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Lagenidium giganteum forma caninum

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Lagenidium giganteum forma caninum
Scientific classification
Domain:
Eukaryota
(unranked):
SAR
Superphylum:
Heterokonta
Class:
Oomycota
Order:
Lagenidiales
Family:
Lagenidiaceae
Genus:
Lagenidium
Species:
L. giganteum
Form:
L. g. f. caninum
Trinomial name
Lagenidium giganteum f. caninum
Histological section of the intestine of a dog with lagenidiosis. Organisms are highlighted in black in the submucosa of the intestine. 10x (Grocott's methenamine silver).

Lagenidium giganteum forma caninum is a fungus-like organism belonging to the genus Lagenidium and causes lagenidiosis in some mammal species. Lagenidiosis is a disease characterized by progressive, severe and invasive cutaneous, subcutaneous and disseminated infection. Clinical and pathological aspects of the disease are almost identical to pythiosis. The first cases of lagenidiosis in mammals were officially reported in dogs in 2003.[1][2] Since then, it has become increasingly recognized in dogs and cats as a cause of skin lesions.[3]

Taxonomy

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The genus Lagenidium was first registered in the Index Fungorum in 1857.[4] It belongs to the family of Lagenidiaceae, order of Lagenidiales and class Oomycota.[5][6][7] Lagenidium contains many saprotrophic species, at least two of which are responsible for disease in animals: L. giganteum forma caninum and L. decidium. [3][2][8] According to The National Center for Biotechnology Information, there are seven species officially registered within the genus, including the f. caninum and 30 unclassified strains.[7]

Lagenidium species can be found in a wide variety of hosts, including algae, phytoplankton, pollen, and crustaceans. The genus consists mainly of entomopathogenic organisms.[9] L. giganteum was formerly used for biological control of mosquitoes, but is now deregistered by the United States Environmental Protection Agency.[10] In 1999, a new species with phylogenetic similarity to L. giganteum was discovered in dogs with skin infection. It was recognized taxonomically and officially as forma caninum in 2013[1][2][11] and has been isolated from mammalian tissue lesions in the last two decades.[2][8] The main phenotypic difference observed between these taxa is the divergent ability to grow at mammalian body temperature (≈ 36-39 °C), strongly suggesting that this feature is key to mammalian pathogenicity.[9] Considering the strong relationship between Lagenidium giganteum forma caninum and L. giganteum f. giganteum, it is also suggested that further investigation of host specificity and potential mammalian pathogenicity of L. giganteum f. giganteum should be assessed.[11] Other genera of oomycetes, such as Pythium and Phytophthora, are economically important plant pathogens and species within the genera Pyhtium, Saprolegnia, Achlya and Aphanomyces are also animal pathogens. However, there are reports of a plant oomycete being pathogenic for animals, or vice versa, including species within Lagenidium genera.[12]

Life cycle

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Life cycle of Saprolegnia sp., an important oomycete pathogen of aquatic amphibians and fishes.

The life cycle and habitat of L. giganteum f. caninum is similar to its related species, L. giganteum, which can grow without a host. It can be found in bodies of fresh water and is observed to sustain mosquito populations.[13] The life cycle of L. giganteum is initiated by a biflagellate zoospore that infects a mosquito larvae host by attachment, and undergoes encystment, penetration, and growth. The zoospore production can occur either by sexual or asexual reproduction that seems to require exogenous sources of sterols structurally related to cholesterol. For mycelial growth, the organism kills the host by starvation. Cells can reproduce asexually while forming an exit tube, where the content migrates to the tube's tip and quickly matures into zoospores, or alternately, two cells can fuse, forming oospores as seen in Saprolegnia sp. cycle. Lagenidum giganteum can undergo a latent stage surviving for long periods (months to years).[14] The saprophytic or vegetative stage of the oomycetes from the genus Lagenidium is characterized by filamentous mycelial growth and requires little carbon and nitrogen sources. Hyphae can survive indefinitely as a saprophyte while using energy source from rotting vegetation, dead insects, or other organic material.[13][14]

Morphologic characteristics

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Histological section of the intestine of a dog with lagenidiosis. Organisms are seen in the lumen of a blood vessel associated with eosinophilic and granulomatous inflammation, necrosis and vasculitis (arrows). The hyphal structures are wide, measuring 2–7 μm, showing negative staining, ribbon-like, rarely septate and have an irregular, non-parallel wall 40x (Hematoxylin & Eosin).

