Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-31T14:36:12.791Z Has data issue: false hasContentIssue false
  • English
  • Français

Transmission of the microsporidian gill parasite, Loma salmonae

Published online by Cambridge University Press:  13 August 2007

Joy A. Becker  and
David J. Speare
Joy A. Becker
Affiliation:
Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE, C1A 4P3, Canada School of Aquaculture University of Tasmania, Launceston, Tasmania7250, Australia
David J. Speare*
Affiliation:
Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE, C1A 4P3, Canada
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Since it was first reported in 1987 at a hatchery in British Columbia, Loma salmonae has become increasingly important as an emerging parasite affecting the Canadian salmonid aquaculture industry. L. salmonae causes Microsporidial Gill Disease of Salmon (MGDS) in farmed Pacific salmonids, Oncorhynchus spp., resulting in respiratory distress, secondary infections and high mortality rates. In the last decade, laboratory studies have identified key transmission factors for this disease and described the pathogenesis of MGDS. L. salmonae enters the host via the gut, where it injects sporoplasm into a host cell, which then migrates to the heart for a two-week merogony-like phase, followed by a macrophage-mediated transport of the parasite to the gill, with a final development stage of a spore-laden xenoma within the endothelial and pillar cells. Xenoma rupture triggers a cascade of inflammatory events leading to severe, persistent, and extensive proliferative branchitis. The development of robust and reliable experimental challenge models using several exposure methods in marine and freshwater environments with several fish hosts, is a primary reason for the success of scientific research surrounding L. salmonae. To date, demonstrated factors affecting MGDS transmission include host species, strain and size, the length of contact time between naïve and infected fish, water temperature and flow rates.

Keywords

Loma salmonaeMicrosporatransmissionsalmonidhost–parasite interactionlife cycle
Type
Review Article
Information
Animal Health Research Reviews , Volume 8 , Issue 1 , June 2007 , pp. 59 - 68
Copyright
Copyright © Cambridge University Press 2007

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

Antonia, DB and Hedrick, RP (1995). Effect of water temperature on infections with the microsporidian Enterocytozoon salmonis in chinook salmon. Diseases of Aquatic Organisms 22: 233–236.CrossRefGoogle Scholar
Bader, JA, Shotts, EB Jr, Steffens, WL and Lom, J (1998). Occurrence of Loma cf. salmonae in brook, brown and rainbow trout from Buford Trout Hatchery, Georgia, USA. Diseases of Aquatic Organisms 34: 211–216.CrossRefGoogle Scholar
Beaman, HJ, Speare, DJ and Brimacombe, M (1999a). Regulatory effects of water temperature on Loma salmonae (Microspora) development in rainbow trout. Journal of Aquatic Animal Health 11: 237–245.2.0.CO;2>CrossRefGoogle Scholar
Beaman, HJ, Speare, DJ, Brimacombe, M and Daley, J (1999b). Evaluating protection against Loma salmonae generated from primary exposure of rainbow trout, Oncorhynchus mykiss (Walbaum), outside of the xenoma-expression temperature boundaries. Journal of Fish Diseases 22: 445–450.CrossRefGoogle Scholar
Becker, JA and Speare, DJ (2004a). Impact of a water temperature shift on xenoma clearance and recovery time during a Loma salmonae (Microsporidia) infection in rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms 58: 185–191.CrossRefGoogle ScholarPubMed
