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The Veterinary Record, March 5, 2005 Pyogranulomatous meningoencephalitis in a goat due to Corynebacterium ulcerans W. E. Morris, F. A. Uzal, A. L. Cipolla PYOGRANULOMAS or cerebral abscesses caused by Staphylococcus aureus, Fusobacterium necrophorum, Arcano- bacterium pyogenes or Corynebacterium species infections have been reported in goats and other animal species (Moriwaki and others 1972, Altman and Bogokovsky 1973, Amand and others 1973, Glass and others 1993, Smith and Sherman 1994). Corynebacterium ulcerans, a microorganism closely related to Corynebacterium pseudotuberculosis, has been isolated from clinical samples from various species (Carter 1995, Radostits and others 2000, Tejedor and others 2000), including human beings (Barret 1986) but, to the authors’ knowledge, there are no reports of infections by this microorganism in goats, nor has it been associated with brain lesions in any other animal species. This short communica- tion describes a pyogranulomatous meningoencephalitis in a goat due to C ulcerans. A six-year-old female Creole goat was submitted to the animal health unit of the National Institute of Agricultural Technology in Bariloche, Patagonia, Argentina. Its clinical signs consisted of circling, vertical nystagmus of the left eye and tilting of the head to the left. The animal was able to drink and eat but it was in poor body condition. Its body tempera- ture was 38·9°C. The goat was anaesthetised using sodium pentobarbitone and then euthanased by intravenous injection of an over- saturated solution of magnesium sulphate, and a full post- mortem examination was carried out. There was pasty, yellowish green, thick pus inside the right acoustic meatus, surrounding the acoustic nerve. A mass, approximately 2·5 cm in diameter, composed of caseous material and surrounded by a thin, fibrous capsule, was observed under the dura mater, infiltrating the cerebellum, cerebellar peduncles, brainstem and occipital cerebral cortex on the right side (Fig 1). This mass extended into the fourth ventricle. No other gross lesions were observed. Impression smears from the brain lesion were stained with Gram stain, and caseous material from the lesion and cere- brospinal fluid were collected asceptically and inoculated on to 7 per cent sheep blood agar and MacConkey’s agar plates. The plates were then incubated at 37°C for 48 hours under aerobic, microaerophilic and anaerobic conditions. Gram- stained smears of the brain lesion demonstrated groups of pleomorphic Gram-positive, non-sporulated rods, often with clubbed ends, occurring singly or in pairs. A pure culture of small, greyish-white, beta-haemolytic colonies grew on the blood agar plates inoculated with caseous material or cere- brospinal fluid and incubated under microaerophilic and aer- obic conditions. Gram-stained smears of these colonies revealed microorganisms morphologically identical to those observed on impression smears of the brain lesion. These colonies were submitted to conventional biochemical tests. The microorganism isolated was nitrate negative, catalase and urease positive and fermented trehalose. Based on these and other conventional biochemical tests, the microorganism was identified as C ulcerans. No growth was observed on MacConkey’s agar or on blood agar plates incubated under anaerobic conditions. The brain was fixed by immersion in 10 per cent buffered formalin for seven days, and haematoxylin and eosin-stained sections were prepared by routine methods from the inter- nal capsule, thalamus, parietal cortex, midbrain at the level of the superior coliculi, cerebellum, cerebellar peduncles, pons and obex. Histological analysis revealed multifocal to coales- cent pyogranulomas in the cerebral cortex, cerebellum, cere- bral peduncles and brainstem. These lesions consisted of a centre of caseous necrosis surrounded by a layer of neu- trophils, macrophages, lymphocytes, plasma cells and multi- nucleated giant cells. A thin capsule of fibrous connective tissue separated the lesions from the surrounding paren- chyma, in which there was mild to moderate haemorrhage and perivascular cuffing of lymphocytes, plasma cells and a few neutrophils. The meninges in the area were severely infil- trated by lymphocytes, plasma cells and macrophages. A diagnosis of chronic active, multifocal to coalescent pyo- granulomatous encephalitis caused by C ulcerans was estab- lished based on pathological and microbiological findings. The microorganism isolated was urease positive, a char- acteristic which is used to distinguish C ulcerans and C pseudotuberculosis (both urease positive) from Coryne- bacterium diphtheriae, which is urease negative (Funke and Bernard 1999). Some strains of C pseudotuberculosis are phenotypically similar to those of C ulcerans, and it has been suggested that carbohydrate fermentation is often an unreli- able method for differentiating between these two species (Sutherland and others 1996). However, it has been shown that fermentation of trehalose reliably differentiates C pseudo- tuberculosis from C ulcerans (Thompson and others 1983, Centicaya and others 2002). In a recent study, 93 strains of C pseudotuberculosis isolated from the lymph nodes of goats and sheep with a caseous lymphadenitis, and which had been identified by a PCR technique using a primer pair specific for the 16S rRNA of C pseudotuberculosis, were subjected to the trehalose test, and all of the strains were negative in this test (Centicaya and others 2002). However, C ulcerans is always positive for trehalose fermentation (Thompson and others Short Communications Veterinary Record (2005) 156, 317-318 W. E. Morris, DVM, MSc, National Institute of Agricultural Technology, Bariloche, Argentina F. A. Uzal, DVM, MSc, PhD, California Animal Health and Food Safety Laboratory System, School of Veterinary Medicine, University of California, Davis, 105 West Central Avenue, San Bernardino, CA 92408, USA A. L. Cipolla, DVM, National Institute of Agricultural Technology, Balcarce, Argentina Correspondence to Dr Uzal FIG 1: Pyogranuloma occupying part of the fourth ventricle of a goat and involving the cerebellum, cerebellar peduncles and pons group.bmj.com on March 28, 2012 - Published by veterinaryrecord.bmj.com Downloaded from

