Disseminated neoplasia in flat oysters Ostrea edulis from Galicia (NW Spain): Occurrence, ultrastructural aspects and relationship with bonamiosis

Abstract

Disseminated neoplasia (DN) was one of the most important pathological conditions found in cultured flat oysters (Ostrea edulis) from different geographical origins grow in Galicia (NW Spain), during a two years selective breeding programme to produce oysters less susceptible to bonamiosis. Histological characteristics observed in oysters affected by DN included intense infiltration of connective tissue of various organs (gills, stomach, digestive gland and gonad) by large undifferentiated cells, with a large nucleus and a high nucleus-to-cytoplasm ratio. The main ultrastructural features were predominance of euchromatin over heterochromatin that was arrayed in small clumps in the nucleus, prominent granular nucleolus, swollen mitochondria with few cristae and high number of free ribosomes in the cytoplasm. A seasonal pattern of DN prevalence was detected, with higher values in spring–summer, but there were no significant differences between geographic origins or families within these origins. However, the intensity of the disease was significantly different between origins; oysters originating outside of Galicia (particularly those originating from Ireland) were more susceptible to develop advanced DN. DN (8%) and bonamiosis (4.9%) were found concurrently in oysters. The nature and significance of this association warrants more investigation to determine its importance, if any.

Introduction

Disseminated neoplasia (DN) has been detected in many bivalve species worldwide, including edible species of oysters (Crassostrea spp. and Ostrea spp.), mussels (Mytilus spp.), cockles (Cerastoderma edule) and clams (Mya arenaria and Macoma balthica) (reviews of Peters, 1988, Elston et al., 1992, Barber, 2004, Ciocan and Sunila, 2005). However, this disease, which can be associated with high mortality, is still poorly understood (Barber, 2004). The cell or tissue of origin remains unknown and this fact has resulted in a variety of descriptive names for the disease (Barber, 2004). Most terms, such as haemic neoplasia, leukaemia (Krishnakumar et al., 1999) and haemic sarcoma (Rodríguez et al., 1997), suggested that cells are haematopoietic in origin; others terms, such as disseminated sarcoma (Peters, 1988) and systemic neoplasia (Moore et al., 1991), emphasized the invasive character. The nomenclature accepted for use, disseminated neoplasia (Peters, personal communication), is the most conservative one and was suggested by Elston et al. (1992). In addition, its etiological agent has never been definitively elucidated and there are continuous controversies surrounding this topic (Barber, 2004) evidenced by several hypotheses postulated to explain the origin of the disease, such as genetic mechanisms or chemical contamination (Peters, 1988, Elston et al., 1992, Barber, 2004, Smolarz et al., 2006). But some cases of chemical contamination fail to explain occurrence of the disease (Krishnakumar et al., 1999, Smolarz et al., 2005a). The disease had been experimentally transmitted from affected individuals to healthy ones, supporting the hypothesis of an infectious agent (Elston et al., 1992, Collins and Mulcahy, 2003, Barber, 2004). Indeed, reverse transcriptase activity indicated the presence of a retrovirus in neoplastic cells of M. arenaria (Medina et al., 1993, House et al., 1998) and, the cockle C. edule (Romalde et al., 2007) from Galicia. However, recent findings suggest that the reverse transcriptase activity is not related to retrovirus but due to activation of endogenous retroelements (AboElkhair et al., 2009).

In flat oysters from Galicia, DN was first reported by Alderman et al. (1977) in the Ría de Nóia-Muros and later by Figueras (1991) in the Ría de Vigo. The latter report found cases of animals concurrently affected by DN and infected by Bonamia ostreae, but there was no analysis of this association.

Bonamiosis is an epizootic disease affecting several oyster (Ostrea edulis) beds in Galicia (NW Spain) since the 1980s (Polanco et al., 1984). A selective breeding programme to produce a resistant strain of oyster O. edulis was started, in 2001, in Galicia. A preliminary study compared disease susceptibility and productive traits among European oyster stocks, which had been shown to be genetically different; the objective was to identify oyster populations that could be used to initiate selective breeding (da Silva et al., 2005a).

This paper represents part of the results obtained in that project. We report the prevalence of DN in families of oysters derived from four European oyster stocks and its relationship with bonamiosis. In addition, we provide new insights on morphological and ultrastructural aspect of the DN in oysters from Galicia.