Becker, JA and Speare, DJ (2004b). Ultraviolet light control of horizontal transmission of Loma salmonae. Journal of Fish Diseases 27: 177–180.CrossRefGoogle ScholarPubMed
Becker, JA, Speare, DJ, Daley, J and Dick, P (2002). Effects of monensin dose and treatment time on xenoma reduction in microsporidial gill disease in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 25: 673–680.CrossRefGoogle Scholar
Becker, JA, Speare, DJ and Dohoo, IR (2003). Effect of water temperature and flow rate on the transmission of microsporidial gill disease caused by Loma salmonae in rainbow trout, Oncorhynchus mykiss. Fish Pathology 38: 105–112.CrossRefGoogle Scholar
Becker, JA, Speare, DJ and Dohoo, IR (2005a). Effect of the number of infected fish and acute exposure period on the horizontal transmission of Loma salmonae (Microsporidia) in rainbow trout, Oncorhynchus mykiss. Aquaculture 244: 1–9.CrossRefGoogle Scholar
Becker, JA, Speare, DJ and Dohoo, IR (2005b). Influence of feeding ratio and size on susceptibility to Microsporidial Gill Disease caused by Loma salmonae in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 28: 173–180.CrossRefGoogle ScholarPubMed
Becker, JA, Speare, DJ and Dohoo, IR (2006). Interaction of water temperature and challenge model on xenoma development rates for Loma salmonae (Microspora) in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 29: 139–145.CrossRefGoogle ScholarPubMed
Bigliardi, E and Sacchi, L (2001). Cell biology and invasion of the microsporidia. Microbes and Infection 3: 373–379.CrossRefGoogle ScholarPubMed
Bruno, DW, Collins, RO and Morrison, CM (1995). The occurrence of Loma salmonae (Protozoa: Microspora) in farmed rainbow trout, Oncorhynchus mykiss Walbaum, in Scotland. Aquaculture 133: 341–344.CrossRefGoogle Scholar
Cali, A and Takvorian, PM (1999). Developmental morphology and life cycles of the microsporidia. In: Wittner, M and Weiss, LM (eds) The Microsporidia and Microsporidiosis. Washington, DC: ASM Press, pp. 85–128.Google Scholar
Canning, EU and Lom, J (1986). Microsporidia of Vertebrates. Orlando, FL: Academic Press.Google Scholar
Chinabut, S, Tonguthai, K and Kamlerd, W (1992). The efficacy of fumagillin DCH against microsporidia and the tissue reaction of the infected African catfish, Clarias gariepinus Burch. In: Shariff, IM, Subasinghe, RP and Arthur, JR (eds) Diseases in Asian Aquaculture I. Manila, Philippines: Fish Health Section, Asian Fisheries Society, pp. 345–354.Google Scholar
Constantine, J (1999). Estimating the cost of Loma salmonae to B.C. aquaculture. BC, Canada: Ministry of Agriculture, Food and Fisheries.Google Scholar
Conteas, CN, Berlin, OGW, Ash, LR and Pruthi, JS (2000). Therapy for human gastrointestinal microsporidiosis. American Journal of Tropical Medicine and Hygiene 63: 121–127.CrossRefGoogle ScholarPubMed
Costa, SF and Weiss, LM (2000). Drug treatment of microsporidiosis. Drug Resistance Updates 3: 384–399.CrossRefGoogle ScholarPubMed
Didier, ES (1998). Microsporidiosis. Clinical Infectious Diseases 27: 1–8.CrossRefGoogle ScholarPubMed
Didier, ES, Didier, PJ, Snowden, KF and Shadduck, JA (2000). Microsporidiosis in mammals. Microbes and Infection 2: 709–720.CrossRefGoogle ScholarPubMed
Dinter, A and Berger, EG (1998). Golgi-disturbing agents. Histochemistry and Cell Biology 109: 571–590.CrossRefGoogle ScholarPubMed
