Вы находитесь на странице: 1из 5

Peer ­reviewed Case ­report

Cerebral abscesses in a pig: Atypical manifestations of


Streptococcus suis serotype 2-induced ­meningoencephalitis
Selwyn A. Headley, DVM, MSc, PhD; Luiz C. Silva, DVM, MSc, PhD; Werner Okano, DVM, MSc, P
­ hD

Summary purulent meningoencephalitis with vasculi- cerebral abscesses with meningitis. This case
This article describes the findings associ- tis. Biochemical analysis demonstrated that represents an atypical manifestation of strep-
ated with Streptococcus suis serotype 2 in a the intralesional bacterium was a gram-pos- tococcal meningoencephalitis of swine and
2.5-month-old mixed-breed male pig. Clini- itive coccus, with negative reactions to the is, to our knowledge, the first description of
cally, the animal demonstrated torticollis, Voges-Proskauer, catalase, and NaCl assays, S suis serotype 2-induced cerebral abscesses
paddling movement, lateral recumbency, and and produced acid in trehalose and salicin in ­pigs.
convulsions. Gross evaluation of the brain broths. A polymerase chain reaction assay,
Keywords: swine, Streptococcus suis serotype
revealed multiple abscesses, asymmetrically using DNA from bacteria cultured from
2, neuropathology, bacteriology, polymerase
located within the right cerebral hemisphere the brain abscesses, amplified the partial
chain ­reaction
and in contact with the meningeal surface. 459 base-pair fragment of the capsular gene
Histopathological evaluation revealed multi- of S suis serotype 2. The histopathological, Received: December 21, 2011
focal to coalescing cerebral abscesses associ- microbiological, and molecular findings sup- Accepted: April 12, 2012
ated with intralesional bacterial colonies and port a diagnosis of S suis serotype 2-induced

Resumen - Absceso cerebral en un cerdo: la polimerasa, utilizando DNA de cultivo de présentait un torticolis, des mouvements
Manifestaciones atípicas de meningo- bacteria de los abscesos del cerebro, ampli- de pédalage, un décubitus latéral, et des
encefalítis inducida por Streptococcus suis ficó el fragmento parcial de 459 pares de convulsions. Une évaluation macroscopique
serotipo 2 bases del gene capsular del S suis serotipo 2. du cerveau a révélé la présence de nombreux
Los hallazgos moleculares, microbiológicos, abcès, disposés de manière asymétrique
Este artículo describe los hallazgos asociados e histopatológicos sustentan un diagnóstico dans l’hémisphère cérébral droit et en
con Streptococcus suis serotipo 2 en un cerdo de absceso cerebral con meningitis inducido contact avec les méninges. L’examen histo-
macho de raza mixta de 2.5 meses de edad. por S suis serotipo 2. Este caso representa pathologique a permis d’observer des abcès
Clínicamente, el animal mostraba tortícolis, una manifestación atípica de meningoence- multifocaux et coalescents associés à des
movimiento de pataleo, recumbencia lateral, falítis estreptococal de cerdo y es, a nuestro colonies bactériennes intra-lésionnelles ainsi
y convulsiones. La evaluación macroscópica conocimiento, la primera descripción de qu’une méningoencéphalite purulente avec
del cerebro reveló múltiples abscesos, ubica- abscesos cerebrales inducidos por S suis sero- vasculite. Les analyses biochimiques ont
dos asimétricamente dentro del hemisferio tipo 2 en cerdos. démontré que les bactéries intra-lésionnelles
cerebral derecho y en contacto con la super- étaient des coques à gram positif, avec des
ficie de la meninge. La evaluación histopa- réactions négatives pour les tests de Voges-
tológica reveló abscesos multifocales adhe- Résumé - Abcès cérébral chez un porc:
Prauskauer, la présence de catalase, et la
ridos a colonias bacterianas intralesionales y Manifestations atypiques de méningo-
tolérance au NaCl, et produisaient de l’acide
meningoencefalítis purulenta con vasculitis. encéphalite induite par Streptococcus suis
dans des bouillons contenant du tréhalose et
El análisis bioquímico demostró que la bac- sérotype 2
de la salicine. Une réaction d’amplification
teria intralesional era un coco gram-positivo, Le présent article rapporte les trouvailles en chaîne par la polymérase, utilisant l’ADN
