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The impact of Anguillicoloides crassus (Nematoda) on European eel swimbladder: histopathology and relationship between neuroendocrine and immune cells

Published online by Cambridge University Press:  13 January 2021

Bahram Sayyaf Dezfuli*
Affiliation:
Department of Life Sciences and Biotechnology, University of Ferrara, St. Borsari 46, 44121Ferrara, Italy
Chiara Maestri
Affiliation:
Department of Life Sciences and Biotechnology, University of Ferrara, St. Borsari 46, 44121Ferrara, Italy
Massimo Lorenzoni
Affiliation:
Department of Cellular and Environmental Biology, University of Perugia, St. Elce di sotto 5, 06123Perugia, Italy
Antonella Carosi
Affiliation:
Department of Cellular and Environmental Biology, University of Perugia, St. Elce di sotto 5, 06123Perugia, Italy
Barbara J Maynard
Affiliation:
The Institute for Learning and Teaching, Colorado State University, Fort Collins, CO80523, USA
Giampaolo Bosi
Affiliation:
Department of Health, Animal Science and Food Safety, Università degli Studi di Milano, St. Trentacoste 2, 20134Milan, Italy
*
Author for correspondence: Bahram Sayyaf Dezfuli, E-mail: [email protected]

Abstract

The swimbladder functions as a hydrostatic organ in most bony fishes, including the European eel, Anguilla anguilla. Infection by the nematode Anguillicoloides crassus impairs swimbladder function, significantly compromising the success of the eel spawning migration. Swimbladders from 32 yellow eels taken from Lake Trasimeno (Central Italy) were analysed by histopathology- and electron microscopy-based techniques. Sixteen eels (50%) harboured A. crassus in their swimbladders and intensity of infection ranged from 2 to 17 adult nematodes per organ (6.9 ± 1.6, mean ± s.e.). Gross observations of heavily infected swimbladders showed opacity and histological analysis found a papillose aspect to the mucosa and hyperplasia of the lamina propria, muscularis mucosae and submucosa. Inflammation, haemorrhages, dilation of blood vessels and epithelial erosion were common in infected swimbladders. In the epithelium of parasitized swimbladders, many empty spaces and lack of apical junctional complexes were frequent among the gas gland cells. In heavily infected swimbladders, we observed hyperplasia, cellular swelling and abundant vacuolization in the apical portion of the gas gland cells. Numerous mast cells and several macrophage aggregates were noticed in the mucosal layer of infected swimbladders. We found more nervous and endocrine elements immunoreactive to a panel of six rabbit polyclonal antibodies in infected swimbladders compared to uninfected.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Bain, CC and Mowat, AM (2014) Macrophages in intestinal homeostasis and inflammation. Immunological Reviews 260, 102117.CrossRefGoogle ScholarPubMed
Barry, J, McLeish, J, Dodd, JA, Turnbull, JF, Boylan, P and Adams, CE (2014) Introduced parasite Anguillicola crassus infection significantly impedes swim bladder function in the European eel Anguilla anguilla (L.). Journal of Fish Diseases 37, 921924.CrossRefGoogle Scholar
Beregi, A, Molnár, K, Békési, L and Székely, C (1998) Radiodiagnostic method for studying swimbladder inflammation caused by Anguillicoloides crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 34, 155160.CrossRefGoogle Scholar
Bosi, G, Domeneghini, C, Arrighi, S, Giari, L, Simoni, E and Dezfuli, BS (2005a) Response of the gut neuroendocrine system of Leuciscus cephalus (L.) to the presence of Pomphorhynchus laevis Muller, 1776 (Acanthocephala). Histology & Histopathology 20, 509518.Google Scholar