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The Veterinary Record, March 5, 2005

Pyogranulomatousmeningoencephalitis in a goat due toCorynebacteriumulceransW. E. Morris, F. A. Uzal, A. L. Cipolla

PYOGRANULOMAS or cerebral abscesses caused byStaphylococcus aureus, Fusobacterium necrophorum, Arcano-bacterium pyogenes or Corynebacterium species infectionshave been reported in goats and other animal species(Moriwaki and others 1972, Altman and Bogokovsky 1973,Amand and others 1973, Glass and others 1993, Smith andSherman 1994). Corynebacterium ulcerans, a microorganismclosely related to Corynebacterium pseudotuberculosis, hasbeen isolated from clinical samples from various species(Carter 1995, Radostits and others 2000, Tejedor and others2000), including human beings (Barret 1986) but, to theauthors’ knowledge, there are no reports of infections by thismicroorganism in goats, nor has it been associated with brainlesions in any other animal species. This short communica-tion describes a pyogranulomatous meningoencephalitis in agoat due to C ulcerans.

A six-year-old female Creole goat was submitted to theanimal health unit of the National Institute of AgriculturalTechnology in Bariloche, Patagonia, Argentina. Its clinicalsigns consisted of circling, vertical nystagmus of the left eyeand tilting of the head to the left. The animal was able to drinkand eat but it was in poor body condition. Its body tempera-ture was 38·9°C.

The goat was anaesthetised using sodium pentobarbitoneand then euthanased by intravenous injection of an over-saturated solution of magnesium sulphate, and a full post-mortem examination was carried out. There was pasty,yellowish green, thick pus inside the right acoustic meatus,surrounding the acoustic nerve. A mass, approximately 2·5 cmin diameter, composed of caseous material and surroundedby a thin, fibrous capsule, was observed under the dura mater,infiltrating the cerebellum, cerebellar peduncles, brainstemand occipital cerebral cortex on the right side (Fig 1). Thismass extended into the fourth ventricle. No other grosslesions were observed.

Impression smears from the brain lesion were stained withGram stain, and caseous material from the lesion and cere-brospinal fluid were collected asceptically and inoculated onto 7 per cent sheep blood agar and MacConkey’s agar plates.The plates were then incubated at 37°C for 48 hours underaerobic, microaerophilic and anaerobic conditions. Gram-stained smears of the brain lesion demonstrated groups ofpleomorphic Gram-positive, non-sporulated rods, often withclubbed ends, occurring singly or in pairs. A pure culture ofsmall, greyish-white, beta-haemolytic colonies grew on theblood agar plates inoculated with caseous material or cere-brospinal fluid and incubated under microaerophilic and aer-obic conditions. Gram-stained smears of these coloniesrevealed microorganisms morphologically identical to thoseobserved on impression smears of the brain lesion. Thesecolonies were submitted to conventional biochemical tests.The microorganism isolated was nitrate negative, catalase andurease positive and fermented trehalose. Based on these andother conventional biochemical tests, the microorganism wasidentified as C ulcerans. No growth was observed onMacConkey’s agar or on blood agar plates incubated underanaerobic conditions.

