Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T05:05:54.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunohistopathological response against anisakid nematode larvae and a coccidian in Micromesistius poutassou from NE Atlantic waters

Published online by Cambridge University Press:  10 March 2021

B. Sayyaf Dezfuli Open the ORCID record for B. Sayyaf Dezfuli [Opens in a new window] ,
E. Simoni ,
G. Bosi ,
M. Palomba ,
S. Mattiucci ,
L. Giulietti ,
M. Bao ,
A. Levsen  and
P. Cipriani
B. Sayyaf Dezfuli*
Affiliation:
Department of Life Sciences & Biotechnology, University of Ferrara, St. Borsari 46, 44121Ferrara, Italy
E. Simoni
Affiliation:
Bioacoustics Research Laboratory, Department of Neurosciences, University of Padua, via G. Orus, 2b, 35129Padua, Italy
G. Bosi
Affiliation:
Department of Health, Animal Science and Food Safety, Università degli Studi di Milano, St. Trentacoste 2, 20134Milan, Italy
M. Palomba
Affiliation:
Department of Public Health and Infectious Diseases, ‘Sapienza-University of Rome’, P.le Aldo Moro, 5, 00185Rome, Italy Laboratory Affiliated to ‘Istituto Pasteur Italia-Fondazione Cenci Bolognetti’, Viale Regina Elena, 291, 00161Roma, Italy
S. Mattiucci
Affiliation:
Department of Public Health and Infectious Diseases, ‘Sapienza-University of Rome’, P.le Aldo Moro, 5, 00185Rome, Italy Laboratory Affiliated to ‘Istituto Pasteur Italia-Fondazione Cenci Bolognetti’, Viale Regina Elena, 291, 00161Roma, Italy
L. Giulietti
Affiliation:
Section of contaminants and biohazards, Institute of Marine Research (IMR), Nordnes, Bergen, Norway
M. Bao
Affiliation:
Section of contaminants and biohazards, Institute of Marine Research (IMR), Nordnes, Bergen, Norway
A. Levsen
Affiliation:
Section of contaminants and biohazards, Institute of Marine Research (IMR), Nordnes, Bergen, Norway
P. Cipriani
Affiliation:
Section of contaminants and biohazards, Institute of Marine Research (IMR), Nordnes, Bergen, Norway
*
Author for correspondence: B.S. Dezfuli, Fax: 0039-0532 455715. E-mail: dzb@unife.it
Get access Rights & Permissions [Opens in a new window]

Abstract

A survey on Anisakis simplex (sensu stricto (s.s.)) from blue whiting, Micromesistius poutassou, in the north-eastern Atlantic Ocean revealed the occurrence of high infection levels of third larval stages in visceral organs and flesh. Larvae were genetically identified with a multilocus approach as A. simplex (s.s.). Histochemical, immunohistochemical and ultrastructural observations were conducted on 30 M. poutassou specimens. Gonads, pyloric caeca and flesh harboured encapsulated larvae of A. simplex (s.s.) but no intense host reaction was encountered around the parasite in the above organs. In the liver, the most infected organ, the larvae co-occurred with the coccidian Goussia sp. Within the granuloma around the A. simplex (s.s.) larvae, two concentric layers were recognized, an inner mostly comprising electron-dense epithelioid cells and an outer layer made of less electron-dense epithelioid cells. Macrophages and macrophage aggregates (MAs) were abundant out of the granulomas, scattered in parenchyma, and inside the MAs, the presence of engulfed Goussia sp. was frequent. In liver tissue co-infected with Goussia sp. and A. simplex (s.s.), hepatocytes showed cytoplasmic rarefaction and acute cell swelling. Results suggest that the host-induced encapsulation of A. simplex (s.s.) larvae is a strategic compromise to minimize collateral tissue damage around the larval infection sites, to facilitate the survival of both parasite and host.

Keywords

Blue whitingAnisakis simplex (s.s.)Goussiagranulomaimmunohistochemistryultrastructure
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e14
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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

