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Localised pyogranulomatous dermatitis due to Mycobacterium abscessus in a cat: A case report
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The Veterinary Journal The Veterinary Journal 179 (2009) 304–306 www.elsevier.com/locate/tvjl
Short Communication
Localised pyogranulomatous dermatitis due to Mycobacterium abscessus in a cat: A case report A. Jassies-van der Lee a,*, D.J. Houwers b, N. Meertens c, A.G.M. van der Zanden d, T. Willemse a,b a
c d
Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 108, 3584 CM, Utrecht, The Netherlands b Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL, Utrecht, The Netherlands Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL, Utrecht, The Netherlands Medical Microbiology and Infection Prevention, Gelre Hospitals, Albert Schweitzerlaan 31, 7334 DZ, Apeldoorn, The Netherlands Accepted 30 August 2007
Abstract A case of pyogranulomatous dermatitis, caused by Mycobacterium abscessus, an unusual opportunistic Mycobacterium spp., is described in a cat. Histopathological examination of the affected skin confirmed the diagnosis and Ziehl-Neelsen staining revealed acid-fast rods. A rapidly growing mycobacterium was found after culture on a Lo¨wenstein–Jensen medium. Real-time polymerase chain reaction for the 16S rDNA (434 bp) sequence and the sequence of the rpoB gene (359 bp) revealed 99% and 100% matches, respectively, with M. abscessus. This is the first report of a feline infection caused by this organism in Europe. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Mycobacterium; M. abscessus; Opportunistic infection; Pyogranuloma; Cats
A 3-year old male, castrated, domestic shorthair cat was referred for investigation of dermal nodules affecting the ventral abdominal skin. One year previously, the cat had been presented to the referring veterinarian with a traumatic skin wound in the same area, which was treated by primary closure (Monocryl, Ethicon) and the animal was given a 1-week course of amoxycillin–clavulanic acid (Synulox, Pfizer; 12.5 mg/kg b.i.d.). Six months after suturing, tiny skin nodules were reported at the same site and 2 months later these had merged into a larger mass. The mass was excised, histopathology indicated pyogranulomatous dermatitis and Ziehl–Neelsen (ZN) staining revealed sparse acid-fast bacilli. Period acid-Schiff (PAS) staining and Gram staining did not reveal other microbial elements. Recurrence was seen 1 week post-surgery. *
Corresponding author. Tel.: +31 302531011; fax: +31 302518126. E-mail address: [email protected] (A. Jassies-van der Lee).
1090-0233/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tvjl.2007.08.026
Ten months after the initial presentation, the animal was referred for a dermatological opinion. The owners reported continued growth of the dermal nodules in the same location. The animal was reported to be otherwise in good health and had no preceding history of other recurrent infections. There was no history of mycobacterial infection or current illness in either the owners or in other cats belonging to the same household. Clinical examination revealed dermal nodules of varying size (diameter 1.5– 5 cm, depth 1 cm) that were firm, non-painful and non-erythematous and had an area of central erosion. Prescapular and axillary lymph nodes were palpably enlarged. A full clinical examination revealed no other abnormalities. The owners elected to not pursue further treatment and the cat was euthanased. Gross necropsy revealed coalescing nodules within the ventral abdominal skin that were centred within the dermis and extended to the epidermis and into subcutaneous tis-
A. Jassies-van der Lee et al. / The Veterinary Journal 179 (2009) 304–306
sues and muscle. Other findings included enlarged sternal, prescapular and axillary lymph nodes as well as a mildly enlarged spleen. Histopathological analysis of the skin lesions revealed coalescing nodules with some concentric fibrosis (pyogranulomas) consisting of many macrophages, neutrophils and multinucleated giant cells surrounding multifocal variably-sized clear spaces (so-called lipocysts). The pyogranulomas were surrounded by perivascular foci of lymphocytes and plasma cells. PAS staining of histopathological sections did not reveal fungal elements, but ZN staining once again demonstrated occasional acid-fast bacilli, especially in the empty central spaces of the pyogranulomas. The lymph nodes and the spleen showed follicular hyperplasia. PAS and ZN stains of histopathological sections from these organs did not reveal any evidence of organisms. The histopathological findings were compatible with cutaneous mycobacteriosis (Gross et al., 2005). Aseptically taken specimens of skin, lymph node and splenic tissue were subjected to standard decontamination and liquefaction (Isenberg, 2004). Polymerase chain reaction (PCR) assays directly on the tissue