con reacciones negativas a las pruebas de associées à une infection par Streptococ- des bactéries obtenues des abcès cérébraux,
Voges-Proskauer, catalasa, y NaCl, y que cus suis sérotype 2 chez un porcelet mâle amplifia le fragment partiel de 459 paires
producía ácido en caldos de trehalosa y sal- âgé de 2.5 mois. Cliniquement, l’animal de bases du gène de la capsule de S suis séro-
icina. Una prueba de reacción en cadena de type 2. Les trouvailles histopathologiques,
microbiologiques, et moléculaires appuient
SAH, WO: Laboratory of Veterinary Pathology, School of Veterinary Medicine, Universidade Norte le diagnostic d’abcès cérébraux et de mén-
do Paraná, Arapongas, Paraná, B
­ razil.
ingite causés par S suis sérotype 2. Ce cas
LCS: Laboratory of Veterinary Microbiology, School of Veterinary Medicine, Universidade Norte do présente une manifestation atypique de
Paraná, Arapongas, Paraná, B
­ razil. méningoencéphalite à streptocoque porcine
Corresponding author: Dr Selwyn A. Headley, Laboratory of Veterinary Pathology, School of Veterinary et est, selon nous, la première fois que des
Medicine, Universidade Norte do Paraná, PR 218 Km 1, Jardim Universitário, Arapongas, PR, Brazil abcès cérébraux associés à S suis sérotype 2
86702-670; Tel: + 55 43 3171-7570; Fax: +55 43 3172–7563; E-mail: h­ eadleysa@gmail.com. sont rapportés chez le porc.
This article is available online at http://www.aasv.org/shap.html.
Headley SA, Silva LC, Okano W. Cerebral abscesses in a pig: Atypical manifestations of Streptococcus suis
­ eningoencephalitis. J Swine Health Prod. 2012;20(4):179–183.
serotype 2-induced m

Journal of Swine Health and Production — Volume 20, Number 4 179


S Case ­description
treptococcus suis is an important gram- submitted for PCR testing at the Veterinary
positive bacterial pathogen of swine Microbiology Diagnostic Laboratory, Uni-
that occurs worldwide and is frequently Clinical h
­ istory versidade Federal de Mato Grosso (UFMS),
associated with encephalitis, meningitis, Three 2.5-month-old mixed-breed pigs (two Cuiabá, MT, Brazil. The PCR protocol used
arthritis, septicemic processes, endocarditis,1-3 males and one female) that were maintained was specific for S suis serotype 218 and con-
bronchopneumonia, polyserositis, rhinitis, on a small subsistence farm located within sisted of the primer pairs (cps2J-s and cps2J)
pericarditis,1,2 and abscesses.2 Although the the city of Arapongas, Paraná, southern that were designed to amplify the 459 base
number of serotypes of S suis has reached Brazil, reportedly demonstrated manifesta- pairs (bp) of the capsular gene (cps) of this
35,4 serotype 2 is the most virulent and most tions of neurological dysfunction, including b­ acterium.17
frequently isolated in diseased animals.5 Epi- paddling, incoordination, and inability to
demiological studies in southern and south- stand. Two of the affected pigs died within 3 Gross fi
­ ndings
eastern Brazil have suggested that infections days after neurological manifestations were A routine necropsy at the Laboratory of
in clinically affected pigs are predominantly observed; the other male pig was submitted Veterinary Pathology-UNOPAR revealed
associated with S suis serotype ­2.6-8 to the Veterinary Teaching Hospital, Univer- lesions close to the right inner ear, restricted
sidade Norte do Paraná (VTH-UNOPAR), primarily to the brain. There was a 3.5-cm
Although pigs are more commonly infected Arapongas, Paraná, Brazil, for evaluation diameter, firm, slightly raised, light-green
by S suis, disease has been infrequently and treatment in late September 2011. On mass centrally located at the right cerebral
diagnosed in ruminants and horses2,3 and arrival, the animal was very thin, but did hemisphere (Figure 1). The meningeal ves-
in cats, dogs, and deer.2 Additionally, S suis not demonstrate clinical manifestations of sels were discretely congested and the cere-
is a zoonotic disease,9,10 with most cases disease during 2 days of observation and was bral sulci were shallow with distended gyri.