Dunn, AM and Smith, JE (2001). Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3: 381–388.CrossRefGoogle ScholarPubMed
Gandhi, S, Locatelli, L and Feist, SW (1995). Occurrence of Loma sp. (Microsporidia) in farmed rainbow trout (Oncorhynchus mykiss) at a site in south west England. Bulletin of the European Association of Fish Pathologists 15: 58–60.Google Scholar
Georgiadis, MP, Gardner, IA and Hedrick, RP (2001). The role of epidemiology in the prevention, diagnosis and control of infectious diseases of fish. Preventive Veterinary Medicine 48: 287–302.CrossRefGoogle ScholarPubMed
Hauck, AK (1984). A mortality and associated tissue reactions of chinook salmon, Oncorhynchus tshawytscha (Walbaum) caused by the microsporidian Loma sp. Journal of Fish Diseases 7: 217–229.CrossRefGoogle Scholar
Hedrick, RP (1998). Relationships of the host, pathogen, and environment: implications for diseases of cultured and wild fish populations. Journal of Aquatic Animal Health 10: 107–111.2.0.CO;2>CrossRefGoogle Scholar
Higgins, MJ, Kent, ML, Moran, JD, Weiss, LM and Dawe, SC (1998). Efficacy of the fumagillin analog TNP-470 for Nucleospora salmonis and Loma salmonae infections in chinook salmon Oncorhynchus tshawytscha. Diseases of Aquatic Organisms 34: 45–49.CrossRefGoogle ScholarPubMed
Jones, SRM and Groman, DB (2001). Cohabitation transmission of infectious salmon anemia virus among freshwater-reared Atlantic salmon. Journal of Aquatic Animal Health 13: 340–346.2.0.CO;2>CrossRefGoogle Scholar
Keeling, PJ and Fast, NM (2002). Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology 56: 93–116.CrossRefGoogle ScholarPubMed
Kent, ML (1998). Introduction. In: Kent, ML and Poppe, TT (eds) Diseases of Seawater Netpen-reared Salmonid Fishes, 2nd edn. Nanaimo, Canada: Fisheries and Oceans Canada, pp. 1–2.Google Scholar
Kent, ML, Elliot, DG, Groff, JM and Hedrick, RP (1989). Loma salmonae (Protozoa: Microspora) infections in seawater reared coho salmon Oncorhynchus kisutch. Aquaculture 80: 211–222.CrossRefGoogle Scholar
Kent, ML, Dawe, SC and Speare, DJ (1995). Transmission of Loma salmonae (Microsporea) to chinook salmon in seawater. Canadian Veterinary Journal 36: 98–101.Google Scholar
Kent, ML, Dawe, SC and Speare, DJ (1999). Resistance to reinfection in chinook salmon Oncorhynchus tshawytscha to Loma salmonae (Microsporidia). Diseases of Aquatic Organisms 37: 205–208.CrossRefGoogle ScholarPubMed
Lapatra, SE (1998). Factors affecting pathogenicity of infectious hematopoietic necrosis virus (IHNV) for salmonid fish. Journal of Aquatic Animal Health 10: 121–131.2.0.CO;2>CrossRefGoogle Scholar
Lapatra, SE, Groberg, WJ, Rohovec, JS and Fryer, JL (1990). Size-related susceptibility of salmonids to two strains of infectious hematopoietic necrosis virus. Transactions of the American Fisheries Society 119: 25–30.2.3.CO;2>CrossRefGoogle Scholar
Lom, J and Nilsen, F (2003). Fish microsporidia: fine structural diversity and phylogeny. International Journal of Parasitology 33: 107–127.CrossRefGoogle ScholarPubMed
Lovy, J, Wadowska, DW, Wright, GM and Speare, DJ (2004). Morphological characterization and notes on the life cycle of a newly discovered variant of Loma salmonae (Putz, Hoffman & Dunbar) from a natural infection of chinook salmon, Oncorhynchus tshawytscha (Walbaum). Journal of Fish Diseases 27: 609–616.CrossRefGoogle ScholarPubMed
Lovy, J, Wright, GM, Wadowska, DW and Speare, DJ (2006). Ultrastructural morphology suggesting a new hypothesis for development of microsporidians seen in Loma salmonae infecting the gills of rainbow trout and brook trout. Journal of Fish Biology 68: 450–457.CrossRefGoogle Scholar
