Cutaneous alternariosis in an immunocompromised dog successfully treated with cold plasma and cessation of immunosuppressive medication

Janine Classen; Berrett Dengler; Christoph J. Klinger; Sonya V. Bettenay; Volker Rickerts; Ralf S. Mueller

doi:10.15654/TPK-160851

Tierärztliche Praxis Ausgabe K: Kleintiere / Heimtiere, Table of Contents

Tierarztl Prax Ausg K Kleintiere Heimtiere 2017; 45(05): 337-343
DOI: 10.15654/TPK-160851

Case Report

Schattauer GmbH

Cutaneous alternariosis in an immunocompromised dog successfully treated with cold plasma and cessation of immunosuppressive medication

Kutane Alternariose eines immunsupprimierten Hundes erfolgreich behandelt mit Kaltplasma und Absetzen der immunsuppressiven Therapie

Janine Classen

¹Clinic of Small Animal Medicine, Centre for Clinical Veterinary Medicine, Ludwig-Maximilians University, Munich, Germany

,

Berrett Dengler

¹Clinic of Small Animal Medicine, Centre for Clinical Veterinary Medicine, Ludwig-Maximilians University, Munich, Germany

,

Christoph J. Klinger

¹Clinic of Small Animal Medicine, Centre for Clinical Veterinary Medicine, Ludwig-Maximilians University, Munich, Germany

,

Sonya V. Bettenay

²Tierdermatologie Deisenhofen, Oberhaching, Germany

,

Volker Rickerts

³Robert Koch Institute, Berlin, Germany

,

Ralf S. Mueller

¹Clinic of Small Animal Medicine, Centre for Clinical Veterinary Medicine, Ludwig-Maximilians University, Munich, Germany

› Author Affiliations

Abstract

Summary

A cutaneous infection with Alternaria spp. was diagnosed in a 2-yearold male intact Irish setter dog, presenting with multifocal papules, plaques and ulcerations involving all four distal limbs, shoulder blades, scrotum, pinnae and nasal mucous membranes. The dog had been treated for inflammatory bowel disease and lymphangiectasia with immunosuppressive doses of cyclosporine and prednisolone for approximately 3 months. The diagnosis was based on clinical signs, the demonstration of fungal elements within skin biopsies, deep fungal culture and fungal PCR from a formalin-fixed tissue specimen. Complete clinical remission was achieved by tapering and cessation of the immunosuppressive medication, treatment with cold atmospheric-pressure plasma (CAPP) and topical enilconazole within 8 weeks.

Zusammenfassung

Bei einem 2 Jahre alten, männlich intakten Irish Setter wurde eine kutane Infektion mit Alternaria spp. diagnostiziert. Der Hund zeigte Papeln, Plaques und Ulzerationen an allen distalen Gliedmaßen, Schulterblättern, Skrotum, Pinnae und nasalen Schleimhäuten. Das Tier erhielt seit ca. 3 Monaten immunsuppressive Dosen von Ciclosporin und Prednisolon zur Behandlung einer chronisch-entzündlichen Darmerkrankung und Lymphangiektasie. Die Diagnose wurde anhand der klinischen Symptomatik, dem Vorliegen von Pilzelementen in Hautbioptaten, einer Pilzkultur aus tiefen Gewebeproben sowie einer PCR-Untersuchung von formalinfixiertem Gewebe auf Pilze gestellt. Durch Absetzen der immunsuppressiven Therapie nach Dosisreduktion sowie topische Behandlung mit Kaltplasma und Enilkonazol ließ sich innerhalb von 8 Wochen eine komplette klinische Remission erreichen.

