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DOI: 10.1177/030098589002700508 1990 27: 354Vet Pathol

B. C. Barr, M. L. Anderson, P. C. Blanchard, B. M. Daft, H. Kinde and P. A. ConradBovine Fetal Encephalitis and Myocarditis Associated with Protozoal Infections

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Vet Pathol 27:354-361 (1990)

Bovine Fetal Encephalitis and Myocarditis Associated with Protozoal Infections

B. C. BARR, M. L. ANDERSON, P. C. BLANCHARD, B. M. DAFT, H. KINDE, AND P. A. CONRAD

California Veterinary Diagnostic Laboratory System and Department of Veterinary Microbiology and Immunology,

University of California, School of Veterinary Medicine, Davis, CA

Abstract. Bovine fetuses submitted to the California Veterinary Diagnostic Laboratory System were eval- uated during a 2-year period (1987 to 1989) for the presence of multifocal necrotizing nonsuppurative encephalitis, nonsuppurative myocarditis, or tissue protozoa. Eighty-two of 445 (1 8%) fetuses submitted met these histologic criteria. Fetuses were from 54 dairy and two beef herds located throughout the state. In 17 fetuses (2 1 Yo) protozoa were found in fetal tissues. Protozoa were found in brain parenchyma of ten fetuses (1 2%), in endothelial cells in four fetuses (5%), in cardiac myofibers in one fetus (lYo), and were associated with endothelial cells in two fetuses (2%). In most fetuses there were no significant gross pathologic findings other than autolysis. While aborted fetuses were from 3 to 9 months gestation, the majority were between 5 and 7 months gestation. They were submitted year round, but more were seen in the fall and winter months. Additional salient histologic features included portal nonsuppurative hepatitis, focal hepatic inflammation and necrosis, and focal nonsuppurative myositis. Nonsuppurative inflammation was also found in decreasing frequency, in the adrenal medulla, kidney, mesentery or abdominal fat, placenta, and lung. In two fetuses (Nos. 1 and 2), the location and morphology of the protozoa were compatible with Sarcocystis spp. The identity of protozoa in the remaining 15 fetuses is unknown. The histopathologic changes in these 82 fetuses and the presence of protozoa in 2 1 Yo of the fetuses suggest these abortions are due to fetal protozoal infections.

Key words: Bovine; encephalitis; fetus; myocarditis; protozoa.

Numerous sporadic cases of bovine protozoal abortion or congenital disease are reported in the litera- t ~ r e . ~ - l 1~15~17-19,24-26,29 Reports of multiple bovine abortions due to protozoal fetal infections, however, are i n f r e q ~ e n t . ~ ~ , ~ ~ Sarcocystis species have been identified or presumed to be the causative agent in a large number of these Toxoplasmosis is a well- documented cause of abortion in sheep and g o a t ~ . ~ , ~ , ~ ~ - l 4 9 l 6 In cattle, however, reports of confirmed abortions due to Toxoplasma gondii are infrequent, and the sig- nificance of this protozoan as a cause of abortion in cattle has been q~estioned.~ Recent evidence has sug- gested that a new protozoal organism, Neospora caninum, is also capable of producing fetal infection and abortion in the bovine.10J1,29,32

Histopathologic changes associated with fetal protozoal infections share unique characteristics that are often useful in making presumptive diagnoses of protozoal infections. For example, Toxoplasrna gondii can cause inflammation in any tissue, but the most frequent or striking inflammatory changes are found in the fetal placenta, brain, and striated muscle. L , 4 ~ 1 2 ~ L 3 ~ 1 6 In particular, multifocal nonsuppurative encephalitis, with focal necrosis and gliosis are well-documented changes

seen in abortions of sheep due to T. gondii,8J6 and similar changes have been found with Sarcocystis and Neospora infections in the bovine

Pathologists at the California Veterinary Diagnostic Laboratory System have recognized a significant number of bovine abortion cases with a similar pattern of encephalitis, accompanied by a nonsuppurative myocarditis. The purpose of this study was 1) to identify and review all bovine fetuses with these histopathologic changes received by the laboratory during a 2-year period; and 2) to determine if there is an association between these changes and protozoal infections.