Magor, BG (1987). First report of Loma sp. (Microsporidia) in juvenile coho salmon (Oncorhynchus kisutch) from Vancouver Island, British Columbia. Canadian Journal of Zoology 65: 751–752.CrossRefGoogle Scholar
Markey, PT, Blazer, VS, Ewing, MS and Kocan, KM (1994). Loma sp. in salmonids from the eastern United States associated with lesions in rainbow trout. Journal of Aquatic Animal Health 6: 318–328.2.3.CO;2>CrossRefGoogle Scholar
Ministry of Agriculture and Lands (MAL) (2005). Fisheries Statistics – Salmon Aquaculture in British Columbia. [Available online at http://www.agf.gov.bc.ca/fish_stats/aqua-salmon.htm.]Google Scholar
Morrison, CM and Sprague, V (1983). Loma salmonae (Putz, Hoffman and Dunbar, 1965) in the rainbow trout, Salmo gairdneri Richardson, and L. fontinalis sp. nov. (Microsporidia) in the brook trout, Salvelinus fontinalis (Mitchill). Journal of Fish Diseases 6: 345–353.CrossRefGoogle Scholar
Nordmo, R and Ramstad, A (1999). Variables affecting the challenge pressure of Aeromonas salmonicida and Vibrio salmonicida in Atlantic salmon (Salmo salar L.). Aquaculture 171: 1–12.CrossRefGoogle Scholar
Poynton, SL (1986). Distribution of the flagellate Hexamita salmonis Moore, 1922 and the microsporidian Loma salmonae Putz, Hoffman and Dunbar, 1965 in brown trout, Salmo trutta L., and rainbow trout, Salmo gairdneri Richardson, in the River Itchen (U.K.) and three of its fish farms. Journal of Fish Biology 29: 417–429.CrossRefGoogle Scholar
Ramsay, JM, Speare, DJ, Sánchez, JG and Daley, J (2001). The transmission potential of Loma salmonae (Microspora) in the rainbow trout, Oncorhynchus mykiss (Walbaum), is dependent upon the method and timing of exposure. Journal of Fish Diseases 24: 453–460.CrossRefGoogle Scholar
Ramsay, JM, Speare, DJ, Dawe, SC and Kent, ML (2002). Xenoma formation during microsporidial gill disease of salmonids caused by Loma salmonae is affected by host species (Oncorhynchus tshawytscha, O. kisutch, O. mykiss) but not by salinity. Diseases of Aquatic Organisms 48: 125–131.CrossRefGoogle Scholar
Ramsay, JM, Speare, DJ, Becker, JA and Daley, J (2003). Loma salmonae-associated xenoma onset and clearance in rainbow trout, Oncorhynchus mykiss (Walbaum): comparison of per os and cohabitation exposure using survival analysis. Aquaculture Research 34: 1329–1335.CrossRefGoogle Scholar
Rodriguez-Tovar, LE, Wright, GM, Wadowska, DW, Speare, DJ and Markham, RJF (2002). Ultrastructural study of the early development and localization of Loma salmonae in the gills of experimentally infected rainbow trout. Journal of Parasitology 88: 244–253.CrossRefGoogle ScholarPubMed
Rodriguez-Tovar, LE, Becker, JA, Markham, RJF and Speare, DJ (2006). Induction time for resistance to Microsporidial Gill Disease caused by Loma salmonae following vaccination of rainbow trout (Oncorhynchus mykiss) with a spore-based vaccine. Fish and Shellfish Immunology 21: 170–175.CrossRefGoogle ScholarPubMed
Sánchez, JG, Speare, DJ and Markham, RJF (2000). Normal and aberrant tissue distribution of Loma salmonae (Microspora) within rainbow trout, Oncorhynchus mykiss (Walbaum), following experimental infection at water temperatures within and outside of the xenoma-expression temperature boundaries. Journal of Fish Diseases 23: 235–242.CrossRefGoogle Scholar