Agius, C and Roberts, RJ (2003) Melano-macrophage centers and their role in fish pathology. Journal of Fish Diseases 26, 499–509.CrossRefGoogle Scholar
Berland, B (1961) Nematodes from some Norwegian marine fishes. Sarsia 2, 1–50.CrossRefGoogle Scholar
Berland, B (2006) Musings on nematode parasites. Fisken Go Havent 11, 1–30.Google Scholar
Bernard, VD and Peanasky, RJ (1993) The serine protease inhibitor family from Ascaris suum: Chemical determination of the five disulphide bridges. Archives of Biochemistry Biophysics 303, 367–376.CrossRefGoogle Scholar
Bruschi, F and Chiumiento, L (2011) Trichinella inflammatory myopathy: Host or parasite strategy? Veterinary Parasitology 23, 42.Google Scholar
Buchmann, K (2012) Fish immune responses against endoparasitic nematodes – experimental models. Journal of Fish Diseases 35, 623–635.CrossRefGoogle ScholarPubMed
Buchmann, K and Mehrdana, F (2016) Effects of anisakid nematodes Anisakis simplex (s.l.), Pseudoterranova decipiens (s.l.) and Contracaecum osculatum (s.l.) on fish and consumer health. Food and Waterborne Parasitology 4, 13–22.CrossRefGoogle Scholar
Chung, JY, Choi, J, Sears, JD, et al. (2016) A melanin-bleaching methodology for molecular and histopathological analysis of formalin-fixed paraffin-embedded tissue. Laboratory Investigation 96, 1116–1127.CrossRefGoogle ScholarPubMed
Cipriani, P, Acerra, V, Bellisario, B, Sbaraglia, GL, Cheleschi, R, Nascetti, G and Mattiucci, S (2016) Larval migration of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in European anchovy, Engraulis encrasicolus: Implications to seafood safety. Food Control 59, 148–157.CrossRefGoogle Scholar
da Silva, WF, Simões, MJ, Gutierre, RC, Egami, MI, Santos, AA, Antoniazzi, MM and Ranzani-Paiva, MJT (2017) Special dyeing, histochemistry, immunohistochemistry and ultrastructure: A study of mast cells/eosinophilic granules cells (MCs/EGC) from Centropomus parallelus intestine. Fish & Shellfish Immunology 60, 502–508.CrossRefGoogle ScholarPubMed
Debenedetti, ÁL, Madrid, E, Trelis, M, Codes, FJ, Gil-Gómez, F, Sáez-Durán, S and Fuentes, MV (2019) Prevalence and risk of anisakid Larvae in fresh fish frequently consumed in Spain: An overview. Fishes 4, 1–16.CrossRefGoogle Scholar
de Buron, I and Roumillat, WA (2010) Histopathology of two philometrid parasites of the southern flounder, Paralichthys lethostigma. Journal of Wildlife Diseases 46, 277–282.CrossRefGoogle ScholarPubMed
Dezfuli, BS, Manera, M, Lorenzoni, M, Pironi, F, Shinn, AP and Giari, L (2015) Histopathology and the inflammatory response of European perch, Perca fluviatilis muscle infected with Eustrongylides sp. (Nematoda). Parasites & Vectors 8, 227–220.CrossRefGoogle Scholar
Dezfuli, BS, Fernandes, CE, Galindo, GM, Castaldelli, G, Manera, M, DePasquale, JA and Giari, L (2016) Nematode infection in liver of the fish Gymnotus inaequilabiatus (gymnotiformes: Gymnotidae) from the pantanal region in Brazil: Pathobiology and inflammatory response. Parasites & Vectors 9, 473.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, 1765–1774.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
Dobson, JT, Seibert, J, The, EM, Da'as, S, Fraser, RB, Paw, BH and Berman, JN (2008) Carboxypeptidasea5 identifies a novel mast cell lineage in the zebrafish providing new insight into mast cell fate determination. Blood 112, 2969–2972.CrossRefGoogle ScholarPubMed
Duchesne, E, Tremblay, MH and Côté, CH (2011) Mast cell tryptase stimulates myoblast proliferation; a mechanism relying on protease activated receptor-2 and cyclooxygenase-2. BMC Musculoskeletal Disorders 12, 235.CrossRefGoogle ScholarPubMed
Esteban, MÁ, Cuesta, A, Chaves-Pozo, E and Meseguer, J (2015) Phagocytosis in teleosts. Implications of the new cells involved. Biology 4, 907–922.CrossRefGoogle ScholarPubMed
Estensoro, I, Mulero, I, Redondo, M, Alvarez-Pellitero, P, Mulero, V and Sitjà-Bobdella, 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 (2020, April 22) Fishery Statistical Collections - Global Capture Production [Document]. URL Retrieved from http://www.fao.org/fishery/statistics/global-capture-production/enGoogle Scholar