Bosi, G, Shinn, AP, Giari, L, Simoni, E, Pironi, F and Dezfuli, BS (2005b) Changes in the neuromodulators of the diffuse endocrine system of the alimentary canal of farmed rainbow trout, Oncorhynchus mykiss (Walbaum), naturally infected with Eubothrium crassum (Cestoda). Journal of Fish Diseases 28, 703711.CrossRefGoogle Scholar
Bosi, G, DePasquale, JA, Manera, M, Castaldelli, G, Giari, L and Dezfuli, BS (2018) Histochemical and immunohistochemical characterization of rodlet cells in the intestine of two teleosts, Anguilla anguilla and Cyprinus carpio. Journal of Fish Diseases 41, 475485.CrossRefGoogle ScholarPubMed
Buchmann, K (2012) Fish immune responses against endoparasitic nematodes – experimental models. Journal of Fish Diseases 35, 623635.CrossRefGoogle ScholarPubMed
Ceccotti, C, Giaroni, C, Bistoletti, M, Viola, M, Crema, F and Terova, G (2018) Neurochemical characterization of myenteric neurons in the juvenile gilthead sea bream (Sparus aurata) intestine. PLoS ONE 13, e0201760. doi:10.1371/journal.pone.0201760.CrossRefGoogle ScholarPubMed
Da Silva, WF, Simões, MJ and Gutierre, RC (2017) Special dyeing, histochemistry, immunohistochemistry and ultrastructure: a study of mast cells/eosinophilic granules cells (MCs/EGC) from Centropomus parallelus intestine. Fish and Shellfish Immunology 60, 502508.CrossRefGoogle ScholarPubMed
De Charleroy, D, Grisez, L, Thomas, K, Belpaire, C and Ollevier, F (1990) The life cycle of Anguillicoloides crassus. Disease of Aquatic Organisms 8, 7784.CrossRefGoogle Scholar
Dekker, W (2003) Status of the European eel stock and fisheries. In Aida, K, Tsukamoto, K and Yamaudi, K (eds), Eel Biology. Tokyo: Springer-Verlag, pp. 237254.CrossRefGoogle Scholar
Dezfuli, BS, Arrighi, S, Domeneghini, C and Bosi, G (2000) Immunohistochemical detection of neuromodulators in the intestine of Salmo trutta L. naturally infected with Cyathocephalus truncatus Pallas (Cestoda). Journal of Fish Diseases 23, 265273.CrossRefGoogle Scholar
Dezfuli, BS, Pironi, F, Giari, L, Domeneghini, C and Bosi, G (2002) Effect of Pomphorhynchus laevis (Acanthocephala) on putative neuromodulators in the intestine of naturally infected Salmo trutta. Journal of Fish Diseases 51, 2735.Google ScholarPubMed
Dezfuli, BS, Bo, T, Lorenzoni, M, Shinn, AP and Giari, L (2015) Fine structure and cellular responses at the host-parasite interface in a range of fish-helminth systems. Veterinary Parasitology 208, 272279.CrossRefGoogle Scholar
Dezfuli, BS, Manera, M, DePasquale, JA, Pironi, F and Giari, L (2017) Liver of the fish Gymnotus inaequilabiatus and nematode larvae infection: histochemical features and expression of proliferative cell nuclear antigen. Journal of Fish Diseases 40, 17651774.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Giari, L, Lorenzoni, M, Carosi, A, Manera, M and Bosi, G (2018) Pike intestinal reaction to Acanthocephalus lucii (Acanthocephala): immunohistochemical and ultrastructural surveys. Parasites & Vectors 11, 424.CrossRefGoogle Scholar
Dezfuli, BS, Castaldelli, G, Tomaini, R, Manera, M, DePasquale, JA and Bosi, G (2020) Challenge for macrophages and mast cells of Chelon ramada to counter an intestinal microparasite, Myxobolus mugchelo (Myxozoa). Diseases of Aquatic Organisms 138, 171183.CrossRefGoogle Scholar
Dumbarton, TC, Stoyek, M, Croll, RP and Smith, FM (2010) Adrenergic control of swimbladder deflation in the zebrafish (Danio rerio). The Journal of Experimental Biology 213, 25362546.CrossRefGoogle Scholar
