Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-25T20:14:52.992Z Has data issue: false hasContentIssue false
  • English
  • Français

Early diagnosis of enteromyxosis in intensively rearedsharpsnout seabream, Diplodus puntazzo

Published online by Cambridge University Press:  16 December 2014

Eleni Golomazou ,
Athanasios Exadactylos ,
Emmanouil E. Malandrakis ,
Theodoros Karatzinos ,
Georgios Gkafas ,
Olga Dadali  and
Panagiota Panagiotaki
Get access

Abstract

Myxozoans are metazoan parasites which are highly pathogenic in commercially importantfish, particularly in aquaculture. Enteromyxosis is an economically significant diseasecaused by the myxosporean parasite Enteromyxum leei.Presently, early diagnosis of enteromyxosis in sharpsnout seabream was achieved bymonitoring fish on a time-scale scheduled basis in combination with a validated moleculardiagnostic technique. Two different successive fish batches of a commercial fish farm weremonitored starting from the first month of on-growing in sea cages until fish reachedcommercial size. Fish weight and water temperature differentially ranged between them.E. leei detection was performed both by classical microscopicobservation of fresh smears and by quantitative polymerase chain reaction (qPCR) whileprevalence, mean intensity and mortality rate were calculated. In total, 520 fish werescreened; 320 from the first batch and 200 from the second one. Parasitosis illustrated aseasonal occurrence pattern (spring and summer). When qPCR was used as a diagnosticmethod, enteromyxosis was diagnosed earlier with more increased prevalence compared to themicroscopic observation. In this case, the parasite was detected at the lowest watertemperature that has ever been recorded (14.7 °C), during the first month of on-growing in sea cages. The two-factorcombination of water temperature and fish weight proved to be the most significant factorthat could determine the emergence and development of parasitosis and smaller fish provedto be more susceptible. Mortality was influenced by both prevalence and intensity ofparasitosis. An earlier diagnosis and identification of all developmental stages of theparasite throughout its life cycle was verified with qPCR, significantly before anyoutbreak occurred. The latter could become a key diagnostic tool for the control ofenteromyxosis, allowing stakeholders and fish farmers to adopt all necessary precautionarymeasures minimizing economic loss in sharpsnout seabream intensive farming.

Keywords

Fish diseaseEarly diagnosisEnteromyxosisqPCRMyxozoan parasitesEnteromyxum leeiSparidaeSharpsnout seabream
Type
Note
Information
Aquatic Living Resources , Volume 27 , Issue 2 , April 2014 , pp. 99 - 106
Copyright
© EDP Sciences, IFREMER, IRD 2014

