Abstract
Protothecosis is a rare disease caused by environmental algae of the genus Prototheca. These are saprophytic, non-photosynthetic, aerobic, colorless algae that belong to the Chlorellaceae family. Seven different species have been described. Prototheca zopfii genotype 2 and P. wickerhamii are most commonly involved in pathogenic infections in humans and animals. The objective of this work is to describe, for the first time, a case of protothecosis caused by P. zopfii genotype 1 in a dog. The dog, a 4-year-old mix bred male, was presented to a veterinary clinic in Montevideo, Uruguay, with multiple skin nodules, one of which was excised by surgical biopsy. The sample was examined histologically and processed by PCR, DNA sequencing, and restriction fragments length polymorphisms for the detection and genotyping of P. zopfii. In addition, transmission electron microscopy and scanning electron microscopy were performed. Histology showed severe ulcerative granulomatous dermatitis and panniculitis with myriads of pleomorphic algae. Algal cells were 4–17 µm in size, with an amphophilic, 2–4-µm-thick wall frequently surrounded by a clear halo, contained flocculant material and a deeply basophilic nucleus, and internal septae with daughter cells (endospores) consistent with endosporulation. Ultrastructurally, algal cells/endospores at different stages of development were found within parasitophorous vacuoles in macrophages. Prototheca zopfii genotype 1 was identified by molecular testing, confirming the etiologic diagnosis of protothecosis.
Similar content being viewed by others
References
Pal M, Abraha A, Rahman MT, Dave P. Protothecosis: an emerging algal disease of humans and animals. Int J Life Sci Biotechnol Pharm Res. 2014;3:1–13.
Stenner VJ, Mackay B, King T, Barrs VR, Irwin P, Abraham L, Swift N, Langer N, Bernays M, Hampson E, Martin P, Krockenberger MB, Bosward K, Latter M, Malik R. Protothecosis in 17 Australian dogs and a review of the canine literature. Med Mycol. 2007;45:249–66.
Masuda M, Hirose N, Ishikawa T, Ikawa Y, Nishimura K. Prototheca miyajii sp. nov., isolated from a patient with systemic protothecosis. Int J Syst Evol Microbiol. 2016;66:1510–20.
Carfora V, Noris G, Caprioli A, Iurescia M, Stravino F, Franco A. Evidence of a Prototheca zopfii genotype 2 disseminated infection in a dog with cutaneous lesions. Mycopathologia. 2017;182:603–8.
Mayorga J, Gómez JFB, Martínez APV, Estrada VFM, Welsh O. Protothecosis. Clin Dermatol. 2012;30:432–6.
Moller A, Truyen U, Roesler U. Prototheca zopfii genotype 2-the causative agent of bovine protothecal mastitis? Vet Microbiol. 2007;120:370–4.
Papadogiannakis EI, Velonakis EN, Spanakos GK, Koutinas AF. Cutaneous disease as sole clinical manifestation of protothecosis in a boxer dog. Case Rep Vet Med. 2016. https://doi.org/10.1155/2016/2878751.
Schöniger S, Roschanski N, Rösler U, Vidovic A, Nowak M, Dietz O, Wittenbrink MM, Schoon HA. Prototheca species and Pithomyces chartarum as causative agents of rhinitis and/or sinusitis in horses. J Comp Pathol. 2016;155:21–125.
Shank AM, Dubielziq RD, Teixeira LB. Canine ocular protothecosis: a review of 14 cases. Vet Ophthalmol. 2015;18:437–42.
Font C, Mascort J, Marquez M, Esteban C, Sanchez D, Durall N, Pumarola M, Lujan-Feliu-Pascual A. Paraparesis as initial manifestation of a Prototheca zopfii infection in a dog. J Small Anim Pract. 2014;55:283–6.
Marquez M, Rodenas S, Molin J, Rabanal RM, Fondevila D, Añor S, Pumarola M. Protothecal pyogranulomatous meningoencephalitis in a dog without evidence of disseminated infection. Vet Rec. 2012;171:100.
Gross TL, Ihrke PJ, Walder EJ, Affolter VK. Infectious nodular and diffuse granulomatous and pyogranulomatous diseases of the skin. In: Gross TL, Ihrke PJ, Walder EJ, Affolter VK, editors. Skin diseases of the dog and cat. Oxford: Blackwell Publishing Inc; 2005. p. 272–319.