Materials and Methods

From June 1, 1987 to May 3 1, 1989, a total of 445 bovine fetuses were submitted to the California Veterinary Diag- nostic Laboratory System, located at Davis, Petaluma (now closed), Tulare and San Bernardino. All fetuses with a diagnosis of encephalitis, myocarditis, or presumptive protozoal infection were collected. One pathologist re-examined all tissue sections from these fetuses by light microscopy. The criteria established for selecting a case in this particular study group were 1) the presence of encephalitis with multifocal necrosis or focal vascular nonsuppurative infiltrates and a nonsuppurative myocarditis, or 2) the identification of pro-

354

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Bovine Fetal Encephalitis and Myocarditis 355

tozoa in fetal tissues. Cases with any other etiologic diagnosis were omitted from the study. The presence of protozoa and any significant inflammatory changes were recorded from each case. The date of submission and the location of the cases in this selected group were recorded, and the clinical histories were reviewed. Estimates of the gestational age of fetuses were determined by one of three methods: crown- rump length,* breeding dates, or estimates made by veteri- narians. Estimates of gestational age based on crown-rump length were as follows: 13-2 1 cm = 3 months; 22-3 1 cm = 4 months; 32-43 cm = 5 months; 44-57 cm = 6 months; 58-67 cm = 7 months; 68-85 cm = 8 months; and greater than 86 cm = 9 months.

Abomasal contents, liver, and lung were cultured on blood agar, and MacConkeys agar at 37 C in 5-10/o CO, for a minimum of 48 to 72 hours. Abomasal contents and liver or lung were cultured on media selective for Campylobacter containing polymyxin B sulfate, trimethoprim, and van- comycin, at 37 C in 5% oxygen, 10% CO,, and 85% nitrogen for 5 to 7 days. Abomasal contents and lung were cultured for Brucella abortus on selective agar for 7 to 10 days33 with and without crystal violet, or by incubation on blood agar for 7 to 10 days. Darkfield examination of abomasal contents, Gram stains of abomasal, liver, and lung impression smears were performed on several cases. Direct fluorescent antibody tests (National Veterinary Services Laboratories, Ames, IA) for Leptospira spp. were run on kidney impression smears in most of the cases.

Total immunoglobulin G levels and titers to infectious bovine rhinotracheitis (IBR) virus and bovine virus diarrhea (BVD) virus were determined by serum neutralization and titers to Leptospira spp. (6 serovars) by microagglutination. In many cases, fetal titers were determined to Parainfluenza 3 virus by hemagglutination, bluetongue virus by agar gel immunodiffusion, and B. abortus by buffered acidified plate antigen. Titers to T. gondii were determined either by latex agglutination or by modified direct agglutination3 (Toxo- screen DA, bioMerieux, Charbonnieres-les-Bains Cedex, France) on blood or fetal fluids from a total of 44 fetuses. Sera from cows were checked routinely for titers to IBR, BVD, Leptospira spp. (6 serovars), and B. abortus. In two herds, multiple paired dam sera (1 3 cows and 4 1 cows bled, respectively) were collected. Paired sera were tested for IBR, BVD, Leptospira spp. (4 serovars), B. abortus, and T. gondii.

The following serologic tests were performed on fetal fluids collected from the body cavities of 69 fetuses for serology: total fetal immunoglobulin G levels in 62 samples and antibody titers to T. gondii in 44 samples, IBR in 63 samples, BVD in 51 samples, Parainfluenza 3 virus in 46 samples, bluetongue virus in 57 samples, 6 serovars of Leptospira spp. in 56 samples, and B. abortus in 27 samples.