Estensoro, I, Mulero, I, Redondo, MJ, Álvarez-Pellitero, P, Mulero, V and Sitjà-Bobadilla, A (2014) Modulation of leukocytic populations of gilthead sea bream (Sparus aurata) by the intestinal parasite Enteromyxum leei (Myxozoa: Myxosporea). Parasitology 141, 425440.CrossRefGoogle Scholar
Fänge, R (1953) The mechanisms of gas transport in the euphysoclist swimbladder. Acta Physiologica 30, 1133.Google ScholarPubMed
Finney, JL, Robertson, GN, McGee, CAS, Smith, FM and Croll, RP (2006) Structure and autonomic innervation of the swim swimbladder in the zebrafish (Danio rerio). The Journal of Comparative Neurology 495, 587606.CrossRefGoogle Scholar
Frisch, K, Davie, A, Schwarz, T and Turnbull, JF (2016) Comparative imaging of European eels (Anguilla anguilla) for the evaluation of swimbladder nematode (Anguillicoloides crassus) infestation. Journal of Fish Diseases 39, 635647.CrossRefGoogle ScholarPubMed
Galindo-Villegas, J, Garcia-Garcia, E and Mulero, V (2016) Role of histamine in the regulation of intestinal immunity in fish. Developmental & Comparative Immunology 64, 178186.CrossRefGoogle ScholarPubMed
Gomez Gonzalez, NE, Cabas, I, Montero, J, Garcia Alcazar, A, Mulero, V and Garcia Ayala, A (2017) Histamine and mast cell activator compound 48/80 are safe but inefficient systemic adjuvants for gilthead seabream vaccination. Developmental & Comparative Immunology 72, 18.CrossRefGoogle ScholarPubMed
Gonzáles-Stegmaier, R, Villarroel-Espíndola, F, Manríquez, R, López, M, Monrás, M, Figueroa, J, Enríquez, R and Romero, A (2017) New immunomodulatory role of neuropeptide Y (NPY) in Salmo salar leucocytes. Developmental & Comparative Immunology 76, 303309.CrossRefGoogle Scholar
Grayfer, L, Kerimoglu, B, Yaparla, A, Hodgkinson, JW, Xie, J and Belosevic, M (2018) Mechanisms of fish macrophage antimicrobial immunity. Frontiers in Immunology 9, 1105.CrossRefGoogle ScholarPubMed
Haenen, OLM, Grisez, L, De Charleroy, D, Belpaire, C and Ollevier, F (1989) Experimentally induced infections of European eel Anguilla anguilla with Anguillicoloides crassus (Nematoda, Dracunculoidea) and subsequent migration of larvae. Diseases of Aquatic Organisms 7, 97101.CrossRefGoogle Scholar
Haenen, OLM, Van Banning, P and Dekker, W (1994) Infection of eel Anguilla anguilla (L.) and smelt Osmerus eperlanus (L.) with Anguillicoloides crassus (Nematoda, Dracunculoidea) in the Netherlands from 1986 to 1992. Aquaculture 126, 219229.CrossRefGoogle Scholar
ICES (2010) International Council for the Exploration of the Sea. Report of the 2010 session of the Joint EIFA C/ICES Working Group on Eels. Hamburg, Germany. Available at http://www.fao.org/3/a-bq586e.pdf.Google Scholar
Johnson, JC, Schwiesow, T, Ekwall, AK and Christiansen, JL (1999) Reptilian melanomacrophages function under conditions of hypothermia: observations on phagocytic behavior. Pigment Cell & Melanoma Research 12, 376382.CrossRefGoogle ScholarPubMed
Kelly, CE, Kennedy, CR and Brown, JA (2000) Physiological status of wild European eels (Anguilla anguilla) infected with the parasitic nematode, Anguillicola crassus. Parasitology 120, 195202.CrossRefGoogle ScholarPubMed
Kirk, RS (2003) The impact of Anguillicoloides crassus on European eels. Fisheries Management and Ecology 10, 385394.CrossRefGoogle Scholar
Knopf, K (2006) The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eel Anguilla japonica: differences in susceptibility and immunity between a recently colonized host and the original host. Journal of Helminthology 80, 129136.CrossRefGoogle ScholarPubMed