specimens were negative. Lo¨wenstein–Jensen slants (with and without pyruvate) and liquid Mycobacterium media from the MB Bact system (BioMe´rieux) were inoculated separately with skin, lymph node and splenic tissues. After 5 days of incubation, substantial growth within the MB Bact system inoculated with skin samples was observed. DNA was extracted using QIAamp DNA mini elute kit (Qiagen). Real-time PCR for IS6110 (which is specific for members of the Mycobacterium tuberculosis complex; Savelkoul et al., 2006) was negative, but for 16S rDNA the assay was clearly positive. This amplification product and that of the rpoB genePCR containing the rpoB-hotspot region (Van der Zanden et al., 2003) were subjected to sequence analysis (3100Avant sequencer, Applied Biosystems). Sequences were assembled, edited and analysed with Lasergene software (DNAStar), deposited in GenBank and compared with known 16S rDNA and rpoB sequences using BLAST. The 16S rDNA (434 bp) sequence appeared to have a 99% match with M. massiliense, M. chelonae, M. abscessus, M. fuerth and M. bolletii. The sequence of the rpoB gene (359 bp) showed a 100% match with M. abscessus. No other identification methods were applied. Mycobacterial infections are uncommon in cats (Gross et al., 2005). Atypical infections caused by opportunistic mycobacteria commonly involve dermal and subcutaneous tissues, usually following traumatic skin damage. Opportunistic mycobacteria implicated in the development of cutaneous granulomas in cats include the M. chelonae-abscessus group, the M. fortuitum group, the M. smegmatis group, M. phlei, M. flavescens and M. thermoresistibile (Willemse et al., 1985; Malik et al., 2000; Jang et al., 2002). They are distributed ubiquitously and can be isolated from soil, dirt and water. Atypical mycobacterial infections in cats are seen at any age (range 1.5–13 years), tend to occur in obese individuals
305
and are commonly observed as nodular pyogranulomatous dermatitis with fistules and discharge of watery exudate (Malik et al., 2000). Special stains such as Ziehl–Neelsen are required for histopathological diagnosis, but the number of bacteria present is sometimes extremely low (Gross et al., 2005). In the present case, identification was achieved by real-time PCR using the sequence of the rpoB gene (Van der Zanden et al., 2003). Other molecular diagnostic techniques that are commonly used for mycobacterial identification are spoligotyping or pulsed-field gel electrophoresis (PFGE) (Dytoc et al., 2005; Gori et al., 2005). Previously, M. chelonae subspecies chelonae and M. chelonae subspecies abscessus were considered to belong to the same species. In 1992, M. abscessus was elevated to species status. To date, the M. chelonae–abscessus group contains three species: M. chelonae, M. abscessus and M. immunogenum (Brown-Elliott and Wallace, 2002; Khan Izhar et al., 2005). The only two documented cases of feline cutaneous mycobacteriosis involving the M. chelonae– abscessus group so far were from the USA (Jang and Hirsch, 2002) and these were also not associated with human infection. However, cats are popular companion animals and consequently close contact with humans is common. We therefore underline the potential health risk for humans, especially immune-compromised individuals, particularly as M. abscessus is considered the most pathogenic rapid-growing mycobacterium in humans (Petrini, 2006). In general, M. abscessus is susceptible to clarithromycin, amikacin and cefoxitin (Brown-Elliott and Wallace, 2002; Dytoc et al., 2005). Most feline atypical mycobacterial infections have been successfully managed with surgical resection and treatment with up to 6 months of antimicrobial agents, either alone or as a combination of doxycycline, ciprofloxacin/enrofloxacin or clarithromycin. However, relapses are commonly seen (Malik et al., 2000). To our knowledge, this is the first report of pyogranulomatous dermatitis in a cat associated with a M. abscessus infection in Europe. References Brown-Elliott, B.A., Wallace, R.J., 2002. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clinical and Microbiological Reviews 15, 716–746. Dytoc, M.T., Honish, L., Shandro, C., Ting, P.T., Chui, L., Fiorillo, L., Robinson, J., Fanning, A., Predy, G., Rennie, R.P., 2005. Clinical, microbiological and epidemiological findings of an outbreak of Mycobacterium abscessus hand-and-foot disease. Diagnostic Microbiology and Infectious Disease 53, 39–45. Gori, A., Bandera, A., Marchetti, G., Degli Esposti, A., Catozzi, L., Nardi, G.P., Gazzola, L., Ferrario, G., Van Embden, J.D.A., Van Soolingen, D., Moroni, M., Franzetti, F., 2005. Spoligotyping and Mycobacterium tuberculosis. Emerging Infectious Diseases 8, 1242– 1248. Gross, TL., Ihrke, P.J., Walder, E.J., Affolter, V.K., 2005. Skin diseases of the dog and cat; Clinical and histopathologic diagnosis, second ed. Blackwell Science, Oxford, UK, pp. 283–288.