For viral isolation organ pools of lung, liver, spleen, kidney, thymus, brain, and, when submitted, placenta, were homogenized, and diluted in a viral transport medium, centrifuged, and the supernatant was inoculated into cultures with Madin-Darby bovine kidney cells. Cultures were incubated in 5% CO, at 37 C for 5 to 7 days. Direct fluorescent antibody tests for noncytopathogenic BVD were performed whether or not cytopathic effects were observed. Cultures were checked for hemadsorption with bovine red cells to

screen for Parainfluenza 3 virus. Direct fluorescent antibody tests for IBR and BVD were run on frozen sections of lung or liver, adrenal, and spleen in 45 fetuses.

Chlamydia1 cultures were performed on tissue pools or placenta from 24 fetuses. Tissues were placed in a chlamydia1 transport medium,28 homogenized, centrifuged, the supernatant inoculated onto McCoy cell cultures, and incubated for 5 days. Cultures were stained with a monoclonal conju- gate to Chlamydia psittaci (California Integrated Diagnostics, Berkeley, CA).

In 58 fetuses, ocular aqueous humor was tested for nitrates by ion exchange chromatography.

Multiple tissues were sampled and placed in 10% neutral buffered formalin, fixed for 24 hours, and processed and embedded in paraffin using routine procedures. Five micron sections were stained with hematoxylin and eosin. The tissues and the number of fetuses from which they were examined included liver (77), kidney (79), heart (82), spleen (61), lung (go), thymus (66), brain (82), gastrointestinal tract (57), adrenal gland (54), skeletal muscle (64), and lymph node (33). Placenta was examined when submitted (1 9). Sections stained with periodic acid-Schiff and Giemsa stains were also examined on some tissue sections.

Results

Eighty-two ( 18%) bovine fetuses that were submitted met the criteria listed in the Materials and Methods. These 82 fetuses were received year-round, although approximately half of the cases were received from November through February. They were submitted from 56 different herds, 54 of which were from dairies. There were multiple abortions reported in 36 herds. Twelve of these herds had more than one fetus (36 fetuses from 12 herds) included in this study group. There were no reports of clinical signs in the cows that aborted.

At necropsy, most fetuses were autolyzed to some degree, with red-tinged fluid in body cavities and sub- cutaneously, and had no significant gross pathologic findings. Pale-tan streaks were found in the muscles of three fetuses, mildly enlarged lymph nodes were found in seven fetuses, and fibrin strands were found in the abdomen of one fetus. Figure 1 summarizes the gestational age of the fetuses. Fetuses were between 3 and 9 months gestation, although at least 75% of the fetuses submitted were between 5 and 7 months gestation.

Serologic results

Fifty-two of the 69 fetal fluids were negative for all tests performed. Total fetal immunoglobulin G levels were greater than 20 mg/dl in 12 fetuses (fetus Nos. 2, 3,6, 12, 16, 18,25, 30,45,48,70, 80). Antibody titers were detected in fetal fluids to BVD in three fetuses (fetus Nos. 36,48,49); IBR in three fetuses (fetus Nos. 9, 19, 36); Parainfluenza 3 virus in two fetuses (fetus Nos. 13, 48); and T. gondii in one fetus (fetus No. 80 with a titer of 1 : 60).


356 Barr et al.

1 2 3 4 5 6 7 8 9 Gestational Age (Months)

Gestational age, in months, of all bovine fetuses diagnosed with nonsuppurative encephalitis and myocarditis, and the number of fetuses where protozoa were found in the tissues.

Fig. 1.

A total of 39 sera were submitted from cows that aborted. Antibody titers to IBR, BVD, and Leptospira spp. were within normal or acceptable ranges. In eight of these samples, antibody titers to T. gondii were determined. Two of these cows had antibody titers of 1 : 64 and 1 : 128 by latex agglutination.