Lagenidium spp. colonies from mammalian strains are characterized by a colorless or yellow aerial mycelia presenting an irregular radiating pattern. The mycelium has oval and spherical segments (30–40 μm) and hyphae are composed by irregular large segments of more than 400 μm, containing 1–2 discharge tubes with terminal vesicles enclosing zoospores (9–12 μm each). Encysted zoospores contain germ tubes.[9] Broad hyphal structures of Lagenidium giganteum forma caninum can also be seen in histopathological specimens with a mean diameter of 4 μm (range, 2–7 μm) and are rarely septate with nonparallel walls and irregular branching.[15]

Pathogenicity and relevance for animals and humans

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The mechanism of infection for Lagenidium giganteum forma caninum and P. insidiosum in animals is similar, and also seems to be similar to the host infection mechanism used for L. giganteum. After finding a suitable host, the zoospores can penetrate the skin, usually in areas with a previous injury.[2] One important relevant risk factor associated with the occurrence of the disease in domestic animals includes swimming in contaminated lakes and ponds with the potential presence of the organism.[9] The main species affected with lagenidiosis are dogs and cats, and the disease has been characterized by clinical and pathological aspects that resemble those caused by P. insidiosum. However, there are often more invasive cutaneous and subcutaneous lesions, with rapid progress and poor response to treatment and prognosis. Cutaneous injuries are seen as ulcerative, firm, and nodular, with a sinus tract and frequently encompassing lymphatic involvement, and in some cases, can be macroscopically similar to cutaneous infections caused by Basidiobolus raranarum.[2] There are no official reports of Lagenidium species causing infection in humans but at least one case of human ocular lagenidiosis has been documented.[16]

Diagnosis

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The diagnosis of various forms of oomycosis in mammals is very difficult by clinical and pathological evaluation alone. It is necessary to perform complementary diagnostic tests to properly describe the causative agent. The definitive diagnosis of Lagenidium giganteum forma caninum is mainly based on culture, serological tests, and molecular-based diagnosis such as conventional or panfungal PCR.[2][15]

Treatment

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While L. giganteum is susceptible to extreme temperatures (less than 8 °C and greater than 34 °C) in the environment and when inside of the mosquito larvae host, to insecticidal substances like organophosphates and carbamates.[13] The organism responds poorly to traditional fungal therapy as use for the other oomycetes. The absence of ergosterol in the oomycete cell makes azole-type antifungal drugs useless. Reports of various drugs (e.g., tigecycline) targeting oomycota in vitro have been published recently,[17] but there is still a lack of strong evidence for them. The clinical management for the disease is currently radical surgery of the affected area.[9]