Ferguson, HW (2006) Systemic pathology of fish: A text and atlas of normal tissues in teleosts and their responses in disease. 2nd edn. London, UK, Scotian Press.Google Scholar
Fernández, M, Aznar, FJ, Montero, FE and Raga, JA (2005) Endoparasites of the blue whiting, Mcromesistius poutassou from north-west Spain. Journal of Helminthology 79, 15–21.CrossRefGoogle ScholarPubMed
Franke, F, Rahn, AK, Dittmar, J, Erin, N, Rieger, JK, Haase, D and Scharsack, JP (2014) In vitro leukocyte response of three-spined sticklebacks (Gasterosteus aculeatus) to helminth parasite antigens. Fish & Shellfish Immunology 36, 130–140.CrossRefGoogle ScholarPubMed
Furtado, WE, Cardoso, L, Figueredo, AB, Marchiori, NC and Martins, ML (2019) Histological and hematological alterations of silver catfish Rhamdia quelen highly parasitized by Lernaea cyprinacea. Diseases of Aquatic Organisms 135, 157–168.CrossRefGoogle ScholarPubMed
Gao, M, Xie, B, Gu, C, Li, H, Zhang, F and Yu, Y (2014) Targeting the proinflammatory cytokine tumor necrosis factor-α to alleviate cardiopulmonary bypass-induced lung injury (review). Molecular Medicine Reports 11, 2373–2378.CrossRefGoogle Scholar
Gauthier, DT, Vogelbein, WK and Ottinger, CA (2004) Ultrastructure of Mycobacterium marinum granuloma in striped bass Morone saxatilis. Diseases of Aquatic Organisms 62, 121–132.CrossRefGoogle ScholarPubMed
Grayfer, L, Hodgkinson, JW and Belosevic, M (2014) Antimicrobial responses of teleost phagocytes and innate immune evasion strategies of intracellular bacteria. Developmental & Comparative Immunology 43, 223–242.CrossRefGoogle ScholarPubMed
Hauck, AK (1977) Occurrence and survival of the larval nematode Anisakis sp. In the flesh of fresh, frozen, brined, and smoked pacific herring, Clupea harengus pallasi. Journal of Parasitology 63, 515–519.CrossRefGoogle ScholarPubMed
Hehlgans, T and Pfeffer, K (2005) The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: Players, rules and the games. Immunology 115, 1–20.CrossRefGoogle ScholarPubMed
Hong, S, Li, R, Xu, Q, Secombes, CJ and Wang, T (2013) Two types of TNF-α exist in teleost fish: Phylogeny, expression, and bioactivity analysis of type-II TNF-α3 in rainbow trout Oncorhynchus mykiss. Journal of Immunology 191, 5959–5972.CrossRefGoogle ScholarPubMed
Horbowy, J, Podolska, M and Nadolna-Altyn, K (2016) Increasing occurrence of anisakid nematodes in the liver of cod (Gadus morhus) from the Baltic Sea: Does infection affect the condition and mortality of fish. Fisheries Research 179, 98–103.CrossRefGoogle Scholar
Jia, J, Qin, J, Yuan, X, Liao, Z, Huang, J, Wang, B, Sun, C and Li, W (2019) Microarray and metabolome analysis of hepatic response to fasting and subsequent refeeding in zebrafish (Danio rerio). BMC Genomics 20, 919.CrossRefGoogle Scholar
Jørgensen, LG, Korbut, R, Jeberg, F, Kania, PW and Buchmann, K (2018) Association between adaptive immunity and neutrophil dynamics in zebrafish (Danio rerio) infected by a parasitic ciliate. PLoS One 11, 1–18.Google Scholar
Karasev, AB (1990) Ecological and geographical analysis of the northeast Atlantic blue whiting parasitic fauna. pp. 307–318 in Monstad, T (Ed) Biology and fisheries of Norwegian spring spawning herring and blue whiting in the northeast Atlantic. Bergen, Institute of Marine Research.Google Scholar
Larsen, AH, Bresciani, J and Buchmann, K (2002) Interactions between ecto- and endoparasites in trout Salmo trutta. Veterinary Parasitology 103, 167–173.CrossRefGoogle ScholarPubMed
Latoszek, E, Kamaszewski, M, Milczarek, K, Puppel, K, Szudrowicz, H, Adamski, A and Ostaszewska, T (2019) Histochemical characteristics of macrophages of butterfly splitfin Ameca splendens. Folia Biologica (Kraków) 67, 53–60.CrossRefGoogle Scholar
Levsen, A, Svanevik, CS, Cipriani, P, Mattiucci, S, Gay, M, Hastie, LC and Pierce, GJ (2018) A survey of zoonotic nematodes of commercial key fish species from major European fishing ground-introducing the FP7 PARASITE exposure assessment study. Fisheries Research 202, 4–21.CrossRefGoogle Scholar
Mackenzie, K and Hemmingsen, W (2014) Parasites as biological tags in marine fisheries research: European Atlantic waters. Parasitology 142, 1–14.Google ScholarPubMed