Multiple paired cow sera were also obtained from cows in two herds diagnosed with this particular abortion problem. In the first herd, blood that was collected from 13 cows had no seroconversions or elevated titers to IBR, Leptospira spp., B. abortus, or T. gondii. In

Table 1. The frequency, distribution, and nature of tissue inflammation in 82 aborted fetuses with encephalitis and myocarditis associated with protozoal infection.

Number Affected/ Percent-

Tissue Number age Af- Histologic Findings Inflammation Exam- fected

ined

Encephalitis

Myocarditis Adrenalitis Myositis Nephritis Hepatitis

Peritonitid steatitis

Placentitis

Pneumonia

82/82

82/82 43/54 46/64 52/79 48/77

25/46

10/19

35/80

100

100 80 72 66 62

54

53

44

Focal nonsuppurative,* focal necrosis

Nonsuppurative Focal nonsuppurative Focal nonsuppurative Focal nonsuppurative Portal nonsuppurative,

Focal nonsuppurative focal necrosis

Focal nonsuppurative,

Focal nonsuppurative, focal necrosis

focal necrosis ~

* Nonsuppurative = mononuclear inflammatory cell infiltrates.

Table 2. The size and location of protozoa observed in aborted fetuses.

Num-

ters

Size of Zoite Cluster (pm)

3 1 4 1 5 3 6 6 7 5 8 6 9 1

10 1 11 1 12 1 13 1 14 2

Brain Brain Brain Brain Brain Brain Brain Brain Brain Brain Brain Brain

1 32 Brain, lymph node, 13-35 x 16-35 abomasum, thymus, adrenal

2 15 Brain, lung, omasum 12-28 x 18-36 14 x 19

Free zoites 1-14 x 13-14 0-16 x 10-16 4-20 x 14-23 6-18 x 16-18

14 x 15 15 x 19 11 x 14 13 x 13

Free zoites Free zoites

15 5 Heart 10-12 x 10-20 16 1 Brain 13 x 20 17 11 Brain, placenta 12-24 x 12-36

the second herd blood was collected from 41 cows. Only elevated antibody titers to BVD were found. The owner indicated the herd had not been vaccinated for BVD for at least 2 years. Seven cows in this herd main- tained persistent titers to BVD (greater than or equal to 1 : 5 12), two cows seroconverted to BVD, while ten cows had no titer to BVD. This herd had seven recent abortions. Two of the aborted cows had no antibody titer to BVD and one aborted cow had a persistent antibody titer of 1 : 5 12. Three fetuses were submitted to the laboratory and met the histologic criteria for this study (Nos. 5, 80, 82). Protozoa were found in one fetus (No. 5).

Histologic results

Protozoa were found microscopically in 17 fetuses that were submitted from 17 of the 56 herds in this study. They were seen in fetuses ranging from 3 to 9 months gestation, although protozoa were found more frequently in fetuses between 3 and 5 months gestation (Fig. 1). Histologically, focal, nonsuppurative infiltrates could be found in several organs (Table 1). Of these affected organs, the pattern and degree of inflammation in the brain, striated muscle, and liver were the most significant. In the brain, there were random small, scattered foci of microglia and necrosis. The focal gliosis was often adjacent to capillaries that had hyperplastic endothelium, with perivascular collec-



Fig. 2. Brain; fetus No. 7. There are foci of microglia in the parenchyma adjacent to a group of capillaries (arrows). The capillaries have thickened walls and are ensheathed by mononuclear cells. Four protozoal zoite clusters (arrowheads show two) lie adjacent to the microglial foci. Bar = 100 pm.

Brain; fetus No. 36 with focal necrosis. Central necrotic debris is surrounded by a thin band of glial cells. Bar = 100 pm.

Brain; fetus No. 7. Higher magnification of the four protozoal clusters in Fig. 1. The nuclei of individual zoites can be seen in these clusters, and a cyst-like membrane or wall is clearly visible around one group (arrow). An unidentified cell nucleus is adjacent to another cluster (arrowhead). Bar = 20 pm.

