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Huffmanela Spp. (Nematoda, Trichosomoididae) from Microchirus Azevia: Tissue Location and Correspondence of Host Muscle Discoloration with Parasite Burden

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Huffmanela Spp. (Nematoda, Trichosomoididae) from Microchirus Azevia: Tissue Location and Correspondence of Host Muscle Discoloration with Parasite Burden Journal of Fisheries and Aquatic Science ISSN 1816-4927 www.academicjournals.com OPEN ACCESS Journal of Fisheries and Aquatic Science ISSN 1816-4927 DOI: 10.3923/jfas.2016.304.310 Research Article Huffmanela spp. (Nematoda, Trichosomoididae) from Microchirus azevia: Tissue Location and Correspondence of Host Muscle Discoloration with Parasite Burden 1Alexandra Esteves, 2Irene Oliveira, 3Paula Ramos, 4Ana Carvalho, 5Nuno Nazário and 1Fernanda Seixas 1Department of Veterinary Sciences, Animal and Veterinary Research Centre (CECAV), Universidade de Trás-os-Montes e Alto Douro (UTAD), 1013 Apartado, 5001-801, Vila-Real, Portugal 2Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), Universidade de Trás-os-Montes e Alto Douro (UTAD), 1013 Apartado, 5001-801, Vila-Real, Portugal 3Laboratory for Pathology of Aquatic Animals, Portuguese Institute of the Sea and Atmosphere (IPMA), I.P. Avenida de Brasília, 1449-006 Lisboa, Portugal 4Veterinary Surgeon, Universidade de Trás-os-Montes e Alto Douro (UTAD), 1013 Apartado, 5001-801, Vila-Real, Portugal 5General Directorate for Veterinary and Food, Ministry of Agriculture, Rural Development and Fishery (DGAV), Ministério de Agricultura, do Desenvolvimen to Rural e Pescas, Largo da Academia Nacional das Belas Artes, nº2, 1249-105, Lisboa, Portugal Abstract Forty four samples of Microchirus azevia (de Brito Capello) were analyzed, 75% of which presented black discoloration of musculature. Usually, the specimens presenting this black discoloration are rejected as unfit for consumption. Bipolar eggs somewhat resembling those of the nematode genus Huffmanela (Nematode, Trichosomoididae) were identified as the cause of the colour changes on the fish muscle. From this study it can be concluded that, although the skin can work as a camouflage for the observed color changes, there is a statistically significant relationship between the degree of color change and the number of eggs microscopically observed per field. The existence of a positive association (using SCA) between the classification of color changes before and after skin removal is a positive aspect regarding the validation of the veterinary inspector’s work when evaluating fish. It is important to highlight that some of the samples without skin color changes at microscopic examination presented trichinelloid eggs. The identification of Huffmanela sp. in a new host (Microchirus azevia) and the evidence that the presence of this parasite is not always accompanied by macroscopically evident changes, strengthens the belief that this infection may have been often underdiagnosed. Key words: Huffmanela, Microchirus azevia, discoloration grade, eggs location Received: February 04, 2016 Accepted: March 22, 2016 Published: June 15, 2016 Citation: Alexandra Esteves, Irene Oliveira, Paula Ramos, Ana Carvalho, Nuno Nazário and Fernanda Seixas, 2016. Huffmanela spp. (Nematoda, Trichosomoididae) from Microchirus azevia: Tissue location and correspondence of host muscle discoloration with parasite burden. J. Fish. Aquat. Sci., 11: 304-310. Corresponding Author: Alexandra Esteves, Department of Veterinary Sciences, Animal and Veterinary Research Centre (CECAV), University of Trás-os-Montes e Alto Douro (UTAD), Quinta de Prados, Bloco Laboratorial, B1.03 5001-801 Vila Real, Portugal Tel: 351 259 350 659/351 259 350 480 Copyright: © 2016 Alexandra Esteves et al. This is an open access article distributed under the terms of the creative commons attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited. Competing Interest: The authors have declared that no competing interest exists. Data Availability: All relevant data are within the paper and its supporting information files. J. Fish. Aquat. Sci., 11 (4): 304-310, 2016 INTRODUCTION associated and (3) To provide a microscopic description of the affected tissues and eventually search for new locations on Microchirus (Zevaia) azevia Capello, 1867 is present on fish organism with the aim of contributing to a better a demersal habitat on mud and sand of continental shelf from understanding of the Huffmanela sp., biology. the shore down to 250 m. Its food consists of a wide range of small benthic invertebrates, mainly amphipods and MATERIALS AND METHODS polychaetes (Algeria). Its distribution includes the Eastern Atlantic (Portugal Southward; a single record from South-West The analyzed sample consisted of 44 Microchiru sazevia of the British Isles) and the Mediterranean (Western portion, obtained on Atlantic coast from 12 catches in different days. Spain