Compressed vertebrae in Atlantic salmon Salmo salar: evidence for metaplastic chondrogenesis as a skeletogenic response late in ontogeny

Abstract

Anterior/posterior (a/p) compression of the vertebral column, referred to as 'short tails', is a recurring event in farmed Atlantic salmon. Like other skeletal deformities, the problem usually becomes evident in a late life phase, too late for preventive measures, making it difficult to understand the aetiology of the disease. We use structural, radiological, histological, and mineral analyses to study 'short tail' adult salmon and to demonstrate that the study of adult fish can provide important insights into earlier developmental processes. 'Short tails' display a/p compressed vertebrae throughout the spine, except for the first post-cranial vertebrae. The vertebral number is unaltered, but the intervertebral space is reduced and the vertebrae are shorter. Compressed vertebrae are characterized by an unchanged central part, altered vertebral end plates (straight instead of funnel-shaped), an atypical inward bending of the vertebral edges, and structural alterations in the intervertebral tissue. The spongiosa is unaffected. The growth zones of adjacent vertebrae fuse and blend towards the intervertebral space into chondrogenic tissue. This tissue produces different types of cartilage, replacing the notochord. The correspondence in location of intervertebral cartilage and deformed vertebral end plates, and the clearly delimited, unaltered, central vertebral parts suggest that the a/p compression of vertebral bodies is a late developmental disorder that may be related to a metaplastic shift of osteogenic tissue into chondrogenic tissue in the vertebral growth zone. Given the lack of evidence for infections, metabolic disorders and/or genetic disorders, we propose that an altered mechanical load could have caused the transformation of the bone growth zones and the concomitant replacement of the intervertebral (notochord) tissue by cartilaginous tissues in the 'short tails' studied here. This hypothesis is supported by the role that notochord cells are known to play in spine development and in maintaining the structure of the intervertebral disk.KEY WORDS: Notochord · Skeletal deformities · Vertebral malformations · Metaplasia · Bone · Salmon · Chondrogenesis Resale or republication not permitted without written consent of the publisherDis Aquat Org 64: [237][238][239][240][241][242][243][244][245][246] 2005 be regarded as undeformed (McKay & Gjerde 1986, Madsen et al. 2000. In Atlantic salmon Salmo salar the pronounced a/p compression of the vertebral column results in a phenotype that is characterized by a reduced fork length (FL) and increased body height, traits that result in a deformity-related high condition factor (CF). These individuals are referred to as 'short tails' (Vågsholm & Djupvik 1998).The appearance of 'short tails' is a recurrent problem in salmon farming. The prevalence can vary from year to year, from region to region, and from cage to cage. Some observations suggest that the prevalence of 'short tails' follows a smolt group, with higher frequencies in groups of fast growth smolts...

Unilateral perivertebral fibrosis associated with lordosis, kyphosis and scoliosis (LKS) in farmed Chinook salmon in New Zealand

“…Traumatic injury is a frequent initiator of inflammation in all species. While external trauma is unlikely to cause perivertebral inflammation, spinal curvature in Atlantic salmon has been suggested to be caused by short-term high intensity exercise (Witten et al 2005). This 'mechanical overload' could result because salmon have been selected for large muscles.…”

“…Twenty different spinal deformity subtypes have been described in Atlantic salmon (Witten et al 2009). In this species, vertebral compressions and fusions are reported most frequently and are suspected to be the result of altered vertebral bone development (Witten et al 2005, 2006, Fjelldal et al 2007). In contrast, vertical or horizontal curvature of the spine (lordosis, kyphosis, scoliosis: LKS) is rare in farmed Atlantic salmon (Boglione et al 2013b).…”

Changes in the expression of genetic characteristics across cohorts in skeletal deformations of farmed salmonids

“…On the one hand, the first explanation seems intuitive because egg incubation and early growth are critical phases for skeletal development in fish and other animals [2,30]. On the other hand, the second explanation is supported by detailed studies of fish bone structure, showing that deformations may appear in later life stages [33].…”

“…Deformations occur at high incidence in rare occasions. This results from a major failure in the management system caused, e.g., by a spread of a disease, unusually warm weather conditions during incubation and early growth phases, or inappropriate feed formulation [3,21,32,33]. The factors causing deformations do not need to be the same in all cohorts, and deformations induced by different stressors need not share common genetic origin.…”

Matrix Gla protein in turbot (Scophthalmus maximus): Gene expression analysis and identification of sites of protein accumulation

“…The immunodetection of Mgp in the mineralizing fronts of vertebral arches and spines, and in vertebral growth zones, corroborates previous findings in vertebrates which indicated that Mgp appears first in sites that will be later calcified, functioning early in the bone formation process (Otawara and Price, 1986). The presence of Mgp in these sites may result from the fact that in fish, bone growth occurs (i) in the contact area of opposing vertebral body end plates (Witten et al, 2005), and (ii) at the periphery of arches and spines. Our work is in agreement with other studies which have also reported the presence of Mgp in the mineralization front in fish (Pinto et al 2003 for gilthead seabream; Simes et al 2003 for meagre; among other authors).…”