Liver; fetus No. 23. There is a dense portal infiltrate of small mononuclear cells (arrow) and a large focus of hepatocellular and inflammatory cell necrosis in the adjacent parenchyma (arrowheads). Bar = 100 pm.

Fig. 3.

Fig. 4.

Fig. 5.

tions of mononuclear cells (Fig. 2). Additionally, there mation (Figs. 2, 4), although they were usually ran- were random foci of necrosis, often in white matter or domly located. brain stem, that vaned from focal, swollen, eosino- In the heart, there was severe autolysis, that often philic axons to foci of necrosis, surrounded by rims of exceeded the degree of autolysis in other organs. There glial cells (Fig. 3). Protozoal clusters could be seen were varying numbers of mixed mononuclear cell in- sometimes in association with these foci of inflam- filtrates in the epicardium, myocardium, and endo-


358 Barr et al.

Fig. 6. Brain; fetus No. 1. A cluster of zoites lies within an endothelial cell of a small vessel. The individual zoites are arranged in a rosette-like pattern around a more lucent central region. There is an endothelial cell nucleus at one side of the cluster of zoites. Bar = 10 pm.

Fig. 7. Fig. 8.

Fig. 9.

Brain; fetus No. 4. A cluster of zoites lies within a capillary. Bar = 10 pm. Brain; fetus No. 6. There is a dense cluster of zoites lying directly within the brain parenchyma. The zoites are

Brain; fetus No. 14. A free cluster of zoites lying within the brain parenchyma. There is no obvious wall or randomly arranged and surrounded by a peripheral cyst-like wall or membrane. Bar = 10 pm.

membrane around the zoites and they are dispersed. Bar = 10 pm.

cardium. Infrequent, focal, interstitial infiltrates of similar mixed mononuclear cells were also found in skeletal muscle.

In the liver two patterns of inflammation were en- countered. Mononuclear inflammatory infiltrates were present in portal areas in 43/77 fetuses (56%), and scattered foci of either hepatocellular necrosis, or sinu- soids filled with fibrin thrombi were present in 27/77 fetuses (35%). In a few cases, both types of lesions were present (Fig. 5) .

Random scattered foci of mononuclear inflammatory cells were found in several other organs (Table 1). Occasional, small foci of necrosis were also found in both the interstitium of the lung, and along the surface of cotyledonary villi in the placenta.

Protozoa found in tissues of 17 fetuses were generally round or ovoid, 1.5-2 x 2-6 pm, with prominent nuclei and, in most cases, a distinct plasmalemma. Par- asites were often in clusters surrounded by a limiting

membrane or wall. These parasites will be referred to as zoites throughout this paper, because a distinction as to whether they were merozoites budding from schi- zonts or tachyzoites/bradyzoites within cysts could not be made by light microscopy. The location and size of the parasite clusters are summarized in Table 2.

In four fetuses (Nos. 1-4), clusters of zoites were primarily or exclusively in endothelial cells (Table 2). In two of these fetuses (Nos. 1 and 2), multiple clusters of organisms were found within endothelial cells in several tissues (Table 2), and in several of these clusters, the zoites had a rosette formation (Fig. 6). In fetus Nos. 3 and 4, only one endothelial cluster of zoites was found in the brain, and there was no rosette formation (Fig. 7).

Eleven fetuses (Nos. 5-1 5 ) had clusters of zoites either in neural cells in the brain or in cardiac myofibers. Most of the clusters had the appearance of cysts, as shown in Figs. 4 and 8, with a distinct peripheral wall



which ranged in thickness from 0.2-2 pm. Zoites were observed in random arrangements, usually close to- gether, with no rosette formation. In fetus Nos. 13 and 14 there were clusters of zoites with no limiting membrane or wall, which were located directly in the brain parenchyma (Fig. 9).