Sánchez, JG, Speare, DJ and Markham, RJF (2001a). Altered tissue distribution of Loma salmonae effects of natural and acquired resistance. Journal of Fish Diseases 24: 33–40.CrossRefGoogle Scholar
Sánchez, JG, Speare, DJ, Markham, RJF and Jones, SRM (2001b). Experimental vaccination of rainbow trout against Loma salmonae using a live low-virulence variant of L. salmonae. Journal of Fish Biology 59: 442–448.Google Scholar
Sánchez, JG, Speare, DJ, Markham, RJF and Jones, SRM (2001c). Isolation of a Loma salmonae variant: biological characteristics and host range. Journal of Fish Biology 59: 427–441.CrossRefGoogle Scholar
Sánchez, JG, Speare, DJ, Markham, RJF, Wright, GM and Kibenge, FSB (2001d). Localization of the initial developmental stages of Loma salmonae in rainbow trout (Oncorhynchus mykiss). Veterinary Pathology 38: 540–546.CrossRefGoogle ScholarPubMed
Shaw, RW and Kent, ML (1999). Fish Microsporidia. In: Wittner, M and Weiss, LM (eds) The Microsporidia and Microsporidiosis. Washington, DC: ASM Press, pp. 418–446.Google Scholar
Shaw, RW, Kent, ML and Adamson, ML (1998). Modes of transmission of Loma salmonae (Microsporidia). Diseases of Aquatic Organisms 33: 151–156.CrossRefGoogle ScholarPubMed
Shaw, RW, Kent, ML and Adamson, ML (2000). Innate susceptibility differences in chinook salmon Oncorhynchus tshawytscha to Loma salmonae (Microsporidia). Diseases of Aquatic Organisms 43: 49–53.CrossRefGoogle ScholarPubMed
Speare, DJ and Daley, J (2003). Failure of vaccination in brook trout Salvelinus fontinalis against Loma salmonae (Microspora). Fish Pathology 38: 27–28.CrossRefGoogle Scholar
Speare, DJ, Arsenault, GJ and Buote, MA (1998a). Evaluation of rainbow trout as a model for use in studies on pathogenesis of the branchial microsporidian Loma salmonae. Contemporary Topics in Laboratory Animal Science 37: 55–58.Google Scholar
Speare, DJ, Beaman, HJ, Jones, SRM, Markham, RJF and Arsenault, GJ (1998b). Induced resistance in rainbow trout, Oncorhynchus mykiss (Walbaum), to gill disease associated with the microsporidian gill parasite Loma salmonae. Journal of Fish Diseases 21: 93–100.CrossRefGoogle ScholarPubMed
Speare, DJ, Daley, J, Markham, RJF, Beaman, HJ and Sánchez, JG (1998c). Loma salmonae associated growth suppression in rainbow trout (Oncorhynchus mykiss) occurs during early-onset xenoma dissolution as determined by in situ hybridization and immunohistochemistry. Journal of Fish Diseases 21: 345–354.CrossRefGoogle Scholar
Speare, DJ, Athanassopoulou, F, Daley, J and Sánchez, JG (1999a). A preliminary investigation of alternatives to fumagillin for the treatment of Loma salmonae infection in rainbow trout. Journal of Comparative Pathology 121: 241–248.CrossRefGoogle ScholarPubMed
Speare, DJ, Beaman, HJ and Daley, J (1999b). Effect of water temperature manipulation on a thermal unit predictive model for Loma salmonae. Journal of Fish Diseases 22: 277–283.CrossRefGoogle Scholar
Speare, DJ, Daley, J, Dick, P, Novilla, M and Poe, S (2000). Ionophore-mediated inhibition of xenoma-expression in trout challenged with Loma salmonae (Microspora). Journal of Fish Diseases 23: 231–233.CrossRefGoogle Scholar
Vávra, J and Larsson, JIR (1999). Structure of the Microsporidia. In: Wittner, M and Weiss, LM (eds) The Microsporidia and Microsporidiosis. Washington, DC: ASM Press, pp. 7–84.Google Scholar
Wittner, M (1999). Historic perspective on the microsporidia: expanding horizons. In: Wittner, M and Weiss, LM (eds) The Microsporidia and Microsporidiosis. Washington, DC: ASM Press, pp. 1–6.CrossRefGoogle Scholar