Keywords

Canine - Alternaria infection - skin - kINPen^® VET - therapy

Schlüsselwörter

Kanin - Alternaria-Infektion - Haut - kINPen^® VET - Therapie

Full Text

References

References
1 Alkawareek MY, Algwari QT, Laverty G, Gorman SP, Graham WG, O’Connell D, Gilmore BF. Eradication of Pseudomonas aeruginosa Biofilms by Atmospheric Pressure Non-Thermal Plasma. PLoS One 2012; 7: e44289.
2 Arndt S, Unger P, Wacker E, Shimizu T, Heinlin J, Li YF, Thomas HM, Morfill GE, Zimmermann JL, Bosserhoff AK, Karrer S. Cold atmospheric plasma (CAP) changes gene expression of key molecules of the wound healing machinery and improves wound healing in vitro and in vivo. PLoS One 2013; 8: e79325.
3 Bekeschus S, Schmidt A, Weltmann K-D, von Woedtke T. The plasma jet kINPen – A powerful tool for wound healing. Clin Plasma Med 2016; 4: 19-28.
4 Blanco JL, Garcia ME. Immune response to fungal infections. Vet Immunol Immunopathol 2008; 125: 47-70.
5 Daeschlein G, Scholz S, Ahmed R, von Woedtke T, Haase H, Niggemeier M, Kindel E, Brandenburg R, Weltmann KD, Juenger M. Skin decontamination by low-temperature atmospheric pressure plasma jet and dielectric barrier discharge plasma. J Hosp Infect 2012; 81: 177-183.
6 Daeschlein G, Scholz S, Woedtke Tv. et al. In Vitro Killing of Clinical Fungal Strains by Low-Temperature Atmospheric-Pressure Plasma Jet. IEEE Transactions on Plasma Science 2011; 39: 815-821.
7 Daeschlein G, Scholz S, Emmert S. et al. Plasma Medicine in Dermatology: Basic Antimicrobial Efficacy Testing as Prerequisite to Clinical Plasma Therapy. Plasma Medicine 2012; 2: 33-69.
8 de Hoog GS, Gene J, Figueras MJ. Atlas of Clinical Fungi. Baarn, The Netherlands: Centraalbureau voor Schimmelcultures; 2000
9 Dedola C, Stuart AP, Ridyard AE. et al. Cutaneous Alternaria infectoria infection in a dog in association with therapeutic immunosuppression for the management of immune-mediated haemolytic anaemia. Vet Dermatol 2010; 21: 626-634.
10 Dye C, Johnson EM, Gruffydd-Jones TJ. Alternaria species infection in nine domestic cats. J Feline Med Surg 2009; 11: 332-336.
11 Fluhr JW, Sassning S, Lademann O. et al. In vivo skin treatment with tissue-tolerable plasma influences skin physiology and antioxidant profile in human stratum corneum. Exp Dermatol 2012; 21: 130-134.
12 Fricke K, Koban I, Tresp H. et al. Atmospheric pressure plasma: a high-performance tool for the efficient removal of biofilms. PLoS One 2012; 7: e42539.
13 Fridman A, Chirokov A, Gutsol A. Non-thermal atmospheric pressure discharges. J Phys D: Appl Phys 2005; 38: R1.
14 Gay-Mimbrera J, Garcia MC, Isla-Tejera B, Rodero-Serrano A, Garcia-Nieto AV, Ruano J. Clinical and biological principles of cold atmospheric plasma application in skin cancer. Adv Ther 2016; 33 (06) 894-909.
15 Grooters AM, Foli CS. Miscellaneous fungal infections. In: Infectious Diseases of the Dog and Cat. Greene CE. ed. Philadelphia: Saunders; 2006: 647-649.
16 Hsu CC, Chang SS, Lee PC, Chao SC. Cutaneous alternariosis in a renal transplant recipient: a case report and literature review. Asian J Surg 2015; 38: 47-57.
17 Hübner NO, Matthes R, Koban I. et al. Efficacy of chlorhexidine, polihexanide and tissue-tolerable plasma against Pseudomonas aeruginosa biofilms grown on polystyrene and silicone materials. Skin Pharmacol Physiol 2010; 23 (Suppl. 01) 28-34.
18 Kam S-K, Lee W-S, Ou T-Y, Teng S-O, Chen F-L. Delftia acidovorans bacteremia associated with ascending urinary tract infections proved by molecular method. J Exp Clin Med 2012; 4: 180-182.
19 Kawamura I, Yagi T, Hatakeyama K. et al. Recurrent vascular catheter-related bacteremia caused by Delftia acidovorans with different antimicrobial susceptibility profiles. J Infect Chemother 2011; 17: 111-113.
20 Khan S, Sistla S, Dhodapkar R, Parija SC. Fatal Delftia acidovorans infection in an immunocompetent patient with empyema. Asian Pac J Trop Biomed 2012; 2: 923-924.
21 Klampfl TG, Isbary G, Shimizu T. et al. Cold atmospheric air plasma sterilization against spores and other microorganisms of clinical interest. Appl Environ Microbiol 2012; 78: 5077-5082.
22 Koban I, Matthes R, Hübner NO. et al. Treatment of Candida albicans biofilms with low-temperature plasma induced by dielectric barrier discharge and atmospheric pressure plasma jet. New J Phys 2010; 12: 073039.
23 Kogelschatz U. Atmospheric-pressure plasma technology. Plasma Physics and Controlled Fusion 2004; 46: B63.
24 Kramer A, Lademann J, Bender C. et al. Suitability of tissue tolerable plasmas (TTP) for the management of chronic wounds. Clinical Plasma Medicine 2013; 1: 11-18.