The brain was fixed by immersion in 10 per cent bufferedformalin for seven days, and haematoxylin and eosin-stainedsections were prepared by routine methods from the inter-nal capsule, thalamus, parietal cortex, midbrain at the level ofthe superior coliculi, cerebellum, cerebellar peduncles, ponsand obex. Histological analysis revealed multifocal to coales-cent pyogranulomas in the cerebral cortex, cerebellum, cere-bral peduncles and brainstem. These lesions consisted of acentre of caseous necrosis surrounded by a layer of neu-trophils, macrophages, lymphocytes, plasma cells and multi-nucleated giant cells. A thin capsule of fibrous connectivetissue separated the lesions from the surrounding paren-chyma, in which there was mild to moderate haemorrhageand perivascular cuffing of lymphocytes, plasma cells and afew neutrophils. The meninges in the area were severely infil-trated by lymphocytes, plasma cells and macrophages.

A diagnosis of chronic active, multifocal to coalescent pyo-granulomatous encephalitis caused by C ulcerans was estab-lished based on pathological and microbiological findings.

The microorganism isolated was urease positive, a char-acteristic which is used to distinguish C ulcerans and C pseudotuberculosis (both urease positive) from Coryne-bacterium diphtheriae, which is urease negative (Funke andBernard 1999). Some strains of C pseudotuberculosis are phenotypically similar to those of C ulcerans, and it has beensuggested that carbohydrate fermentation is often an unreli-able method for differentiating between these two species(Sutherland and others 1996). However, it has been shownthat fermentation of trehalose reliably differentiates C pseudo-tuberculosis from C ulcerans (Thompson and others 1983,Centicaya and others 2002). In a recent study, 93 strains ofC pseudotuberculosis isolated from the lymph nodes of goatsand sheep with a caseous lymphadenitis, and which had beenidentified by a PCR technique using a primer pair specific forthe 16S rRNA of C pseudotuberculosis, were subjected to thetrehalose test, and all of the strains were negative in this test(Centicaya and others 2002). However, C ulcerans is alwayspositive for trehalose fermentation (Thompson and others

Short Communications

Veterinary Record (2005)156, 317-318

W. E. Morris, DVM, MSc,National Institute ofAgricultural Technology,Bariloche, ArgentinaF. A. Uzal, DVM, MSc, PhD,California Animal Healthand Food SafetyLaboratory System,School of VeterinaryMedicine, University ofCalifornia, Davis,105 West Central Avenue,San Bernardino,CA 92408, USA

A. L. Cipolla, DVM,National Institute ofAgricultural Technology,Balcarce, Argentina

Correspondence to Dr Uzal

FIG 1: Pyogranuloma occupying part of the fourth ventricle ofa goat and involving the cerebellum, cerebellar pedunclesand pons

group.bmj.com on March 28, 2012 - Published by veterinaryrecord.bmj.comDownloaded from

The Veterinary Record, March 5, 2005

1983). Although the differentiation between C ulcerans and C pseudotuberculosis was based on a single biochemical reac-tion, the trehalose test, the present results are in agreementwith previous studies (Centicaya and others 2002) and indi-cate that the microorganism isolated in the present study wasC ulcerans. Trehalose fermentation also differentiates C ulcer-ans from A pyogenes (Thompson and others 1983), anothermicroorganism phenotypically similar to C ulcerans and acommon pathogen of goats (Smith and Sherman 1994).

The presence of pus in the right acoustic meatus of thegoat in the present study suggests that the infection in the cen-tral nervous system originated in the middle ear and thenprogressed to the inner ear, meninges and brain. In many ani-mal species, middle ear infections often progress to the brain,and in some animals, such as lambs and pigs, the infectionoften ascends from the pharynx via the auditory tube to themiddle ear (Wilcock 1992, Summers and others 1995,Radostits and others 2000). In other species, such as dogs andcats, chronic otitis externa is an important predisposing fac-tor for brain infections (Wilcock 1992). In the present study,there was no sign of otitis externa, suggesting that the bacte-ria had reached the middle ear through the auditory tubefrom the pharynx.

Fibrous proliferation in the central nervous system is usu-ally rudimentary unless the inflammatory process is close tothe meningeal surface (Glass and others 1993, Summers andothers 1995). In the present case, the connection of the abscessto the meninges might have been responsible for the fibrouscapsule that was found.