and Algeria) (http://species-identification.org/species. From the analyzed fish specimens, 33 (75%) exhibited php?species_group=fnam&id=1995). unusual black discoloration on the dorsal and ventral Veterinaries working at auction centers on the Portuguese musculature and 11 (25%) didn’t exhibit any discoloration coast have described the presence of unusual black change. discoloration on musculature of the pleuronecti form fish All specimens were measured, weighed and classified in Microchirus azevia (de Brito Capello). These color changes are a three grades system, based on the degree of discoloration of evident on the ventral (blind) face and also on dorsal faces of the ventral surface as observed through the skin, as grade (0) theses specimens. Usually, the specimens presenting this Specimens presented no skin color change; grade (1) black discoloration are rejected by fishermen or classified as Specimens presented a slight black discoloration of the skin unfit for consumption by veterinarian services due to their and grade (2) Specimens showed pronounced black repulsive appearance. discoloration. At a preliminary stage, it is verified that these unusual After this preliminary classification, ventral skin was color anomalies (black discolorations) of the muscle could removed from fish specimens, exposing the musculature. be explained by the presence of dark brown nematode Specimens were then subject to a reclassification and eggs compatible with genera Huffmanela. Huffmanela considering the degree of muscle discoloration as it was Moravec et al.1 comprises 20 valid species2-7 of extra-intestinal previously described. This classification was adapted from the nematodes, whose adults deposit eggs in the skin, gill, somatic one proposed by Mendes et al.12 for Trisopterus lucus. musculature, swimbladder, bone and mesenteries5,6. The fish were then subject to post mortem examination Advanced dark-shelled eggs of this parasite occur at the histopathology laboratory of the Universidade de frequently in masses in the host fish’s tissues, appearing as Trás-os-Montes e Alto Douro and fixed in 10% formalin. Tissue black spots. The eggs are lead with thin shells and then in the samples were processed for light microscopy in accordance host tissue, they increase in size and change in colour. The with standard methods, sectioned at 3 :m and stained with chitinous layer of the egg shell becomes thicker and gradually Haematoxylin and Eosin (H and E). turns from colourless to brown or even black8. To confirm whether the macroscopic discoloration Taxonomy of Huffmanela spp. has largely been based grading was in accordance with the parasitism intensity, the on egg morphology with considerations of host affiliation, egg number of eggs were evaluated microscopically on infection site and host geographic location1-4,9-11. Huffmanela longitudinal sections of the muscle. Ten microscopic sp. had already been described in the gadid Trisopterus luscus consecutive fields of muscle tissue were evaluated, using a 20x Linnaeus caught off the Portuguese coast by Mendes et al.12 power magnification objective in a blind trial and the eggs and redescribed by Esteves et al.10. average was calculated. To allow a better characterization of In the present study, it is evaluated that 44 Microchiru the eggs, in the absence of fresh samples, the fixed muscle sazevia, 75% of which presented black discoloration in the was submitted to muscle scraping and then the eggs were muscle. The aims of the present study were (1) to confirm the wet-mounted in lactophenol on cover slipped glass slides and presumptive diagnosis that the black discoloration observed photographed using a light microscope (Nikon Eclipse E600) on Microchirus azevia specimens were due to the presence equipped with a camera (Nikon DXM 1200) and the Image J of nematode eggs of the genus Huffmanela, (2) To confirm version 1.44o software. Fifty six eggs were measured in whether the degree of discoloration of fish and the observed micrometers and data were expressed as Mean±Standard number of eggs, counted in histological sections were Deviation (SD). 305 J. Fish. Aquat. Sci., 11 (4): 304-310, 2016 Statistical analysis: Statistical analysis was performed using Kruskal-Wallis test was used to compare fish size, fish SPSS software (version 20.0 SPSS Inc., Chicago). To study the weight and egg counts among the 3 discoloration grades and statistical analysis associations between the discoloration the Dunn test, as post hoc test for multi comparison between degree on samples before and after removal of the ventral groups, when applicable. Values of p<0.05 were considered as skin, a chi-square test with residual adjusted values was used. statistically significant. If p was lower than 0.05 cells containing adjusted residuals above |2.0| were analyzed. Due to small sample size, a Monte RESULTS Carlo correction was
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