of human infections occurring in Europe thus discharged without being subjected to Transverse sections of the formalin-fixed
and Asia.9 Streptococcus suis is frequently therapeutic intervention. However, when brain revealed several abscesses, varying from
isolated in pigs submitted for slaughter with the pig was returned to the farm, similar 0.3 to 0.7 cm in diameter, asymmetrically
manifestations of valvular endocarditis11,12 neurological manifestations were reportedly located throughout the right cerebral hemi-
or meningitis13,14 or with cardiac-associated observed by the owner, who indicated that sphere. The brain stem and cerebellum were
brain lesions.15 Nevertheless, meningitis is these became more intense, progressive, not affected. These multifocal to coalesc-
the most important clinical manifestation of and regular. The pig was readmitted to the ing space-occupying abscesses resulted in
porcine S suis infection.9 However, descrip- VTH-UNOPAR 7 days later in extremis, marked destruction of the white and gray
tions of S suis-induced cerebral abscesses were demonstrating torticollis, paddling move- matter of the right cerebral hemisphere and
not located in major databases. In swine, ment, lateral recumbency, and convulsions. moderate dilation of the contralateral ventri-
abscesses have been frequently associated with The owner requested euthanasia. The dura- cle (Figure 2). The margins of some abscesses
Streptococcus porcinus in what are commonly tion of the period between the reported were externally delimited by the meningeal
known as jowl abscesses, streptococcal lymph- onset of neurological manifestations and surface, and some abscesses were contiguous
adenitis, cervical abscesses,3,10 feeder boils, or necropsy was 21 days. The attending veteri- with the lateral ventricle. Endocarditis and
swine strangles,16 but these are cutaneous or narian indicated that there was no history arthritis were not observed, and no other
subcutaneous lesions affecting lymph nodes of reproductive or respiratory disease in the organs or systems were ­affected.
without involvement of the central nervous herd and that the ration was composed of
s­ ystem. commercially produced corn admixed with Histopathological ­alterations
A tentative diagnosis of S suis is easily household waste. Additionally, it is uncertain Significant histopathological alterations
obtained in diseased pigs and is based on if the pig had been medicated at the farm. were restricted to the cerebrum; no other
characteristic clinical manifestations, the Further, the additional nine weaned pigs, one systems or tissues were affected. Neurologi-
age of the infected animal, and gross pathol- boar, and three sows at the farm did not dem- cal lesions were characterized by multifocal
ogy.5,10 Confirmation of infection in pigs onstrate similar clinical manifestations. Initial to coalescing abscesses that were located
requires bacterial isolation and observation differential diagnoses included streptococcal throughout the cerebrum. Some abscesses
of histopathological alterations in affected meningitis and porcine h ­ erpesvirus. were adjacent to the meningeal surface
tissues.5,9 Routine identification of S suis is A routine necropsy was performed soon after and others were deep within the neuro-
generally based on the following criteria: euthanasia. Selected tissue (lungs, liver, kid- parenchymal tissue or in contact with the
absence of growth in 6.5% NaCl agar, a neg- neys, intestine, and lymph nodes) and brain ependymal layer of the cerebral ventricle
ative reaction to the Voges-Proskauer (VP) (from several areas) were collected, fixed by (Figure 3). Few abscesses contained intra-
test, and acid production in trehalose and immersion in 10% buffered formalin solution, lesional bacterial colonies. In most tissue
salicin broths.1,3 Further characterization and routinely processed for histopathological sections, the abscesses were surrounded by
of S suis has been achieved by polymerase evaluation. Duplicate tissue sections of the varying amounts of connective tissue, this