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A. Jassies-van der Lee et al. / The Veterinary Journal 179 (2009) 304–306
Isenberg, H.D., 2004. Clinical Microbiology Procedures Handbook, second ed. American Society for Microbiology (ASM), Washington, USA, p 7.1.2.1. Jang, S.S., Hirsch, D.C., 2002. Rapidly growing members of the genus Mycobacterium affecting dogs and cats. Journal of the American Animal Hospital Association 38, 217–220. Khan Izhar, U.H., Selvaraju Suresh, B., Yadav Jagjit, S., 2005. Method for rapid identification and differentiation of the species of the Mycobacterium chelonae complex based on 16S-23S rRNA gene internal transcribed spacer PCRr-restriction analysis. Journal of Clinical Microbiology 43, 4466–4472. Malik, R., Wigney, D.I., Dawson, D., Martin, P., Hunt, G.B., Love, D.N., 2000. Infection of the subcutis and skin of cats with rapidly growing mycobacteria: a review of microbiological and clinical findings. Journal of Feline Medicine and Surgery 2, 35–48.
Petrini, B., 2006. Mycobacterium abscessus: an emerging rapid-growing potential pathogen. Acta Pathologica, Microbiologica et Immunologica Scandinavica 114, 319–328. Savelkoul, P.H.M., Catsburg, A., Mulder, S., Oostendorp, L., Schirm, J., Wilke, H., van der Zanden, A.G.M., Noordhoek, G.T., 2006. Detection of Mycobacterium tuberculosis complex with real time PCR: Comparison of different primer-probe sets based on the IS6110 element. Journal of Microbiological Methods 66 (1), 177–180. Van der Zanden, A.G.M., Te Koppele-Vije, E.M., Vijaya Bhanu, N., Van Soolingen, D., Schouls, L.M., 2003. Use of DNA extracts from Ziehl– Neelsen-stained slides for molecular detection of rifampin resistance and spoligotyping of Mycobacterium tuberculosis. Journal of Clinical Microbiology 41, 1101–1108. Willemse, T., Groothuis, D.G., Koeman, J.P., Beyer, E.G., 1985. Mycobacterium thermoresistibile: Extrapulmonary infection in a cat. Journal of Clinical Microbiology 21, 854–856.
The Veterinary Journal The Veterinary Journal 179 (2009) 304–306 www.elsevier.com/locate/tvjl
Short Communication
Localised pyogranulomatous dermatitis due to Mycobacterium abscessus in a cat: A case report A. Jassies-van der Lee a,*, D.J. Houwers b, N. Meertens c, A.G.M. van der Zanden d, T. Willemse a,b a
c d
Department of Clinical Sciences of Companion Animals, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 108, 3584 CM, Utrecht, The Netherlands b Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL, Utrecht, The Netherlands Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL, Utrecht, The Netherlands Medical Microbiology and Infection Prevention, Gelre Hospitals, Albert Schweitzerlaan 31, 7334 DZ, Apeldoorn, The Netherlands Accepted 30 August 2007
Abstract A case of pyogranulomatous dermatitis, caused by Mycobacterium abscessus, an unusual opportunistic Mycobacterium spp., is described in a cat. Histopathological examination of the affected skin confirmed the diagnosis and Ziehl-Neelsen staining revealed acid-fast rods. A rapidly growing mycobacterium was found after culture on a Lo¨wenstein–Jensen medium. Real-time polymerase chain reaction for the 16S rDNA (434 bp) sequence and the sequence of the rpoB gene (359 bp) revealed 99% and 100% matches, respectively, with M. abscessus. This is the first report of a feline infection caused by this organism in Europe. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Mycobacterium; M. abscessus; Opportunistic infection; Pyogranuloma; Cats
A 3-year old male, castrated, domestic shorthair cat was referred for investigation of dermal nodules affecting the ventral abdominal skin. One year previously, the cat had been presented to the referring veterinarian with a traumatic skin wound in the same area, which was treated by primary closure (Monocryl, Ethicon) and the animal was given a 1-week course of amoxycillin–clavulanic acid (Synulox, Pfizer; 12.5 mg/kg b.i.d.). Six months after suturing, tiny skin nodules were reported at the same site and 2 months later these had merged into a larger mass. The mass was excised, histopathology indicated pyogranulomatous dermatitis and Ziehl–Neelsen (ZN) staining revealed sparse acid-fast bacilli. Period acid-Schiff (PAS) staining and Gram staining did not reveal other microbial elements. Recurrence was seen 1 week post-surgery. *
Corresponding author. Tel.: +31 302531011; fax: +31 302518126. E-mail address: [email protected] (A. Jassies-van der Lee).