Mattiucci, S, Cipriani, P, Webb, SC, Paoletti, M, Marcer, F, Bellisario, B and Nascetti, G (2014) Genetic and morphological approaches distinguish the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). Journal of Parasitology 100, 199–214.CrossRefGoogle Scholar
Mattiucci, S, Acerra, V, Paoletti, M, Cipriani, P, Levsen, A, Webb, SC and Nascetti, G (2016) No more time to stay “single” in the detection of Anisakis pegreffii, A. simplex (s. s.) and hybridization events between them: A multi-marker nuclear genotyping approach. Parasitology 143, 998–1011.CrossRefGoogle Scholar
Mattiucci, S, Cipriani, P, Levsen, A, Paoletti, M and Nascetti, G (2018) Molecular epidemiology of anisakis and anisakiasis: An ecological and evolutionary road Map. Advances in Parasitology 99, 93–263.CrossRefGoogle ScholarPubMed
McNeil, HP, Adachi, R and Stevens, RL (2007) Mast cell-restricted tryptases: Structure and function in inflammation and pathogen defense. Journal of Biological Chemistry 282, 20785–20789.CrossRefGoogle ScholarPubMed
Mladineo, I, Popovic, M, Drmic-Hofman, I and Poljak, V (2016) A case report of Anisakis pegreffii (Nematoda, anisakidae) identified from archival paraffin sections of a Croatian patient. BMC Infectious Diseases 16, 42.CrossRefGoogle ScholarPubMed
Palomba, M, Cipriani, P, Giulietti, L, Levsen, A, Nascetti, G and Mattiucci, M (2020) Differences in gene expression profiles of seven proteins in third-stage larvae of Anisakis simplex (sensu stricto) by sites of infection in blue whiting (Micromesistius poutassou). Genes 11, 559.CrossRefGoogle Scholar
Reite, OB and Evensen, Ø (2006) Inflammatory cells of teleostean fish: A review focusing on mast cells/eosinophilic granule cells and rodlet cells. Fish Shellfish Immunology 20, 192–208.CrossRefGoogle ScholarPubMed
Rieger, AM, Konowalchuk, JD, Grayfer, L, Katzenback, BA, Havixbeck, JJ, Kiemele, MD and Barreda, DR (2012) Fish and mammalian phagocytes differentially regulate pro-inflammatory and homeostatic responses in vivo. PLoS One 7, e47070.CrossRefGoogle ScholarPubMed
Ronza, P, Losada, AP, Villamarín, A, Bermúdez, R and Quiroga, MI (2015) Immunolocalization of tumor necrosis factor alpha in turbot (Scophthalmus maximus, L.) tissues. Fish & Shellfish Immunology 45, 470–476.CrossRefGoogle ScholarPubMed
Secombes, CJ (1996) The nonspecific immune system: Cellular defenses. pp. 63–103 in Iwama, G, Nakanishi, T (Eds) The fish immune system. London, Academic Press.Google Scholar
Secombes, CJ and Ellis, AE (2012) The immunology of teleosts. pp. 144–664 in Roberts, RJ (Ed) Fish pathology. Chichester, Blackwell Publishing.CrossRefGoogle Scholar
Seno, H, Sawada, M, Fukuzawa, H, Morita-Fujisawa, Y, Takaishi, S, Hiai, H and Chiba, T (2002) Involvement of tumor necrosis factor alpha in intestinal epithelial cell proliferation following paneth cell destruction. Scandinavian Journal of Gastroenterology 37, 154–160.CrossRefGoogle ScholarPubMed
Sitjà-Bobadilla, A, Estensoro, I and Pérez-Sánchez, J (2016) Immunity to gastrointestinal microparasites of fish. Developmental and Comparative Immunology 64, 187–201.CrossRefGoogle ScholarPubMed
Stosik, MP, Tokarz-Deptuła, B and Deptuła, W (2019) Melanomacrophages and melanomacrophage centres in osteichthyes. Central European Journal of Immunology 44, 201–205.CrossRefGoogle ScholarPubMed
Umberger, CM, de Buron, I, Roumillat, WA and Mcelroy, E (2013) Effects of a muscle-infecting parasitic nematode on the locomotor performance of their fish host. Journal of Fish Biology 82, 1250–1258.CrossRefGoogle ScholarPubMed
Ventura, AS, Ishikawa, MM, de Araujo Gabriel, AM, Silbiger, HLN, Cavichiolo, F and Takemoto, RM (2016) Histopathology from liver of tuvira (Gymnotus spp.) parasitized by larvae of nematodes. Ciência Rural 46, 1233–1239.CrossRefGoogle Scholar
Williams, JM, Duckworth, CA, Burkitt, MD, Watson, AJM, Campbell, BJ and Pritchard, DM (2015) Epithelial cell shedding and barrier function: A matter of life and death at the small intestinal villus tip. Veterinary Pathology 52, 445–455.CrossRefGoogle ScholarPubMed