chain reaction (PCR) assay that targets the brain were stained by the Masson’s trichrome, being more evident in abscesses that were
capsular gene of S suis serotype 2.17,18 This periodic acid-Schiff (PAS), and Grocott contiguous with the meningeal surface. Mas-
report describes the findings associated with methenamine silver (GMS) stain techniques. son’s trichrome stain clearly identified the
S suis serotype 2-induced cerebral abscesses Swabs of brain abscesses and fresh brain sec- extensive connective tissue that encapsulated
in a pig and extends the spectrum of disease tions that included abscesses were collected the abscesses (not shown). In areas of con-
syndromes associated with this ­pathogen. for bacteriological analyses. Aliquots of the tact with the affected meninges, there was
cultured bacteria derived from the brain were marked vasculitis and perivasculitis, with
180 Journal of Swine Health and Production — July and August 2012
accumulations of purulent exudate. Menin-
Figure 1: Gross demonstration of cerebral abscess in the brain of a 2.5-month-old gitis was observed throughout most of the
mixed-breed pig. A large firm mass, 3.5 cm in diameter, is evident in the right affected cerebral hemisphere. Within the
cerebral hemisphere (arrow). Scale in ­centimetres. neurological tissue adjacent to the abscesses
there were varying degrees of vasculitis,
liquefaction necrosis, vascular proliferation,
astrocytosis, neuronal necrosis and degenera-
tion, and tissue edema. Special stains (GMS
and PAS) demonstrated no mycotic ­agents.

Bacteriological ­characteristics
Streptococcus suis was identified by biochemi-
cal evaluation, as described,1,3 from the
swabs and brain sections. The bacterium was
a gram-positive coccus that produced alpha
hemolysis on sheep blood agar, reacted nega-
tively to the V-P and NaCl assays, and pro-
duced acid in trehalose and salicin broths.
Other biochemical characteristics included
positive reactions with esculin hydrolase,
arginine hydrolase, maltose, glucose, inulin,
and lactose, but negative reactivity to sorbi-
tol and ­catalase.

Molecular ­characterization
The desired partial 459 bp fragment of the
capsular gene of S suis serotype 2 was ampli-
Figure 2: Formalin-fixed section of the brain of a 2.5-month-old mixed-breed pig. fied from the cultured bacteria submitted for
Within the right cerebral hemisphere, there are several inspissated green abscesses PCR assay to the Veterinary Microbiology
(arrows) of varying sizes (0.3 to 0.7 cm in diameter). Observe that some abscesses Diagnostic Laboratory, ­UFMS.
are externally located at the meningeal surface while others are in contact with
the lateral ventricle. Note also that the left lateral ventricle (star) is dilated. Scale in Discussion
c­ entimetres. The clinical signs observed in this case have
been described in porcine streptococcal-
induced meningitis.10,19 The pathological
findings are manifestations of cerebral
abscesses, while the bacteriological char-
acteristics of the pathogen are consistent
with those attributed to S suis.1,3 Further,
PCR assay using DNA derived from the
cultured bacteria amplified the 459 bp frag-
ment of the capsular gene of S suis serotype
2; similar results have been described.17,18
Therefore, the absence of other infectious
agents, as demonstrated by histochemical
staining (PAS and GMS), suggests that S
suis serotype 2 participated in the etiopatho-
genesis of the cerebral abscesses observed
in this animal. To our knowledge, this case
represents the first description of S suis-
induced cerebral abscesses in swine without
pathological manifestations of systemic
disease. Microabscesses of the brain have
been described in slaughtered pigs with extra-
neural demonstration of S suis infection.15
Abscesses in pigs are more frequently associ-
ated with S porcinus in the formation of jowl
abscesses,3,10,16 during which multiple periph-
eral lymph nodes are affected. Abscesses were
Journal of Swine Health and Production — Volume 20, Number 4 181
cerebral hemisphere, resulting in multiple
Figure 3: Histological section of the cerebrum of a 2.5-month-old mixed-breed abscesses (chronic space-occupying lesions).
