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��ࡱ�>��	��������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������+QbjbjW�W�>�5�5��GG�������ggggg����{{{8�<�4{�3�##(KKK&&&`3b3b3b3b3b3b3$y6�+9f�3-g&&&&&�3ggKK��3(!(!(!&�gKgK`3(!&`3(!(!::&,�&K������s�^#�������f&
L3�30�3p&.�9~ p�9�&�&��9g ',&&(!&&&&&�3�3� :&&&�3&&&&���������������������������������������������������������������������9&&&&&&&&&+-:Hepatic steatosis in young cobia, Rachycentron canadum (Linnaeus, 1766), raised in net pens in Brazil

M T Shimada1, G S Claudiano2, J R Engracia Filho2,4, F R Moraes2, R G Moreira3 and J R E Moraes1,2

1 � Aquaculture Center of Unesp (Caunesp), S�o Paulo State University (UNESP), Via Prof. Paulo Donato Castellane, km 05, Jaboticabal, SP 14884-900, Brazil 
2 � Department of Veterinary Pathology, School of Agrarian and Veterinary Sciences, S�o Paulo State University (UNESP), Via Prof. Paulo Donato Castellane, km 05, Jaboticabal, SP 14884-900, Brazil
3 � Department of Physiology, Institute of Biosciences, University of S�o Paulo, Rua do Mat�o, travessa 14, n.321- sala 220, Cidade Universit�ria - S�o Paulo � SP, Brazil 
4 � School of Agricultural Sciences and Veterinary Medicine, Pontifical Catholic University of Paran�, Curitiba/PR, Brazil 

*Corresponding author. Tel.: +55 (016) 997852072.
E-mail address: julietaengracia@gmail.com (J.R.E. de Moraes). 
�

Running title
Steatosis in cobia.
Abstract
This article discusses the pathophysiology of hepatic steatosis in cobias, which were raised in net pens at two different fish farms with growth interference and predisposition to opportunistic diseases. We necropsied cobia with a history of relatively slow growth and high mortality, lethargy, fin ulceration, depigmentation, physical deformities, and certain external parasites. On the microscopic exam, we observed that the liver was increased in volume and pallid, with a softened or friable consistency. Liver fragments were collected, fixed in ten percent formaldehyde buffer or frozen to obtain histological slices, and stained with hematoxylin-eosin or Sudan black, respectively. The histopathological exam revealed increased volume of the hepatocytes, an increase in volume, cytoplasmic macrovacuoles with well-defined edges, and peripheral nuclei. Staining with Sudan black revealed black-colored vacuoles, which allowed steatosis to be diagnosed. The provision of fish meal reduced the severity of steatosis. A portion of the dry feed fish used in one of the fish farms was analyzed for fatty acids. We verified an imbalance in the proportion of fatty acids, which was characterized by a higher quantity of oleic acid than docosahexaenoic acid. This imbalance may have favored the observed accumulation of lipids.

Keywords: teleostei, saltwater fish, fatty acids, liver, histology.
Introduction
	Compared to mammals, fish have a greater quantity of vacuolized hepatocytes due to increased glycogen or lipid content, which differ between them in proportion to their state of health [1]. In captive fish, lipid vacuolization is obvious and uniform, as a result of artificial feeding that promotes disequilibrium between the capture of fatty acids (FAs) by hepatocytes and their metabolism and use [2].
	During lipid metabolism, the liver synthesizes and degrades FAs and esterifies lipids by triglycerides (TGs). An imbalance in the types of FA in the diet can generate fat metamorphosis and steatosis, characterized by the abnormal accumulation of TGs in hepatocytes. Steatosis leads to a pallid liver with cytoplasmic vacuolization of the hepatocytes. Vacuoles can vary in size, but large vacuoles can dislocate the nucleus to the cell periphery because of the fat�s greater relatively high density of fat [3]. 
	Few studies are available in the literature concerning hepatic steatosis in marine organisms. Rachycentron canadum, or the cobia, is a carnivorous marine teleost and the only remaining Rachycentridae. Found in tropical and subtropical waters, it is migratory, pelagic, and does not form shoals [4]. Cobia is highly marketable as a result of its rapid growth, and marine agriculture has shown increasing interest in the fish [5]. Here we describe the incidence of hepatic steatosis in cobia (R. canadum) raised in net pens on the coast of Brazil. We discuss the pathophysiology of the lesion, its potential interference with growth, and its role in predisposing cobia to illness. 

