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Case Reports |
Correspondence: 1Corresponding Author: Christophe Hugnet, Clinique Vétérinaire des Lavandes, Quartier Boulagne, 26160 La Bégude de Mazenc, France. enzovet{at}orange.fr
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Key Words: Discospondylitis • dogs • osteomyelitis • polymerase chain reaction • Scedosporium apiospermum
Scedosporium apiospermum, 1 of 2 anamorphs of Pseudallescheria boydii, is a eutrophic filamentous fungus commonly isolated from soil, vegetation, polluted water, and animal feces in temperate climates.6,16 It is now recognized as an emerging agent of severe fungal infections in immunosuppressed human patients. In humans, S. apiospermum has been classically implicated in subcutaneous infections and in asymptomatic pulmonary colonization, whereas systemic infections are more frequently observed in patients with an impaired immune system.8 Few reports of scedosporiosis have been reported in animals, most of which are of traumatic origin. Scedosporium apiospermum infections in dogs have been associated with nasal infection, mycetoma, or keratomycosis.4,15
A 6-year-old, 30-kg, female German Shepherd Dog was presented with a rear limb motor disorder. This dog lived both indoors and outdoors in a leishmaniasis enzootic area in the south of France. Deworming and vaccination had been conducted on a regular basis. Four weeks before presentation, the dog had an acute onset of fever, which resolved after a 10-day administration of enrofloxacina (5 mg/kg, orally, once a day). However, the fever recurred after treatment was discontinued. Simultaneously, an insidious onset of a posterior motor disorder was observed, which evolved from paresia to paralysis 3 days before referral. The intravenous corticosteroid treatment by the referring veterinarian resulted in slight amelioration of this neurological disorder.
At presentation, body temperature was normal (38.4°C), mucosal surfaces appeared pink, and cardiac and respiratory examinations were unremarkable. There was a marked paravertebral muscular atrophy. The rear limbs were paretic with a severe proprioceptive deficit involving both rear limbs. Neurological examination showed increased patellar, cranial tibial, and femoral reflexes. The urinary bladder was full and could not be mechanically emptied. Palpation of the spine evoked severe pain at the thoracolumbar and lumbosacral junctions. The panniculus muscular reflex was absent posterior to the thoracolumbar junction. Hip manipulation was difficult, and creaking sounds were heard.
Routine hematology indicated leukocytosis (16,050 cells/µl; reference [ref.] interval: 5,000–15,000 cells/µl) with mature neutrophilia (11,765 cells/µl; ref. interval: 3,000–10,500 cells/µl). The other hematologic variables were within reference intervals. Serum total alkaline phosphatase activity, alanine aminotransferase activity, urea concentration, and creatine concentration were also within reference intervals. Biochemical abnormalities included hyperproteinemia (91 g/l; ref. interval: 52–82 g/l) with an albumin/globulin ratio <0.7 (ref. interval: 0.92–1.30). Serum protein electrophoresis revealed hyperproteinemia with normoalbuminemia (34.8 g/l; ref. interval: 22–35 g/l), normoalphaglobulinemia (alpha1, 2.6 g/l, ref. interval: 5–8 g/l; alpha2, 7.1 g/l, ref. interval: 5–10 g/l), hyperbetaglobulinemia (beta1, 6.2 g/l, ref. interval: 5–11 g/l; beta2, 13.0 g/l; ref. interval: 3–7 g/l), and hypergammaglobulinemia (27.3 g/l; ref. interval: 5–18 g/l). The serum protein electrophoretic pattern indicated a polyclonal gammopathy, consistent with a general antibody response associated with infection. Urinalysis was performed, and abnormalities were not found. Serological testing for Leishmania infantum (in-house immunochromatographic test on membrane)b was positive. Cytological examination of bone marrow smears revealed amastigotes and phagocytized erythroblasts within macrophages, megakaryocytic dysplasia, and neutrophilic hyperplasia. These results were consistent with active leishmaniasis.
Spinal survey radiographs disclosed narrowing of the vertebral canal at the lumbosacral junction (cauda equina syndrome) as well as moderate to marked bilateral hip arthrosis. In addition, a large area of osteolysis and osteoproliferation involved the T13 and L1 vertebrae (Fig. 1). These vertebral lesions were consistent with osteomyelitis and discospondylitis; however, a bone tumor could not be excluded. Because of the poor clinical prognosis and the painful nature of the osseous lesions, the dog was euthanized at the owners' request.