pig. Intracerebral abscesses (arrows) are poorly surrounded by connective tissue Although extension of bacterial infection
(hematoxylin-eosin, original magnification ×
­ 40). via the dura is uncommon, this results in
localization of the abscess at the meninges,21
as occurred in this case. The involvement
of the ependymal layer of the cerebral ven-
tricle with the abscesses in this pig and of
meningitis in pigs experimentally infected19
further demonstrates the progressive nature
of S suis-induced meningoencephalitis.
Therefore, we believe that these lesions
should be considered atypical manifesta-
tions of S suis serotype 2 infection, which
progressed from acute purulent meningitis
to cerebral abscesses. The thickened fibrotic
capsule of the abscesses closest to the menin-
ges was additional evidence that the lesions
were stepwise progressions, since fibrous
encapsulation of abscesses within the brain
is rudimentary unless the abscess is close to
the meningeal surface, which is a source of
collagenous tissue.21,22 This reflects the inca-
pacity of the neurological parenchyma to
synthesize adequate amounts of connective
not observed within the lymph nodes of this a complete bacteriological evaluation was tissue, as was observed in abscesses located
pig. Additionally, purulent streptococcal not performed (ie, bacteriological evalua- deep within the brain. It must be high-
meningitis or meningoencephalitis10,20 is tion of samples from different organs), it lighted that this case is unusual, since the
more frequently attributed to the neuro- is likely that the animal had recuperated pig was not treated at the veterinary hospital
logical manifestations observed in this pig. from an extraneurological manifestation due to the absence of neurological manifes-
Therefore, we propose that these lesions be of purulent infection, since the onset of tations while the animal was observed for
considered atypical manifestations of strep- disease was observed at least 21 days prior to 2 days, and it is uncertain what therapeutic
tococcal ­meningoencephalitis. necropsy. Hence, it is reasonable to assume measures were administered at the ­farm.
that the animal was bacteremic before being
In this case, there was histological manifesta- Although cerebral lesions are frequent
euthanized, with hematogenous dissemina-
tion of extensive purulent meningoencepha- sequelae of either streptococcal endocar-
tion to the brain terminating in bacterial
litis and well-encapsulated cerebral abscesses. ditis15 or arthritis,14 these conditions were
sequestration at the meninges or neurologi-
Meningitis, meningoencephalitis, or both not observed in this pig. Recently, cerebral
cal tissue21,22 and progressing to chronic
are common neurological manifestations microabscesses and granulomatous encepha-
abscess formation. The extensive nature of
of S suis.10,15,20 Meningitis with purulent litis were described in a study of slaughtered
the meningitis associated with the close
vasculitis with extension of disease into the pigs with endocarditis-associated brain
proximity to the right ear might suggest
choroid plexus and spinal cord has been lesions.15 These histological alterations were
extension from a transient infection of otitis
described in pigs experimentally infected not observed in this pig. Further, the distribu-
interna,22 but corresponding characteristic
with S suis.19 Although the pathogenesis of tion of brain lesions associated with left-side
clinical manifestations were not related and
S suis meningitis has not been completely valvular endocarditis in pigs is focal and
typical gross lesions were not observed when
elucidated, it has been proposed that the disseminated.15 The lesions of this pig were
the brain was being removed. Additionally,
bacterium can gain entry into the brain by extensive, space-occupying, and asymmetric.