1090-0233/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tvjl.2007.08.026
Ten months after the initial presentation, the animal was referred for a dermatological opinion. The owners reported continued growth of the dermal nodules in the same location. The animal was reported to be otherwise in good health and had no preceding history of other recurrent infections. There was no history of mycobacterial infection or current illness in either the owners or in other cats belonging to the same household. Clinical examination revealed dermal nodules of varying size (diameter 1.5– 5 cm, depth 1 cm) that were firm, non-painful and non-erythematous and had an area of central erosion. Prescapular and axillary lymph nodes were palpably enlarged. A full clinical examination revealed no other abnormalities. The owners elected to not pursue further treatment and the cat was euthanased. Gross necropsy revealed coalescing nodules within the ventral abdominal skin that were centred within the dermis and extended to the epidermis and into subcutaneous tis-
A. Jassies-van der Lee et al. / The Veterinary Journal 179 (2009) 304–306
sues and muscle. Other findings included enlarged sternal, prescapular and axillary lymph nodes as well as a mildly enlarged spleen. Histopathological analysis of the skin lesions revealed coalescing nodules with some concentric fibrosis (pyogranulomas) consisting of many macrophages, neutrophils and multinucleated giant cells surrounding multifocal variably-sized clear spaces (so-called lipocysts). The pyogranulomas were surrounded by perivascular foci of lymphocytes and plasma cells. PAS staining of histopathological sections did not reveal fungal elements, but ZN staining once again demonstrated occasional acid-fast bacilli, especially in the empty central spaces of the pyogranulomas. The lymph nodes and the spleen showed follicular hyperplasia. PAS and ZN stains of histopathological sections from these organs did not reveal any evidence of organisms. The histopathological findings were compatible with cutaneous mycobacteriosis (Gross et al., 2005). Aseptically taken specimens of skin, lymph node and splenic tissue were subjected to standard decontamination and liquefaction (Isenberg, 2004). Polymerase chain reaction (PCR) assays directly on the tissue specimens were negative. Lo¨wenstein–Jensen slants (with and without pyruvate) and liquid Mycobacterium media from the MB Bact system (BioMe´rieux) were inoculated separately with skin, lymph node and splenic tissues. After 5 days of incubation, substantial growth within the MB Bact system inoculated with skin samples was observed. DNA was extracted using QIAamp DNA mini elute kit (Qiagen). Real-time PCR for IS6110 (which is specific for members of the Mycobacterium tuberculosis complex; Savelkoul et al., 2006) was negative, but for 16S rDNA the assay was clearly positive. This amplification product and that of the rpoB genePCR containing the rpoB-hotspot region (Van der Zanden et al., 2003) were subjected to sequence analysis (3100Avant sequencer, Applied Biosystems). Sequences were assembled, edited and analysed with Lasergene software (DNAStar), deposited in GenBank and compared with known 16S rDNA and rpoB sequences using BLAST. The 16S rDNA (434 bp) sequence appeared to have a 99% match with M. massiliense, M. chelonae, M. abscessus, M. fuerth and M. bolletii. The sequence of the rpoB gene (359 bp) showed a 100% match with M. abscessus. No other identification methods were applied. Mycobacterial infections are uncommon in cats (Gross et al., 2005). Atypical infections caused by opportunistic mycobacteria commonly involve dermal and subcutaneous tissues, usually following traumatic skin damage. Opportunistic mycobacteria implicated in the development of cutaneous granulomas in cats include the M. chelonae-abscessus group, the M. fortuitum group, the M. smegmatis group, M. phlei, M. flavescens and M. thermoresistibile (Willemse et al., 1985; Malik et al., 2000; Jang et al., 2002). They are distributed ubiquitously and can be isolated from soil, dirt and water. Atypical mycobacterial infections in cats are seen at any age (range 1.5–13 years), tend to occur in obese individuals
305