Knopf, K, Naser, K, Van der Heijden, MHT and Taraschewski, H (2000) Humoral immune response of European eel Anguilla anguilla experimentally infected with Anguillicola crassus. Diseases of Aquatic Organisms 42, 6169.CrossRefGoogle ScholarPubMed
Køie, M (1991) Swimbladder nematodes (Anguillicoloides Spp.) and gill monogeneans (Pseudodactylogyrus Spp.) parasitic on the European eel (Anguilla anguilla). ICES Journal of Marine Science 47, 391398.CrossRefGoogle Scholar
Koshio, S (2016) Immunotherapies targeting fish mucosal immunity–current knowledge and future perspectives. Frontiers in Immunology 6, 643.CrossRefGoogle ScholarPubMed
Kuwahara, A, Niimi, A and Itagaki, H (1974) Studies on a nematode parasitic in the air bladder of the eel. I. Description of Anguillicola crassa n. sp. (Philometridea, Anguillicolidae). Japanese Journal of Parasitology 23, 275279.Google Scholar
Lefebvre, F, Fazio, G, Palstra, AP, Székely, C and Crivelli, AJ (2011) An evaluation of indices of gross pathology associated with the nematode Anguillicoloides crassus in eels. Journal of Fish Diseases 34, 3145.CrossRefGoogle ScholarPubMed
Lefebvre, F, Wielgoss, S, Nagasawa, K and Moravec, F (2012) On the origin of Anguillicoloides crassus, the invasive nematode of anguillid eels. Aquatic Invasions 7, 443453.CrossRefGoogle Scholar
Lundin, K (1991) Effects of vasoactive intestinal polypeptide, substance P, 5-hydroxytryptamine, met-enkephalin and neurotensin on the swimbladder smooth muscle of two teleost species, Gadus morhua and Anguilla anguilla. Fish Physiology and Biochemistry 9, 7782.CrossRefGoogle Scholar
Lundin, K (1999) Morphology and phylogeny of the Nemertodermatida (Platyhelminthes, Acoelomorpha). PhD Dissertation, Göteborg, Suisse.Google Scholar
Lundin, K and Holmgren, S (1984) Vasoactive intestinal polypeptide-like immunoreactivity and effects of VIP in the swimbladder of the cod, Gadus morhua. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 154, 627633.CrossRefGoogle Scholar
Lundin, K and Holmgren, S (1989) The occurrence and distribution of peptide- or 5-HT-containing nerves in the swimbladder of four different species of teleosts (Gadus morhua, Ctenolabrus rupestris, Anguilla anguilla, Salmo gairdneri). Cell and Tissue Research 257, 641647.CrossRefGoogle Scholar
Maina, JN (2000) Functional morphology of the gas-gland cells of the air-bladder of Oreochromis alcalicus graham (Teleostei: Cichlidae): an ultrastructural study on a fish adapted to a severe, highly alkaline environment. Tissue and Cell 32, 117132.CrossRefGoogle Scholar
Maizels, RM, Smits, HH and McSorley, HJ (2018) Modulation of host immunity by helminths: the expanding repertoire of parasite effector molecules. Immunity 49, 801818.CrossRefGoogle ScholarPubMed
Molnár, K (1994) Formation of parasitic nodules in the swimbladder and intestinal walls of the eel Anguilla anguilla due to infections with larval stages of Anguillicoloides crassus. Diseases of Aquatic Organisms 20, 163170.CrossRefGoogle Scholar
Molnár, K and Székely, C (1995) Parasitological survey of some important fish species of Lake Balaton. Parasitologia Hungarica 28, 6382.Google Scholar
Molnár, K, Baska, F, Csaba, G, Glávits, R and Székely, C (1993) Pathological and histopathological studies of the swimbladder of eels Anguilla anguilla infected by Anguillicoloides crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 15, 4150.CrossRefGoogle Scholar