25 Lackmann JW, Bandow JE. Inactivation of microbes and macromolecules by atmospheric-pressure plasma jets. Appl Microbiol Biotechnol 2014; 98: 6205-6213.
26 Lademann J, Ulrich C, Patzelt A. et al. Risk assessment of the application of tissue-tolerable plasma on human skin. Clinical Plasma Medicine 2013; 1: 5-10.
27 Lang KJ, Chinzowu T, Cann KJ. Delftia acidovorans as an unusual causative organism in line-related sepsis. Indian J Microbiol 2012; 52: 102-103.
28 Lyke KE, Miller NS, Towne L, Merz WG. A case of cutaneous ulcerative alternariosis: rare association with diabetes mellitus and unusual failure of itraconazole treatment. Clin Infect Dis 2001; 32: 1178-1187.
29 Mahmood S, Taylor KE, Overman TL, McCormick MI. Acute infective endocarditis caused by Delftia acidovorans, a rare pathogen complicating intravenous drug use. J Clin Microbiol 2012; 50: 3799-3800.
30 Matthes R, Koban I, Bender C. et al. Antimicrobial efficacy of an atmospheric pressure plasma jet against biofilms of Pseudomonas aeruginosa and Staphylococcus epidermidis. Plasma Processes and Polymers 2013; 10: 161-166.
31 McKay JS, Cox CL, Foster AP. Cutaneous alternariosis in a cat. J Small Anim Pract 2001; 42: 75-78.
32 Metelmann H-R, Vu TT, Do HT. et al. Scar formation of laser skin lesions after cold atmospheric pressure plasma (CAP) treatment: A clinical long term observation. Clinical Plasma Medicine 2013; 1: 30-35.
33 Miller Jr. WH, Griffin C, Campbell KL. Small Animal Dermatology. St. Louis, Missouri: Elsevier; 2013
34 Morrison VA, Weisdorf DJ. Alternaria: a sinonasal pathogen of immunocompromised hosts. Clin Infect Dis 1993; 16: 265-270.
35 Napp M, Daeschlein G, von Podewils S. et al. In vitro susceptibility of methicillin-resistant and methicillin-susceptible strains of Staphylococcus aureus to two different cold atmospheric plasma sources. Infection 2016; 44: 531-537.
36 Outerbridge CA, Myers SL, Summerbell RC. Phaeohyphomycosis in a cat. Can Vet J 1995; 36: 629-630.
37 Palmeiro BS. Cyclosporine in veterinary dermatology. Vet Clin North Am Small Anim Pract 2013; 43: 153-171.
38 Pastor FJ, Guarro J. Alternaria infections: laboratory diagnosis and relevant clinical features. Clin Microbiol Infect 2008; 14: 734-746.
39 Preissner S, Kastner I, Schutte E. et al. Adjuvant antifungal therapy using tissue tolerable plasma on oral mucosa and removable dentures in oral candidiasis patients: a randomised double-blinded split-mouth pilot study. Mycoses 2016; 59: 467-475.
40 Rickerts V, Khot PD, Myerson D. et al. Comparison of quantitative real time PCR with Ssquencing and ribosomal RNA-FISH for the identification of fungi in formalin fixed, paraffin-embedded tissue specimens. BMC Infectious Diseases 2011; 11: 1-12.
41 Romano C, Vanzi L, Massi D, Difonzo EM. Subcutaneous alternariosis. Mycoses 2005; 48: 408-412.
42 Roosje PJ, de Hoog GS, Koeman JP, Willemse T. Phaeohyphomycosis in a cat caused by Alternaria infectoria E. G. Simmons. Mycoses 1993; 36: 451-454.
43 Schmidt A, Wende K, Bekeschus S, Bundscherer L, Barton A, Ottmüller K, Weltmann K-D, Masur K. Non-thermal plasma treatment is associated with changes in transcriptome of human epithelial skin cells. Free Radic Res 2013; 47: 577-592.
44 Stonecipher KG, Jensen HG, Kastl PR, Faulkner A, Rowsey JJ. Ocular infections associated with Comamonas acidovorans. Am J Ophthalmol 1991; 112: 46-49.
45 Trompeter FJ, Neff WJ, Franken O, Heise M, Neiger M, Liu S, Pietsch GJ, Saveljew AB. Reduction of Bacillus subtilis and Aspergillus niger spores using nonthermal atmospheric gas discharges. IEEE Transactions on Plasma Science 2002; 30: 1416-1423.
46 Vandersee S, Richter H, Lademann J, Beyer M, Kramer A, Knorr F, Lange-Asschenfeldt B. Laser scanning microscopy as a means to assess the augmentation of tissue repair by exposition of wounds to tissue tolerable plasma. Laser Physics Letters 2014; 11: 115701.
47 Vandervoort KG, Brelles-Marino G. Plasma-mediated inactivation of Pseudomonas aeruginosa biofilms grown on borosilicate surfaces under continuous culture system. PLoS One 2014; 9: e108512.
48 Wende K, Barton A, Bekeschus S. et al. Proteomic tools to characterize non-thermal plasma effects in eukaryotic cells. Plasma Medicine 2013; 3: 81-95.
49 Yasuda H, Miura T, Kurita H, Takashima K, Mizuno A. Biological evaluation of DNA damage in bacteriophages inactivated by atmospheric pressure cold plasma. Plasma Processes and Polymers 2010; 7: 301-308.
50 Zimmermann JL, Dumler K, Shimizu T. et al. Effects of cold atmospheric plasmas on adenoviruses in solution. J Phys D: Appl Phys 2011; 44: 505201-505209.