent transmission) and by anal intubation (Diamant, 1997;Diamant and Wajsbrot, 1997;Sitjà-Bobadilla et al, 2007;Estensoro et al, 2010). It was first described in cultured gilthead sea bream (Diamant, 1992) but it has since been detected in many ornamental and cultured fish in the Canary Islands, the Mediterranean and Red Sea and in Western Japan .…”

Early diagnosis of enteromyxosis in intensively reared sharpsnout seabream,Diplodus puntazzo

“…Arrested development, or latency in the host at low water temperatures is probably the explanation for infected fish in such cases (Olson 1981), while the infective dose in the water during winter is not enough to establish successfully the infection (Alama-Bermejo et al 2013), as in case of the present study. Mature spores can survive in seawater during cold seasons, while parasite's viability may be supported by several parameters, such as its localization in intestinal mucosal remnants and its ability to remain infectious despite temperature and salinity fluctuations (Ibarra et al 1992;Yokoyama and Urawa 1997;Estensoro et al 2010).…”

“…Moreover, infected fish that survived through parasitosis developed self-recovery immune mechanisms preventing reinfection while the parasite was easily rejected since located in the intestine. Recovery mechanisms of infected fish have been reported in case of enteromyxosis (Golomazou et al 2006a, b;Yanagida et al 2006;Estensoro et al 2010) and the ability of fish to recover successfully from E. leei infection could be partly related to certain immune response mechanisms such as the capacity of the organism to restore peroxidases to preinfection levels (Munoz et al 2007). Furthermore, the cellular response of infected fish is activated involving elements of innate and adaptive immunity (Estensoro et al 2014;Davey et al 2011).…”

“…This ease of transmission, in combination with the abundance of invertebrates and wild fish, which act as reservoirs of these myxosporeans, are also responsible for the spread of the disease under farmed conditions and hamper its prevention and control. Myxozoan infection depends on water temperature and enteromyxosis outbreaks have been reported at high water temperatures (Le Breton and Marques 1995;Golomazou et al 2005;Palenzuela 2006;Yanagida et al 2006), while low water temperature is considered as an inhibitory factor for the development of the disease (Estensoro et al 2010).…”

“…E. leei is usually detected by classical parasitogical diagnostic techniques, when the dissemination of the disease has been already occurred, causing high mortalities to infected fish. DNA-based assays have also been described for the detection of myxosporeans in fish including Enteromyxum species (Fox et al 2000;Cavender et al 2004;Kelley et al 2004;Yanagida et al 2005;Hallett and Bartholomew 2006;Sitjà-Bobadilla et al 2007;Griffin et al 2009;Estensoro et al 2010;Hunt 2011;Piazzon et al 2012;Alonso et al 2014). However a robust validated molecular diagnostic technique, which could be applied for simultaneous detection and quantification of this parasite, has never been applied to date on any host species.…”