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Reports of scedosporiosis in animals are infrequent. To date, S. apiospermum infections in dogs have been associated with nasal infection, mycetoma, or keratomycosis.1,2,4,15 Only 2 cases of Scedosporium inflatum osteomyelitis have been described in veterinary medicine, 1 in an adult beagle dog involving the humerus14 and another in a horse with arthritis and osteomyelitis of the metacarpophalangeal joint.17
In humans, the clinical presentation of scedosporiosis is largely dependent on the fungal strain, portal of entry, and immune status of the patient.3,10 Three clinical syndromes can be distinguished: 1) localized disease after trauma, such as subcutaneous mycetoma, arthritis, osteomyelitis, endophthalmitis, or onychomycosis; 2) large asymptomatic or symptomatic colonization of cavities, mainly pulmonary cases, but also sinusitis or otitis; and 3) invasive systemic diseases such as pneumonia, endocarditis, or central nervous system disorders.10 Classically, S. apiospermum has been implicated in subcutaneous infections and asymptomatic pulmonary colonization. Systemic infections are more frequently observed in patients with an impaired immune system or in victims of near drowning10; however, infections also have been documented in immunocompetent patients.8 Vertebral osteomyelitis associated with S. apiospermum is infrequent in humans, with less than 10 cases reported in the medical literature.10 Progressive spinal pain is the most common presentation in human patients. Systemic fungal infections in humans are usually related to direct extension of pulmonary infections, hematogenous spread, or direct inoculation of the organism. In most of these reports, dissemination of mycotic infection often involves the central nervous system.
Most cases of S. apiospermum infection in dogs and horses are of traumatic origin.7,12,14,15 In the dog of the present report, the portal of entry of S. apiospermum was unknown; the owner did not mention the presence of wounds or nasal discharge before presentation of the dog for illness. The relationship between scedosporiosis and leishmaniasis in this dog is also unclear. However, phagocytic capabilities of macrophages from Leishmania-infected animal models (mainly mouse and hamsters) are altered via disturbed cytokine production.9 In northeastern Spain (an endemic area of leishmaniasis), a 2007 report demonstrated that chronic infection with leishmaniasis may predispose dogs to secondary vector-borne infections (Tabar L, Francino O, Altet L, et al.: 2007, PCR-based of coinfection with multiple vector-borne pathogens related to leishmania infantum infection in dogs from north eastern Spain [Abstract], p. 203. Seventeenth European Society of Veterinary Internal Medicine-Companion Animals Congress, September 13–15, Budapest, Hungary). Thus, chronic leishmaniasis may explain the unusual localization of S. apiospermum infection in this dog to the thoracolumbar vertebrae. Another explanation may be the predisposition of German Shepherd Dogs to develop fungal infection (especially disseminated aspergillosis) and discospondylitis. There also may be a relationship in this breed with defective immunoglobulin A production and altered mucosal immunity, which may allow initial penetration of the fungus.5
Scedosporium infections are difficult to diagnose clinically, and histological lesions are similar to those due to Aspergillus sp. and other hyphomycetes. Routine special stains, such as PAS, do not discriminate S. apiospermum from other related fungi. Therefore, mycological culture is recommended for specific identification. When culture has not been performed or only formalin-fixed tissues are available for study, as in the current case, PCR analysis and genetic sequencing of the amplicons may be used to specifically identify the fungus from infected tissues. For example, a previous study distinguished S. apiospermum from A. fumigatus by an in situ hybridization technique using rDNA probes.11
Scedosporiosis is often resistant to treatment with traditional antifungal drugs such as amphotericin B, miconazole, or itraconazole. When possible, surgical excision of infected tissue is the optimal form of treatment. In one human patient, successful treatment of a chronic, fungal, vertebral infection was achieved with a combination of surgery (abscess debridement, surgical drain placement, ostectomy, osseous autograft implantation, and vertebral stabilization), drug administration ( intravenous and oral voriconazole administration for at least 1 year), and bed rest.8,13 In dogs, systemic scedosporiosis is usually fatal; however, localized infection such as that involving the nasal cavities may be cured with appropriate treatment. One previous study described treatment of nasal fungal infection by endoscopic removal of the fungal mass, which resulted in clinical improvement within 2 weeks.4 In another case report, a nasal granuloma was treated by oral administration of ketoconazole (10 mg/kg of body weight, twice a day). Medication decreased the nasal discharge after 1 month of treatment and was continued until the dog died in a car accident 7 months later.2
To the authors' knowledge, this is the first description of chronic vertebral osteomyelitis and discospondylitis due to S. apiospermum infection in the dog. Moreover, S. apiospermum infection has never been reported in a dog from France. The present case report documents that S. apiospermum may cause vertebral osteomyelitis and discospondylitis in dogs. Furthermore, the clinical presentation and histological findings of S. apiospermum infection may be similar to those of A. fumigatus infection. Specific identification of S. apiospermum, A. fumigatus, and other hyphomycetes is best accomplished by techniques such as mycological culture, PCR analysis, or immunostaining.
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a Baytril® Taste TabsTM Antibacterial Tablets, Bayer AG, Leverkusen, Germany.
b Speed® LEISH, Virbac France SAS, Carros cedex, France.
c DNeasy® Tissue Kit, Qiagen SA, Courtaboeuf cedex, France.
d Applied Biosystems, Courtaboeuf cedex, France.
e ABI PRISMTM, Applied Biosystems, Courtaboeuf cedex, France.
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