References

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  1. ^ a b Amy M. Grooters; Christoffel F.J. Spies; Chi-yu Chen; Sally L. Glockling; C. André Lévesque; Arthur W.A.M. de Cock. "Index Fungorum no. 34". Index Fungorum.
  2. ^ a b c d e f g Grooters, Amy M. (2003-07-01). "Pythiosis, lagenidiosis, and zygomycosis in small animals". Veterinary Clinics of North America: Small Animal Practice. 33 (4): 695–720. doi:10.1016/S0195-5616(03)00034-2. ISSN 0195-5616. PMID 12910739.
  3. ^ a b Hartfield, J.N.; Grooters, A.M.; Waite, K.J. (2014). "Development and Evaluation of an ELISA for the Quantitation of Anti-Lagenidium giganteum forma caninum Antibodies in Dogs". Journal of Veterinary Internal Medicine. 28 (5): 1479–1484. doi:10.1111/jvim.12427. ISSN 0891-6640. PMC 4895562. PMID 25274441.
  4. ^ "Index Fungorum - Names Record". www.indexfungorum.org. Retrieved 2023-11-03.
  5. ^ "Lagenidium Schenk 1857 names - Encyclopedia of Life". eol.org. Retrieved 2023-11-03.
  6. ^ "ITIS - Report: Lagenidiaceae". www.itis.gov. Retrieved 2023-11-03.
  7. ^ a b taxonomy. "Taxonomy browser (Lagenidium)". www.ncbi.nlm.nih.gov. Retrieved 2023-11-03.
  8. ^ a b Shmalberg, Justin; Moyle, Patrick S.; Craft, William F.; Walton, Stuart A. (April 2020). "Severe meningoencephalitis secondary to calvarial invasion of Lagenidium giganteum forma caninum in a dog". Open Veterinary Journal. 10 (1): 31–38. doi:10.4314/ovj.v10i1.6. PMC 7193878. PMID 32426254.
  9. ^ a b c d e Vilela, Raquel; Taylor, John W.; Walker, Edward D.; Mendoza, Leonel (February 2015). "Lagenidium giganteum Pathogenicity in Mammals". Emerging Infectious Diseases. 21 (2): 290–297. doi:10.3201/eid2102.141091. ISSN 1080-6040. PMC 4313650. PMID 25625190.
  10. ^ "Search Results | Govinfo". www.govinfo.gov. Retrieved 2023-11-03.
  11. ^ a b Spies, Christoffel F. J.; Grooters, Amy M.; Lévesque, C. André; Rintoul, Tara L.; Redhead, Scott A.; Glockling, Sally L.; Chen, Chi-yu; de Cock, Arthur W. A. M. (2016-08-01). "Molecular phylogeny and taxonomy of Lagenidium-like oomycetes pathogenic to mammals". Fungal Biology. 120 (8): 931–947. doi:10.1016/j.funbio.2016.05.005. ISSN 1878-6146. PMID 27521626.
  12. ^ Phillips, Andrew J.; Anderson, Victoria L.; Robertson, Emma J.; Secombes, Chris J.; van West, Pieter (January 2008). "New insights into animal pathogenic oomycetes". Trends in Microbiology. 16 (1): 13–19. doi:10.1016/j.tim.2007.10.013. ISSN 0966-842X. PMID 18096392.
  13. ^ a b c "Lagenidium giganteum". biocontrol.entomology.cornell.edu. Retrieved 2023-11-03.
  14. ^ a b Kerwin, James L. (2007). "Oomycetes: Lagenidium giganteum". Journal of the American Mosquito Control Association. 23 (2 Suppl): 50–57. doi:10.2987/8756-971X(2007)23[50:OLG]2.0.CO;2. ISSN 8756-971X. PMID 17853597. S2CID 21140193.
  15. ^ a b Rodrigues Hoffmann, Aline; Ramos, Maiara G.; Walker, Randall T.; Stranahan, Lauren W. (November 2023). "Hyphae, pseudohyphae, yeasts, spherules, spores, and more: A review on the morphology and pathology of fungal and oomycete infections in the skin of domestic animals". Veterinary Pathology. 60 (6): 812–828. doi:10.1177/03009858231173715. ISSN 1544-2217. PMID 37222139. S2CID 258863690.
  16. ^ Reinprayoon, Usanee; Permpalung, Nitipong; Kasetsuwan, Ngamjit; Plongla, Rongpong; Mendoza, Leonel; Chindamporn, Ariya (August 2013). "Lagenidium sp. Ocular Infection Mimicking Ocular Pythiosis". Journal of Clinical Microbiology. 51 (8): 2778–2780. doi:10.1128/JCM.00783-13. ISSN 0095-1137. PMC 3719631. PMID 23740721.
  17. ^ Worasilchai, N.; Chindamporn, A.; Plongla, R.; Torvorapanit, P.; Manothummetha, K.; Chuleerarux, N.; Permpalung, N. (2020). "In Vitro Susceptibility of Thai Pythium insidiosum Isolates to Antibacterial Agents". Antimicrobial Agents and Chemotherapy. 64 (4). doi:10.1128/AAC.02099-19. PMC 7179303. PMID 32015039.
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