Materials and Methods
	Young cobias (R. canadum) were collected from two fish farms. The first sampling was performed in 2011 at a fish farm dedicated to fattening, located on the northern coast of the State of S�o Paulo (Site 1). Fish at this site had retarded growth and higher mortality rates. They were raised in net pens and fed only commercial feed for carnivorous saltwater fish; however, from July, they began to be fed fish waste. Sample collection and anatomopathological exams at this location took place in March (n = 8), when the fish were 45 days old (n = 16), July (n = 12), and September (n = 8). In June 2012, sampling was performed at a second fish farm (Site 2) on the southern coast of Rio de Janeiro (n = 15). These fish were raised in an offshore system of net pens and fed a fish paste of moistened freshwater fish feed and sardines, which was cooked in a pressure cooker. Fish at both sites were collected if they were lethargic and had easily identifiable macroscopic changes. 
	The collected fish were submitted to necroscopy. Liver fragments were collected, fixed in 10% buffered formaldehyde, and processed by a routine protocol for making histological slides from paraffin-embedded tissues. Tissue sections of 4 �m in thickness were stained using the hematoxylin and eosin (HE) method and evaluated by light microscopy. Some liver fragments were frozen in liquid nitrogen, sliced, and stained with Sudan black. 
	The FA composition of the feed provided to fish at Site 1 was analyzed. Total lipids were extracted with chloroform: methanol: water (2:1:0.5), in accordance with the method of Folch et al. [7], and the lipid extract was methylated with acetyl chlorate (5% HCl in methanol) [6]. The composition of FAs with methyl esters was determined by using a gas chromatography (GC) machine (Varian model 3900), which was attached to a flame ionizer (FID) and auto-injector. 
	The FAs were analyzed in a CP Wax 52 CB capillary column (0.25 �m thickness, 0.25 mm internal diameter, 30 m length), using hydrogen as a carrier gas at a linear velocity of 22 cm/s. The temperature program was: 170 �C for 1 min, followed by a ramp at 2.5 �C/min up to 240 �C, and a final wait time of 5 min. Temperatures in the injector and in the FID were 250 and 260 �C, respectively. FAs were identified by comparison to the retention time, using a known FA methyl esters (FAME) pattern (Supelco, 37 components; Sigma-Aldrich; Mixture, Me93, Larodan and Qualmix, PUFA fish M, Menhaden Oil, Larodan).

Results
	The external necroscopic exam of fish collected in March 2011 from Site 1 showed fin ulceration and cutaneous depigmentation. Each fish displayed one to four examples of parasites, which were most often located in the dorsal area of the head. Parasites were identified as the monogenoids Neobenedenia melleni and Tuxophorus caligoides. The internal exam of fish collected in 2011 showed a coelomic cavity containing variable amounts of clear liquid. The livers were increased in volume and pallid to varying degrees (Figure 1 A,B). Whitish nodules in the liver with 0.5 to 2.0 mm in diameter and distributed in a diffuse and multifocal way, were identified and characterized histologically as granulomas. 

Figure 1 here

Their microbiological analysis and genotype indicated infection by Photobacterium damselae subsp piscicida, the agent responsible for pasteurellosis or pseudotuberculosis. The most common change in fish collected from Site 2, in 2012 was an extremely pallid liver with an increased volume (Figure 2). 

Figure 2 here

	On the histopathological exam, most (17/24) of the cobia livers collected from Site 1 in March and May 2011 had hepatocytes with increased volume. The hepatocytes were round and had cytoplasmic macrovacuoles with well-defined limits and a peripheral nucleus, distributed in a diffuse way. More than 70% of the histological slice was comprised of macrovacuoles. The findings suggested a lesion with steatosis or fatty metamorphosis (Figure 3A). The severity and distribution of these changes were maintained in livers sampled in May, but there was an increase in the proportion of microvacuoles. 

Figure 3 here

	In July and September, the vacuolization was moderate to discreet, with a reduction in liver compromise. Livers collected from Site 2 in 2012 had microvacuoles with the same characteristics as those above, indicating that the fish had steatosis (Figure 3B). The vacuoles stained black by Sudan black, characteristic of lipids, confirming the diagnosis of steatosis in the cases observed.
	Table 1 shows the composition of FAs in the feed used by Site 1. We verified an imbalance in the proportion of FAs. In particular, there was a higher quantity of oleic acid than docosahexaenoic acid (DHA).