Huth N, Wenkel RF, Roschanski N, Rösler U, Plagge L, Schöniger S. Prototheca zopfii genotype 2-induced nasal dermatitis in a cat. J Comp Pathol. 2015;152:287–90.
Ginel PJ, Perez J, Molleda JM, Lucena R, Mozos E. Cutaneous protothecosis in a dog. Vet Rec. 1997;140:651–3.
Phelps NBD, Mor SK, Armién AG, Pelican KM, Goyal SM. Description of the microsporidian parasite, Heterosporis sutherlandae n. sp. infecting fish in the Great Lakes region, USA. PLoS ONE. 2015;18:e0132027.
Aouay A, Coppée F, Cloet S, Cuvelier P, Belayew A, Lagneau PE, Mullender C. Molecular characterization of Prototheca strains isolated from bovine mastitis. J Mycol Med. 2015;18:224–7.
Sobukawa H, Kano R, Ito T, Onozaki M, Makimura K, Hasegawa A, Kamata H. In vitro susceptibility of Prototheca zopfii genotypes 1 and 2. Med Mycol. 2011;49:222–4.
Ito T, Kano R, Sobukawa H, Ogawa J, Honda Y, Hosoi Y, Shibuya H, Sato T, Hasegawa A, Kamata H. Experimental infection of bovine mammary gland with Prototheca zopfii genotype 1. J Vet Med Sci. 2011;73:117–9.
Ribeiro MG, Rodrigues de Farias M, Roesler U, Roth K, Rodigheri SM, Ostrowsky MA, Salerno T, Sigueira AK, Fernandes MC. Phenotypic and genotypic characterization of Prototheca zopfii in a dog with enteric signs. Res Vet Sci. 2009;87(3):479–81.
Souza NL, Estrela-Lima A, Moreira ELT, Ribeiro LGR, Xavier MN, Silva TMA, Costa EA, Santos RL. Systemic canine protothecosis. Braz J Vet Pathol. 2009;2(2):102–6.
Spampinato MF, Kujman S, Cantón J, Daglio C, Catena M. Prototecosis canina: primer reporte en Argentina. Rev Vet. 2017;28(2):168–71 (in Spanish).
Morandi S, Cremonesi P, Capra E, Silvetti T, Decimo M, Bianchini V, Alves AC, Vargas AC, Costa GM, Ribeiro MG, Brasca M. Molecular typing and differences in biofilm formation and antibiotic susceptibilities among Prototheca strains isolated in Italy and Brazil. J Dairy Sci. 2016;99(8):6436–45.
Lane LV, Meinkoth JH, Brunker J, Smith SK 2nd, Snider TA, Thomas J, Bradway D, Love BC. Disseminated protothecosis diagnosed by evaluation of CSF in a dog. Vet Clin Pathol. 2012;41(1):147–52.
Ahrholdt J, Murugaiyan J, Straubinger RK, Jagielski T, Roesler U. Epidemiological analysis of worldwide bovine, canine and human clinical Prototheca isolates by PCR genotyping and MALDI-TOF mass spectrometry proteomic phenotyping. Med Mycol. 2012;50(3):234–43.
Hirose N, Hua Z, Kato Y, Zhang Q, Li R, Nishimura K, Masuda M. Molecular characterization of Prototheca strains isolated in China revealed the first cases of protothecosis associated with Prototheca zopfii genotype 1. Med Mycol. 2017. https://doi.org/10.1093/mmy/myx039.
Irrgang A, Murugaiyan J, Weise C, Azab W, Roesler U. Well-known surface and extracellular antigens of pathogenic microorganisms among the immunodominant proteins of the infectious microalgae Prototheca zopfii. Front Cell Infect Microbiol. 2015;5:67.
Acknowledgements
The authors thank Yisell Perdomo from the “Instituto Nacional de Investigación Agropecuaria” (INIA, Uruguay), Jan Shivers and Dean Muldoon from the University of Minnesota Veterinary Diagnostic Laboratory (USA), and Dominique Rollin from the Centers for Disease Control and Prevention (CDC) for technical assistance. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the CDC.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical Approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Handling Editor: Rui Kano.
Rights and permissions
About this article
Cite this article
Silveira, C.S., Cesar, D., Keating, M.K. et al. A Case of Prototheca zopfii Genotype 1 Infection in a Dog (Canis lupus familiaris). Mycopathologia 183, 853–858 (2018). https://doi.org/10.1007/s11046-018-0274-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11046-018-0274-5