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alama-Bermejo, G., Šíma, R., Raga, J.A., Holzer, A.S., 2013, Understanding myxozoan infection dynamics in the sea: Seasonality and transmission of Ceratomyxa puntazzi. Int. J. Parasitol. 43, 771–780. CrossRefGoogle ScholarPubMed
Alonso M., Lago F.M., Gómez-Reino M., Fernández Casal J., Martín Varela I., Vieites J.M., Espineira M., 2014, Non-invasive fast real-time PCR assay for detection of the enteric parasite Enteromyxum scophthalmi in cultured turbot (Scophthalmus maximus L.) Aquac. Res. 1–12.
Álvarez-Pellitero, P., Palenzuela, O., Sitjà-Bobadilla, A., 2008, Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol. Int. 57, 110–120. CrossRefGoogle Scholar
Bretagne, S., Costa, J., 2006, Towards a nucleic acid-based diagnosis in clinical parasitology and mycology. Clin. Chim. Acta 363, 221–228. CrossRefGoogle ScholarPubMed
Cavender, W.P., Wood, J.S., Powell, M.S., Overturf, K., Cain, K.D., 2004, Real-time quantitative polymerase chain reaction (QPCR) to identify Myxobolus cerebralis in rainbow trout Oncorhynchus mykiss. Dis. Aquat. Org. 60, 205–213. CrossRefGoogle ScholarPubMed
Diamant, A., 1998, Red drum Sciaenops ocellatus (Sciaenidae), a recent introduction to Mediterranean mariculture, is susceptible to Myxidium leei (Myxosporea). Aquaculture 162, 33–39. CrossRefGoogle Scholar
Diamant, A., Ram, S., Paperna, I., 2006, Experimental transmission of Enteromyxum leei to freshwater fish. Dis. Aquat. Org. 72, 171–178. CrossRefGoogle ScholarPubMed
Davey, G.C., Calduch-Giner, J.A., Houeix, B., Talbot, A., Prunet, P., Pérez-Sánchez, J., Cairns, M.T., 2011, Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei. Mol. Immunol. 48, 2102–2112. CrossRefGoogle ScholarPubMed
Estensoro, I.M., Redondo, J., Alvarez-Pellitero, P., Sitjà-Bobadilla, A., 2010, Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata. Dis. Aquat. Org. 92, 51–58. CrossRefGoogle ScholarPubMed
Estensoro, I., Jung-Schroers, V., Álvarez-Pellitero, P., Steinhagen, D., Sitjà-Bobadilla, A., 2013, Effects of Enteromyxum leei (Myxozoa) infection on gilthead sea bream (Sparus aurata) (Teleostei) intestinal mucus: Glycoprotein profile and bacterial adhesion. Parasitol. Res. 112, 567–576. CrossRefGoogle ScholarPubMed
Estensoro, I., Mulero, I., Redondo, M., Álvarez-Pellitero, P., Mulero, V., Sitjà-Bobadilla, A., 2014, Modulation of leukocytic populations of gilthead sea bream (Sparus aurata) by the intestinal parasite Enteromyxum leei (Myxozoa: Myxosporea). Parasitology 141, 425–440. CrossRefGoogle Scholar
FAO, Food and Agriculture Organization of the United Nations, 2011, Fishery and Aquaculture Statistics, Aquaculture Production 2009.
Fleurance, R., Sauvegrain, C., Marques, A., Le Breton, A., Guereaud, C., Cherel, Y., Wyers, M., 2008, Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis. Aquat. Org. 79, 219–228. CrossRefGoogle ScholarPubMed
Fox, M.D., Palenzuela, O., Bartholomew, J.L., 2000, Strategies for the diagnosis of Ceratomyxa shasta using the polymerase chain reaction: Comparison of lethal and nonlethal sampling with microscopic examination. J. Aquat. Anim. Health 12, 100–106. 2.0.CO;2>CrossRefGoogle Scholar
Golomazou, E., Karagouni, E., Athanassopoulou, F., 2005, The most important Myxosporean parasite species affecting cultured Mediterranean fish. J. Hell. Vet. Med. Soc. 55, 342–352. Google Scholar
Golomazou, E., Athanassopoulou, F., Karagouni, E., Tsagozis, P., Tsantilas, H., Vagianou, S., 2006a, Experimental transmission of Enteromyxum leei Diamant, Lom and Dykova, 1994 in sharpsnout sea bream, Diplodus puntazzo C. and the effect on some innate immune parameters. Aquaculture 260, 44–53. CrossRefGoogle Scholar