Mosberian-Tanha, P, Landsverk, T, Press, CM, Mydland, LT, Schrama, JW and Overland, M (2018) Granulomatous enteritis in rainbow trout (Oncorhynchus mykiss) associated with soya bean meal regardless of water dissolved oxygen level. Journal of Fish Diseases 41, 269280.CrossRefGoogle ScholarPubMed
Mulero, I, Noga, EJ, Meseguer, J, Garcia-Ayala, A and Mulero, V (2008) The antimicrobial peptides piscidins are stored in the granules of professional phagocytic granulocytes of fish and are delivered to the bacteria-containing phagosome upon phagocytosis. Developmental & Comparative Immunology 32, 15311538.CrossRefGoogle ScholarPubMed
Munoz, P, Peñalver, J, Ruiz de Ybañez, R and Garcia, J (2015) Influence of adult Anguillicoloides crassus load in European eels swimbladder on macrophage response. Fish and Shellfish Immunology 42, 221224.CrossRefGoogle ScholarPubMed
Nilsson, S (2009) Nervous control of fish swimbladders. Acta Histochemica 111, 176184.CrossRefGoogle ScholarPubMed
Nimeth, K, Zwerger, P, Würtz, J, Salvenmoser, W and Pelster, B (2000) Infection of the glass eel swimbladder with the nematode Anguillicola crassus. Parasitology 121, 7583.CrossRefGoogle ScholarPubMed
Palstra, AP, Heppener, DFM, Van Ginneken, VJT, Székely, C and Van den Thillart, GEEJM (2007) Swimming performance of silver eels is severely impaired by the swimbladder parasite Anguillicoloides crassus. Journal of Experimental Marine Biology and Ecology 352, 244256.CrossRefGoogle Scholar
Pelster, B (1995) Metabolism of the swimbladder tissue. In Hochachka, PW and Mommsen, TP (eds), Biochemistry and Molecular Biology of Fishes 4. Amsterdam: Elsevier, pp. 101118. doi: 10.1016/S1873-0140(06)80008-1.Google Scholar
Pelster, B (2015) Swimbladder function and the spawning migration of the European eel Anguilla anguilla. Frontiers in Physiology 5, 486.CrossRefGoogle ScholarPubMed
Pereira, RT, Rodrigues de Freitas, T, Cardoso de Oliveira, IR, Santos Costa, L, Andrés Vigliano, F and Vieira Rosa, P (2017) Endocrine cells producing peptide hormones in the intestine of Nile tilapia: distribution and effects of feeding and fasting on the cell density. Fish Physiology and Biochemistry 43, 13991412.CrossRefGoogle ScholarPubMed
Pratt, TC, O'Connor, LM, Stacey, JA, Stanley, DR, Mathers, A, Johnson, LE, Reid, SM, Verreault, G and Pearce, J (2019) Pattern of Anguillicoloides crassus infestation in the St. Lawrence river watershed. Journal of Great Lakes Research 44, 991997.CrossRefGoogle Scholar
Robertson, GN, McGee, CAS, Dumbarton, TC, Croll, RP and Smith, FM (2007) Development of the swimbladder and its innervation in the zebrafish, Danio rerio. Journal of Morphology 268, 967985.CrossRefGoogle ScholarPubMed
Salger, SA, Reading, BJ and Noga, EJ (2017) Tissue localization of piscidin host-defense peptides during striped bass (Morone saxatilis) development. Fish Shellfish Immunology 61, 173180.CrossRefGoogle ScholarPubMed
Salinas, I and Magadán, S (2017) Omics in fish mucosal immunity. Developmental & Comparative Immunology 75, 99108.CrossRefGoogle ScholarPubMed
Schwerte, T, Holmgren, S and Pelster, B (1999) Vasodilation of swimbladder vessels in the European eel (Anguilla anguilla) induced by vasoactive intestinal polypeptide, nitric oxide, adenosine and protons. The Journal of Experimental Biology 202, 10051013.CrossRefGoogle ScholarPubMed
Secombes, CJ and Ellis, AE (2012) The immunology of teleosts. In Roberts, RJ (ed.), Fish Pathology 4. Chicester: Blackwell Publishing, pp. 144166.CrossRefGoogle Scholar
Shahbazi, F, Holmgren, S and Jensen, J (2009) Cod CGRP and tachykinins in coeliac artery innervation of the Atlantic cod, Gadus morhua: presence and vasoactivity. Fish Physiology and Biochemistry 35, 369376.CrossRefGoogle ScholarPubMed