To the authors’ knowledge the present study is the firstreport of an infection by C ulcerans in a goat, as well as thefirst reported case of pyogranulomatous meningoencephali-tis due to the same agent reported in any species. Thismicroorganism is also a human pathogen, and the zoonoticpotential of the infection needs to be emphasised (Kisley andothers 1994).

ACKNOWLEDGEMENTS

The authors thank Ms E. Vidal for excellent technical assis-tance, Mrs S. J. Uzal for reviewing and Mrs S. Fitisemanu fortyping the manuscript.

ReferencesALTMAN, G. & BOGOKOVSKY, B. (1973) Brain abscess due to Coryne-

bacterium haemolyticum. Lancet i, 378-379AMAND, W., ANSLEY, J. & JOHNSON, J. (1973) Brain abscess in a Barbados

sheep. Journal of the American Veterinary Medical Association 163, 562-564BARRET, N. J. (1986) Communicable disease associated with milk and dairy

products in England and Wales: 1983-1984. Journal of Infection 12, 265-272CARTER, G. R. (1995) Corynebacterium. In Diagnostic Procedures in

Veterinary Bacteriology and Mycology. Eds G. R. Carter, J. R. Cole. San Diego,Academic Press. pp 263-270

CENTIKAYA, B., KARAHAN, M., ATIL, E., KALIN, R., DE BAERE, T. & VANEE-CHOUTTE, M. (2002) Identification of Corynebacterium pseudotuberculosisisolates from sheep and goats by PCR. Veterinary Microbiology 88, 75-83

FUNKE, G. & BERNARD, K. A. (1999) Coryneform Gram-positive rods. InManual of Clinical Microbiology. 7th edn. Eds P. R. Murray, E. J. Baron,M. A. Pfaller, F. C. Tenover, R. H. Yolken. Washington DC, American Societyfor Microbiology Press. pp 319-345

GLASS, B., DE LAHUNTA, A. & JACKSON, C. (1993) Brain abscess in a goat.Cornell Veterinarian 83, 275-282

KISLEY, S. R., PRICE, S. & WARD, T. (1994) Corynebacterium ulcerans: a poten-tial cause of diphtheria. Communications on Disease Reproduction of the CDC

Review 5, R63-R64MORIWAKI, M., WATASE, H., FUKUMOTO, M. & HYASHI, S. (1972)

Exophthalmos due to rete mirabile caused by infection with Corynebacteriumpyogenes in cattle. National Institute of Animal Health Quarterly 13, 14-22

RADOSTITS, O. M., GAY, C. C., BLOOD, D. C. & HINCHCLIFF, W. C. (2000)Diseases caused by bacteria. In Veterinary Medicine: a Textbook of theDiseases of Cattle, Sheep, Pigs, Goats and Horses. 9th edn. Sydney, W. B.Saunders. pp 701-752

SMITH, M. C. & SHERMAN, D. M. (1994) Nervous system. In Goat Medicine.Philadelphia, Lea & Febiger. pp 123-178

SUMMERS, B. A., CUMMINGS, J. F. & DE LAHUNTA, A. (1995) Inflamma-tory diseases of the central nervous system. In Veterinary Neuropathology. StLouis, Mosby. pp 95-188

SUTHERLAND, S. S., HART, R. A. & BULLER, N. B. (1996) Genetic differencesbetween nitrate-negative and nitrate-positive Corynebacterium pseudotuber-culosis strains using restriction fragment length polymorphisms. VeterinaryMicrobiology 49, 1-9

TEJEDOR, M. T., MARTIN, J. L., LUPIOLA, P. & GUTIERREZ, C. (2000)Caseous lymphadenitis caused by Corynebacterium ulcerans in a dromedarycamel. Canadian Veterinary Journal 41, 126-127

THOMPSON, S., GATES-DAVIS, D. & YOUNG, D. C. T. (1983) Rapid micro-biochemical identification of Corynebacterium diphteriae and other medicallyimportant Corynebacteria. Journal of Clinical Microbiology 18, 926-929

WILCOCK, B. P. (1992) The eye and ear. In Pathology of Domestic Animals.4th edn. Eds K. V. F. Jubb, P. C. Kennedy, N. Palmer. San Diego, AcademicPress. pp 441-529

Short Communications

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doi: 10.1136/vr.156.10.317 2005 156: 317-318Veterinary Record

 W. E. Morris, F. A. Uzal and A. L. Cipolla 

Corynebacterium ulceransa goat due to Pyogranulomatous meningoencephalitis in

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