initial bacterial colonization within the nasal
destruction of the blood-brain-barrier.5,10 Consequently, the morphology and distribu-
mucosa,5 with transient rhinitis and sub-
Further, the actions of the suilysin protein19 tion of the brain lesions observed in this case
sequent dissemination to the brain via the
and other virulence factors5 are key elements are different from those described in slaugh-
cribriform plate,22 cannot be discarded as a
to understand the mechanism of streptococ- tered pigs with brain-associated e­ ndocarditis.
possible source of contamination. Therefore,
cal ­meningoencephalitis.
a resolved extraneural lesion cannot be com- Epidemiological studies performed in the
The method of brain involvement in this pletely excluded as the source of contami- geographical location of this farm have
case remains obscure, but active vascular nation for the brain, since forms of direct demonstrated that S suis serotype 2 is the
dissemination from extraneural organs was extension to the brain were not ­observed. most predominate serotype in clinically
not considered the source of infection, since affected pigs.6-8 These data agree with the
Nevertheless, the brain lesions of this pig
pathological alterations suggestive of initial atypical finding of asymmetrical cerebral
probably initiated at the meninges (acute
bacterial lesions were not observed in any abscesses induced by S suis serotype 2 in this
meningitis) and progressed into the right
tissue or system examined. Nevertheless, as
182 Journal of Swine Health and Production — July and August 2012
pig. Furthermore, S suis serotype 2 is most 3. Songer JG, Post KW. Veterinary Microbiology: 14. Vasconcelos D, Middleton DM, Chirino-Trejo JM.
frequently associated with diseases of pigs Bacterial and Fungal Agents of Animal Disease. Saint Lesions caused by natural infection with Streptococ-
Louis, Missouri: Elsevier/Saunders. ­2005:43–53. cus suis type 9 in weaned pigs. J Vet Diagn Invest.
­ orldwide.5
w 4. Higgins R, Gottschalk M, Boudreau M, Lebrun A, ­1994;6:335–341.
Henrichsen J. Description of six new capsular types 15. Karstrup CC, Jensen HE, Aalbaek B, Leifsson PS,
Implications (29–34) of Streptococcus suis. J Vet Diagn Invest.
­1995;7:405–406.
Boye M, Agerholm JS. Endocarditis-associated
brain lesions in slaughtered pigs. J Comp Path.
• Cerebral abscesses represent an unusual ­2011;144:289–295.
5. Gottschalk M, Segura M. The pathogenesis of
manifestation of streptococcal menin- the meningitis caused by Streptococcus suis: the unre- 16. Katsumi M, Kataoka Y, Takahashi T, Kikuchi N,
goencephalitis of ­swine. solved questions. Vet Microbiol. ­2000;76:259–272. Hiramune T. Biochemical and serological examina-
• Diagnosis of cerebral abscesses should 6. Pagnani KJR, Castro AFP, Gottschalk M, tion of ß-hemolytic streptococci isolated from
Silveira WD, Nakazato G. Serotyping of Streptococ- slaughtered pigs. J Vet Med Sci. 1­ 998;60:129–131.
be based on characteristic gross and
cus suis strains isolated from pigs in the States of São 17. Marois C, Bougeard S, Gottschalk M,
histopathological features and bacterio- Paulo, Minas Gerais and Paraná, Brazil. Pesquisa Kobisch M. Multiplex PCR assay for detection of
logical ­culture. Veterinária Brasileira. ­2002;22:1–5. Streptococcus suis species and serotypes 2 and 1/2
• PCR targeting the capsular gene of 7. Martinez G, Castro AFP, Pagnani KJR, Naka- in tonsils of live and dead pigs. J Clin Microbiol.
zato G, Silveira WD, Gottschalk M. Clonal distribu- ­2004;42:3169–3175.