Table 1 here




Discussion
	The changes to the cobia livers�including increased volume, pallid appearance, and histologic presentation of lipid vacuoles stained by Sudan black�were compatible with a diagnosis of steatosis or fatty metamorphosis. This finding generally reflects nutritional and metabolic disturbances [3]. 
	Literature about hepatic steatosis in aquatic organisms, specifically in saltwater fish, is scarce. In freshwater fish, the degradation of excess oleic acid predominantly occurs in peroxisomes. However, it is difficult for saltwater fish to replicate this organelle. This difficulty contributes to the accumulation of FA and the development of steatosis [9]. The accumulation of fat in the liver may be physiological or pathological, although variations in the ability of different species of fish to store lipids make such differentiation difficult. D. labrax normally stores lipids in the liver and S. auratus in adipose tissue. Quantities higher than 45-50% and 10-12%, respectively, in the liver of these species should be considered pathological [10]. However, there are no such data for cobia. 
	In a previous study, Sparus aurata were fed with a feed supplemented with fish oil (100%), soybean oil (60%) + anchovy oil (40%), rape oil (60%) + anchovy oil (40%), linseed oil (60%) + anchovy oil (40%), or soybean oil + rape oil + linseed oil (60%) + anchovy oil (40%) for 6 months and then with anchovy oil (100%) for 95 days. Fish that received linseed oil (60%) had a hepatic morphology similar to those that received anchovy oil (100%). However, those that received soybean oil (60%) had severe steatosis. After a period of re-feeding with anchovy oil (100%), the steatosis receded. These results indicate that non-essential FAs of plant origin induce the appearance of steatosis in the following order: linoleic acid > lineolenic acid > oleic acid. Nevertheless, the changes produced by vegetable oils were reversible; when the fish were re-fed with a diet that included fish oil (100%), the lesion receded [11].
	Steatosis was described in gilthead sea bream (Sparus auratus L.) and sea bass (Dicentrarchus labrax L.), accompanied by higher mortality when natural feed was substituted by artificial feed. The severity of the change was proportional to the time that the fish ingested artificial feed. The introduction of natural feed reduced the severity of the steatosis [9, 12]. In the present study, we noted a similar effect, as cobia fed artificial feed had a severe picture of macrovacuolar steatosis. When artificial feed was substituted for the fish waste (from July 2011), we observed a substitution by microvacuoles and a reduction in the extent of the change to the histological slice, showing that the lesions had grown less severe. In other words, the process reversed. 
	Lipids play an important role in fish nutrition, especially essential FAs. Natural feed for freshwater fish is rich in essential FAs, such as linoleic acid (18:2n-6) and linolenic acid (18:3n-3), and natural feed for saltwater fish is rich in eicosapentaenoic acid (EPA) (20:5n-3) and DHA (22:6n-3) [13]. This difference between fish feeds stems from the inability of saltwater fish to convert essential FAs into DHA and EPA, and is reflected in the specific requirement for FAs to satisfy this need [14, 15] EPA and DHA are fundamental for the optimal growth and development of fish and make up the phospholipids of the cell membrane [16]. 
	Feed for saltwater fish containing a high oleic acid (C18:1n9)/DHA (C22:6n3) ratio and the esterification of DHA lead to TG accumulation in the hepatocytes and steatosis. In the present study, the feed analyzed had a higher quantity of oleic acid than DHA [9], which might have contributed to the accumulation of lipids in the hepatocytes. 
	The liver is responsible for the metabolism of proteins, lipids, and carbohydrates, the synthesis of vitellogenin for gonad growth, the production of immunoglobulins, and the detoxification of xenobiotics [17]. This last function makes the liver the target of various contaminants from the aquatic environment. For this reason, fish are used as bioindicators of environmental pollution through a microscopic evaluation of different organs. Although histopathology has been used to evaluate the direct and indirect effects of toxic agents [18], the structural changes are not specific [19]. Although this research did not cover xenobiotics, steatosis is common in fish exposed to toxic agents [20, 21], such as polyaromatic hydrocarbons, heavy metals [22], and sodium perchlorate [23].
	Lesions compromising more than 70% of the hepatic parenchyma can lead to clinical signs of insufficiency, such as a delay in growth and a predisposition to infections by opportunistic pathogens, followed by higher mortality [3, 9]. In this study, the fish had delayed growth, moderate to severe hepatic steatosis, and infection by P. damselae subsp piscicida, an opportunistic bacterium. The substitution of fish waste improved the picture of steatosis. This result suggests that the occurrence of steatosis was related to the type of feed used previously, in which the proportion of oleic acid (C18:1 n9) to DHA (C22:6 n3) was higher.


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Acknowledgements
We would like to thank the Coordinating Body for Higher Education Professional Development (Coordena��o de Aperfei�oamento de Pessoal de N�vel Superior - Capes), for financing the project conceived by Edital Ci�ncias do Mar 09/2009, which led to this article.









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