Golomazou, E., Athanassopoulou, F., Karagouni, E., Vagianou, S., Tsantilas, H., Karamanis, D., 2006b, Efficacy and toxicity of orally administrated anti-coccidial drug treatment on Enteromyxum leei infections in sharpsnout seabream (Diplodus puntazzo C.). Isr. J. Aquac. Bamidgeh 58, 157–169. Google Scholar
Gómez, D., Bartholomew, J., Sunyer, J.O., 2014, Biology and mucosal immunity to myxozoans. Dev. Comp. Immunol. 43, 243–256. CrossRefGoogle ScholarPubMed
Gradil, M.A., Wright, M.G., Wadowska, W.D., Fast, D.M., 2014, Ontogeny of the immune system in Acipenserid juveniles. Dev. Comp. Immunol. 44, 303–314. CrossRefGoogle ScholarPubMed
Griffin, M.J., Pote, L.M., Camus, A.C., Mauel, M.J., Greenway, T.E., Wise, D.J., 2009, Application of a real-time PCR assay for the detection of Henneguya ictaluri in commercial channel catfish ponds. Dis. Aquat. Org. 86, 223–233. CrossRefGoogle ScholarPubMed
Hallett, S.L., Bartholomew, J.L., 2006, Application of a real-time PCR assay to detect and quantify the myxozoan parasite Ceratomyxa shasta in river water samples. Dis. Aquat. Org. 71, 109–118. CrossRefGoogle ScholarPubMed
Hunt, P.W., 2011, Molecular diagnosis of infections and resistance in veterinary and human parasites. Vet. Parasitol. 180, 12–46. CrossRefGoogle ScholarPubMed
Ibarra, A.M., Hedrick, R.P., Gall, G.A.E., 1992, Inheritance of susceptibility to Ceratomyxa shasta (Myxozoa) in rainbow trout and the effect of length of exposure on the liability to develop ceratomyxosis. Aquaculture 104, 217–229. CrossRefGoogle Scholar
Johnson, K.A., Flynn, J.K., Amend, D.F., 1982, Onset of immunity in salmonid fry vaccinated by direct immersion in Vibrio anguillarum and Yersinia ruckeri bacterins. J. Fish Dis. 5, 197–205. CrossRefGoogle Scholar
Katharios, P., Rigos, G., Divanach, P., 2011, Enteromyxum leei (Myxozoa), a lethal intruder of tropical pet fish: First case in humphead wrasse, Cheilinus undulatus (Rüppell, 1835). J. Exotic Pet Med. 20, 138–143. CrossRefGoogle Scholar
Katharios, P., Kokkari, C., Sterioti, A., Smyrli, M., Kalatzis, G.P., 2014, Enteromyxum leei infection in parrotfish, Sparisoma cretense: Histopathological, morphological and molecular study. Vet. Parasitol. 199, 136–143. CrossRefGoogle ScholarPubMed
Kelley, G.O., Zagmutt-Vergara, F.J., Leutenegger, C.M., Myklebust, K.A., Adkison, M.A., McDowell, T.S., Marty, G.D., Kahler, A.L., Bush, A.L., Gardner, I.A., Hedrick, R.P., 2004, Evaluation of five diagnostic methods for the detection and quantification of Myxobolus cerebralis. J. Vet. Diagn. Invest. 16, 202–211. CrossRefGoogle ScholarPubMed
Kent, M., Andree, K.B., Bartholomew, J.L., El-Matbouli, M., Desser, S.S., Devlin, R.H., Feist, S.W., Hallet, S.L., Hedrick, R.P., Hoffmann, R.W., Khattra, J., Lester, R.J.G., Longshaw, M., Palenzuela, O., Xiao, L., 2001, Recent advances in our knowledge of Myxozoa. J. Eukaryot. Microbiol. 48, 395–413. CrossRefGoogle ScholarPubMed
Le Breton, A., Marques, A., 1995, Occurrence of an histozoic Myxidium infection in two marine culture species: Puntazzo puntazzo C. and Pagrus major. Bull. Eur. Assoc. Fish Pathol. 15, 210–212. Google Scholar
Merella, P., Cherchi, S., Salati, F., Garippa, G., 2005, Parasitological survey of sharpsnout seabream Diplodus puntazzo (Cetti, 1777) reared in sea cages in Sardinia (western Mediterranean). Bull. Eur. Assoc. Fish Pathol. 25, 140–147. Google Scholar
Miller M., 1997, RxC, a program for the analysis of contingency tables. Department of Biological Sciences, Northern Arizona University.
Montero, F., Cuadrado, M., Padros, F., Crespo, S., Raga, J.A., 2007, Cryptocaryon irritans and Enteromyxum leei, two threats for the culture of Diplodus puntazzo in the Mediterranean. Bull. Eur. Assoc. Fish Pathol. 27, 242–247. Google Scholar