S suis serotype 2 is an adequate diagnos-
tion of an atypical MRP, EF, and suilysin phenotype 18. De Faria ACS, da Silva MC, Oliveira Filho JX,
tic method to further characterize this of virulent Streptococcus suis serotype 2 strains in de Oliveira JT, de Paula DAJ, Chitarra CS,
­pathogen. Brazil. Can J Vet Res. ­2003;67:52–55. Nakazato L, Dutra V. Prevalence of Streptococcus suis
8. Del’Arco AE, Santos JL, Bevilacqua PD, Faria JE, type 2 using the polimerase chain reaction in slaugh-
Acknowledgements Guimarães WV. Swine infection by Streptococcus tered pigs in the State of Mato Grosso, Brazil [in
This study was partially financed by the Pró- suis: a retrospective study. Arquivo Brasileiro de Portuguese]. Ciência Rural. 2­ 010;40:130–134.
Reitoria de Pesquisa e Pós-Graduação, Uni- Medicina Veterinária e Zootecnia. ­2008;60:878–883. 19. Zheng P, Zhao YX, Zhang AD, Kang C,
*9. Gottschalk M. Porcine Streptococcus suis strains Chen HC, Jin ML. Pathologic analysis of the
versidade Norte do Paraná. The authors are brain from Streptococcus suis type 2 experimentally
as potential sources of infections in humans: an
grateful to Dr Geraldo Guerino Neto for the underdiagnosed problem in North America. J Swine infected pigs. Vet Pathol. ­2009;46:531–535.
submission of this case for routine necropsy. Heath Prod. ­2004;12:197–199. 20. Reams RY, Glickman LT, Harrington DD,
We thank Dr Valéria Dutra, Universidade 10. Higgins JM, Gottschalk M. Streptococcal Thacker HL, Bowersock TL. Streptococcus suis infec-
diseases. In: Straw BE, Zimmerman JJ, D’Allaire S, tion in swine: a retrospective study of 256 cases.
Federal de Mato Grosso, Cuiabá, MT, Bra- Part II. Clinical signs, gross and microscopic lesions
Taylor DJ, eds. Diseases of Swine. 9th ed. Ames, Iowa:
zil, for performing the molecular techniques Blackwell Publishing; 2­ 006:769–783. and coexisting microorganisms. J Vet Diagn Invest.
used during this study. Dr S. A. Headley ­1994;6:326–334.
11. Sanford SE. Gross and histopathological findings
is a recipient of the National Council for in unusual lesions caused by Streptococcus suis in pigs. 21. Summers BA, Cummings JF, de Lahunta A.
I. Cardiac lesions. Can J Vet Res. ­1987;51:481–485. Veterinary Neuropathology. Saint Louis, Missouri:
Scientific and Technological Development Mosby. ­1995:156–159.
(CNPq; Brazil) ­fellowship. 12. Jensen HE, Gyllensten J, Hofman C, Leifsson PS,
Agerholm JS, Boye M, Bent A. Histologic and bac- 22. Zachary JF. Nervous system. In: Zachary JF.
teriologic findings in valvular endocarditis of slaugh- McGavin MD, eds. Pathologic Basis of Veterinary
Disease. 5th ed. Saint Louis, Missouri: Elsevier/
References ter-age pigs. J Vet Diagn Invest. 2010;22:921–927.
Mosby. ­2012:771–870.
1. Higgins JM, Gottschalk M. An update on 13. Sanford SE. Gross and histopathological find-
Streptococcus suis identification. J Vet Diagn Invest. ings in unusual lesions caused by Streptococcus suis * Non-referred reference.
­1990;2:249–252. in pigs. II. Central nervous system lesions. Can J Vet
2. Staats JJ, Feder I, Okwumabua O, Chengappa MM. Res. ­1987;51:486–489.
Streptococcus suis: past and present. Vet Res Commun.
­1997;21:381–407.

Journal of Swine Health and Production — Volume 20, Number 4 183

Вам также может понравиться