Shi, C and Pamer, EG (2011) Monocyte recruitment during infection and inflammation. Nature Reviews Immunology 11, 762774.CrossRefGoogle ScholarPubMed
Sjöberg, NB, Petersson, E, Wickström, H and Hansson, S (2009) Effects of the swimbladder parasite, Anguillicola crassus on the migration of European silver eels Anguilla anguilla in the Baltic Sea. Journal of Fish Biology 74, 21582170.CrossRefGoogle ScholarPubMed
Sprengel, G and Luchtenberg, H (1991) Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla. Diseases of Aquatic Organisms 11, 3135.CrossRefGoogle Scholar
Steinel, NC and Bolnick, DI (2017) Melanomacrophage centers as a histological indicator of immune function in fish and other poikilotherms. Frontiers in Immunology 8, 827.CrossRefGoogle ScholarPubMed
Sures, B, Knopf, K and Kloas, W (2001) Induction of stress by the swimbladder nematode Anguillicola crassus in European eels, Anguilla anguilla, after repeated experimental infection. Parasitology 123, 179184.CrossRefGoogle ScholarPubMed
Székely, C, Molnár, K, Muller, T, Szabò, A, Romvávri, R, Hancz C, and Bercsényi, M (2004) Comparative study of X-ray computerised tomography and conventional X-ray methods in diagnosis of swimbladder infection in eels caused by Anguillicoloides crassus. Diseases of Aquatic Organisms 58, 157164.CrossRefGoogle Scholar
Székely, C, Molnar, K and Rácz, OZ (2005) Radiodiagnostic method for studying the dynamics of Anguillicoloides crassus (Nematoda: Dracunculoidea) infection and pathological status of the swimbladder in Lake Balaton eels. Diseases of Aquatic Organisms 64, 157164.CrossRefGoogle Scholar
Tafalla, C, Leal, E, Yamaguchi, T and Fischer, UT (2016) T cell immunity in the teleost digestive tract. Developmental & Comparative Immunology 64, 167177.CrossRefGoogle ScholarPubMed
Terech-Majewska, E, Schulz, P and Siwichi, AK (2015) Influence of nematode Anguillicoloides crassus infestation on the cellular and humoral innate immunity in European eel (Anguilla anguilla L.). Central European Journal of Immunology 40, 127131.CrossRefGoogle Scholar
Van Banning, P and Haenen, OLM (1990) Effect of the swimbladder nematode Anguillicoloides crassus in wild and farmed eel, Anguilla anguilla. In Perkins, FO and Cheng, TC (eds), Pathology in Marine Science. New York: Academic Press, pp. 317330.Google Scholar
Van Ginneken, VJT and Maes, GE (2005) The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Reviews in Fish Biology and Fisheries 15, 367398.CrossRefGoogle Scholar
Vogel, G (2010) Europe tries to save its eels. Science (New York, N.Y.) 329, 505507.CrossRefGoogle ScholarPubMed
Wang, SJ, Sharkey, KA and McKay, DM (2018) Modulation of the immune response by helminths: a role for serotonin? Bioscience Reports 38, BSR20180027. doi:10.1042/BSR20180027.CrossRefGoogle ScholarPubMed
Wang, J, Lei, P, Gamil, AAA, Lagos, L, Yue, Y, Schirmer, K, Mydland, LT, Øverland, M, Krogdahl, Å and Kortner, TM (2019) Rainbow trout (Oncorhynchus mykiss) intestinal epithelial cells as a model for studying gut immune function and effects of functional feed ingredients. Frontiers in Immunology 10, 152.CrossRefGoogle ScholarPubMed
Würtz, J and Taraschewski, H (2000) Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Diseases of Aquatic Organisms 39, 121134.CrossRefGoogle ScholarPubMed
Würtz, J, Taraschewski, H and Pelster, B (1996) Changes in gas composition in the swimbladder of the European eel (Anguilla anguilla) infected with Anguillicoloides crassus (Nematoda). Parasitology 112, 233238.CrossRefGoogle Scholar