Muñoz, P., Cuesta, A., Athanassopoulou, F., Golomazou, H., Crespo, S., Padrós, F., Sitjà-Bobadilla, A., Albiñana, G., Esteban, M.A., Alvarez-Pellitero, P., Meseguer, J., 2007, Sharpsnout sea bream (Diplodus puntazzo) humoral immune response against the parasite Enteromyxum leei (Myxozoa). Fish Shellfish Immunol. 23, 636–645. CrossRefGoogle Scholar
Murray, T.S., Cappello, M., 2008, The molecular diagnosis of parasitic diseases. Pediatr. Infect. Dis. J. 27(2), 163–164. CrossRefGoogle ScholarPubMed
Olson, R.E., 1981, Effects of low temperature on the development of the microsporidian Glugea stephani in English sole (Parophrys vetulus). J. Wildlife Dis. 17, 559–562. CrossRefGoogle Scholar
Padros, F., Palenzuela, O., Hispano, C., Tosas, O., Zarza, C., Crespo, S., Alvarez-Pellitero, P., 2001, Myxidium leei (Myxozoa) infections in aquarium-reared Mediterranean fish species. Dis. Aquat. Org. 47, 57–62. CrossRefGoogle ScholarPubMed
Palenzuela, O., 2006, Mixozoan infections in Mediterranean mariculture. Parassitologia 48, 27–29. Google ScholarPubMed
Piazzon, C., Mallo, N., Martin, I., Fernandez-Casal, J., Sanmartin, M.L., Lamas, J., Leiro, J.M., 2012, Development of a real-time PCR assay for detection and quantification of Enteromyxum scophthalmi parasites in turbot intestinal samples. Aquaculture 366–367, 122–128. CrossRefGoogle Scholar
Rigos, G., Katharios, P., 2010, Pathological obstacles of newly introduced fish species in Mediterranean mariculture: a review. Rev. Fish Biol. Fish. 20, 47–70. CrossRefGoogle Scholar
Rigos, G., Christophilogiannis, P., Yiagnisi, M., Andriopoulou, A., Koutsodimou, M., Nengas, I., Alexis, M., 1999, Myxosporean infections in Greek mariculture. Aquac. Int. 7, 361–364. CrossRefGoogle Scholar
Roberts R.J., 1989, Fish pathology. Bailliere, Tindall, London.
Roberts R.J., Shepherd C.J., 1997, Handbook of trout and salmon diseases. Fishing News Books, Oxford.
Sakiti, P.N., Tarer, V., Jacquemin, D., Marques, A., 1996, Présence en Méditerranée occidentale d’une Myxosporidie histozoïque pathogène dans les élevages de daurade, Sparus aurata L. Ann. Sci. Nat. Zool. Paris 17, 123–127. Google Scholar
Sambrook J., Fritsch E.F., Maniatis T., 1989, Molecular Cloning: A Laboratory Manual, second ed. vol. 3. Cold Spring Harbor Laboratory Press.
Sitjà-Bobadilla, A., Diamant, A., Palenzuela, O., Álvarez-Pellitero, P., 2007, Host factors and experimental conditions on the horizontal transmission of Enteromyxym leei (Myxozoa) to gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). J. Fish Dis. 29, 1–8. Google Scholar
Van Lieshout, L., Verweij, J.J., 2010, Newer diagnostic approaches to intestinal protozoa. Curr. Opin. Infect. Dis. 23, 488–493. CrossRefGoogle ScholarPubMed
Yamaguti S., 1963, Systema Helminthum Vol. I-II. Interscience Publishers, New York.
Yanagida, T., Freeman, M.A., Nomura, Y., Takami, I., Sugihara, Y., Yokoyama, H., Ogawa, K., 2005, Development of a PCR-based method for the detection of enteric myxozoans causing the emaciation disease of cultured tiger puffer. Fish Pathol. 40, 22–28. CrossRefGoogle Scholar
Yanagida, T., Sameshima, M., Nasu, H., Yokoyama, H., Ogawa, K., 2006, Temperature effects on the development of Enteromyxum spp. (Myxozoa) in experimentally infected tiger puffer, Takifugu rubripes (Temmink & Schlegel). J. Fish Dis. 29, 561–567. CrossRefGoogle Scholar
Yasuda, H., Ooyama, T., Nakamura, A., Iwata, K., Palenzuela, O., Yokoyama, H., 2005, Occurrence of the myxosporean emaciation disease caused by Enteromyxum leei in cultured Japanese flounder Paralichthys olivaceus. Fish Pathol. 40, 175–180. CrossRefGoogle Scholar
Yokoyama, H., Urawa, S., 1997, Fluorescent labelling of actinospores for determining the portals of entry into fish. Dis. Aquat. Org. 30, 165–169. CrossRefGoogle Scholar