and are commonly observed as nodular pyogranulomatous dermatitis with fistules and discharge of watery exudate (Malik et al., 2000). Special stains such as Ziehl–Neelsen are required for histopathological diagnosis, but the number of bacteria present is sometimes extremely low (Gross et al., 2005). In the present case, identification was achieved by real-time PCR using the sequence of the rpoB gene (Van der Zanden et al., 2003). Other molecular diagnostic techniques that are commonly used for mycobacterial identification are spoligotyping or pulsed-field gel electrophoresis (PFGE) (Dytoc et al., 2005; Gori et al., 2005). Previously, M. chelonae subspecies chelonae and M. chelonae subspecies abscessus were considered to belong to the same species. In 1992, M. abscessus was elevated to species status. To date, the M. chelonae–abscessus group contains three species: M. chelonae, M. abscessus and M. immunogenum (Brown-Elliott and Wallace, 2002; Khan Izhar et al., 2005). The only two documented cases of feline cutaneous mycobacteriosis involving the M. chelonae– abscessus group so far were from the USA (Jang and Hirsch, 2002) and these were also not associated with human infection. However, cats are popular companion animals and consequently close contact with humans is common. We therefore underline the potential health risk for humans, especially immune-compromised individuals, particularly as M. abscessus is considered the most pathogenic rapid-growing mycobacterium in humans (Petrini, 2006). In general, M. abscessus is susceptible to clarithromycin, amikacin and cefoxitin (Brown-Elliott and Wallace, 2002; Dytoc et al., 2005). Most feline atypical mycobacterial infections have been successfully managed with surgical resection and treatment with up to 6 months of antimicrobial agents, either alone or as a combination of doxycycline, ciprofloxacin/enrofloxacin or clarithromycin. However, relapses are commonly seen (Malik et al., 2000). To our knowledge, this is the first report of pyogranulomatous dermatitis in a cat associated with a M. abscessus infection in Europe. References Brown-Elliott, B.A., Wallace, R.J., 2002. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clinical and Microbiological Reviews 15, 716–746. Dytoc, M.T., Honish, L., Shandro, C., Ting, P.T., Chui, L., Fiorillo, L., Robinson, J., Fanning, A., Predy, G., Rennie, R.P., 2005. Clinical, microbiological and epidemiological findings of an outbreak of Mycobacterium abscessus hand-and-foot disease. Diagnostic Microbiology and Infectious Disease 53, 39–45. Gori, A., Bandera, A., Marchetti, G., Degli Esposti, A., Catozzi, L., Nardi, G.P., Gazzola, L., Ferrario, G., Van Embden, J.D.A., Van Soolingen, D., Moroni, M., Franzetti, F., 2005. Spoligotyping and Mycobacterium tuberculosis. Emerging Infectious Diseases 8, 1242– 1248. Gross, TL., Ihrke, P.J., Walder, E.J., Affolter, V.K., 2005. Skin diseases of the dog and cat; Clinical and histopathologic diagnosis, second ed. Blackwell Science, Oxford, UK, pp. 283–288.
306
A. Jassies-van der Lee et al. / The Veterinary Journal 179 (2009) 304–306
Isenberg, H.D., 2004. Clinical Microbiology Procedures Handbook, second ed. American Society for Microbiology (ASM), Washington, USA, p 7.1.2.1. Jang, S.S., Hirsch, D.C., 2002. Rapidly growing members of the genus Mycobacterium affecting dogs and cats. Journal of the American Animal Hospital Association 38, 217–220. Khan Izhar, U.H., Selvaraju Suresh, B., Yadav Jagjit, S., 2005. Method for rapid identification and differentiation of the species of the Mycobacterium chelonae complex based on 16S-23S rRNA gene internal transcribed spacer PCRr-restriction analysis. Journal of Clinical Microbiology 43, 4466–4472. Malik, R., Wigney, D.I., Dawson, D., Martin, P., Hunt, G.B., Love, D.N., 2000. Infection of the subcutis and skin of cats with rapidly growing mycobacteria: a review of microbiological and clinical findings. Journal of Feline Medicine and Surgery 2, 35–48.
Petrini, B., 2006. Mycobacterium abscessus: an emerging rapid-growing potential pathogen. Acta Pathologica, Microbiologica et Immunologica Scandinavica 114, 319–328. Savelkoul, P.H.M., Catsburg, A., Mulder, S., Oostendorp, L., Schirm, J., Wilke, H., van der Zanden, A.G.M., Noordhoek, G.T., 2006. Detection of Mycobacterium tuberculosis complex with real time PCR: Comparison of different primer-probe sets based on the IS6110 element. Journal of Microbiological Methods 66 (1), 177–180. Van der Zanden, A.G.M., Te Koppele-Vije, E.M., Vijaya Bhanu, N., Van Soolingen, D., Schouls, L.M., 2003. Use of DNA extracts from Ziehl– Neelsen-stained slides for molecular detection of rifampin resistance and spoligotyping of Mycobacterium tuberculosis. Journal of Clinical Microbiology 41, 1101–1108. Willemse, T., Groothuis, D.G., Koeman, J.P., Beyer, E.G., 1985. Mycobacterium thermoresistibile: Extrapulmonary infection in a cat. Journal of Clinical Microbiology 21, 854–856.