In the remaining two fetuses, Nos. 16 and 17, some of the zoite clusters were closely associated with endothelial cells, but whether they were within these cells could not be determined. Fetus No. 16 had one cluster of 28 zoites adjacent to the nucleus of a capillary endothelial cell in the brain. In fetus No. 17, eleven zoite clusters were seen in the brain and placenta. Two of the six clusters in the brain of fetus No. 17 were associated with endothelial cells. The clusters in the brain, as well as three clusters in the placenta, were similar to those shown in Figs. 4 and 8. In the remaining two placental clusters, the zoites were arranged in rosettes and surrounded by a membrane or wall that was 1-2 pm in thickness (Fig. 10).

Discussion

Eighteen percent (82/445) of the total bovine fetal submissions to the diagnostic laboratory during a 2-year period were found to have a consistent pattern of multifocal nonsuppurative encephalitis and myocarditis, suggesting a common infectious disease process. Mi- crobiologic, serologic, and histopathologic examinations did not reveal viral, or bacterial pathogens. The fetuses shared a similar pattern of encephalitis, with distinctive foci of necrosis (Fig. 3) or focal vascular oriented gliosis (Fig. 2). This inflammatory pattern is similar to the encephalitis induced by Toxoplasma gondii, Sarcocystis species, and Neospora caninum infections in ruminant ~ ~ ~ u s ~ s . ~ J ~ J ~ , ~ ~ , ~ ~ Nonsuppurative myocarditis, myositis, hepatitis, nephritis, and focal placentitis found in a large percentage of the fetuses (Table 1) have also been reported in protozoal abor- t i o n ~ . ~ , ' ~ , ~ ~ , ~ ~ , ~ ~ Protozoa were found in 17 of the 82 fetuses with nonsuppurative encephalitis and myocarditis. We conclude that protozoal infections are the cause of these abortions.

Sarcocystis species, Neospora caninum and Toxo- plasma gondii, have all been documented to cause abortion or congenital infection in r u m i n a n t ~ , ~ , ~ J ~ 15,L7,22,24,29,31,32 although there is a controversy whether Toxoplasma is a significant cause of bovine abortion. Attempts to induce experimentally bovine fetal Tox- oplasma infection and abortion have been unsuccessfu16~23~30~3 Dubey has reviewed reports of bovine Toxoplasma abortion, and concluded that Tox- oplasma infection is probably not a significant cause of bovine ab~r t ion .~ Sarcocystis has been well documented as a cause of sporadic abortion in the cow. The organism is identified by its specific endothelial cell

Fig. 10. Placenta; fetus No. 17. There is a dense interstitial cluster of zoites. They are arranged in a rosette-like pattern and are surrounded by a cyst-like wall or membrane with an adjacent unidentified cell nucleus. A large vessel containing red cells lies above the cluster. Bar = 10 km.

tropism, and the presence of rosetting arrays of organisms reflecting its form of asexual reproduction, termed end~po lygony . '~ J~ ,~ ' ,~~ A Neospora caninum-like organism has also been identified in aborted bovine fetuses. It is very similar in appearance to Toxoplasma and has only been differentiated in fetuses by immu- noperoxidase using specific antisera. 1,20,29

The identity of the protozoa in most of these 17 fetuses is unknown. Sarcocystis was diagnosed in only two fetuses (Nos. 1 and 2) and was based on the presence of protozoal clusters in endothelial cells of multiple tissues, and the rosette arrangement of Z O ~ ~ ~ S ' ~ J ~ , ~ ~ - ~ ~ (Fig. 6). In ten of the 17 fetuses (Nos. 5- 14), however, Sarcocystis could be ruled out since the protozoa in these cases were located directly within brain parenchyma (Figs. 8 and 9). Additionally, of the 42 fetuses examined for antibody titers to T. gondii, only one fetus (No. 80) was positive, and there were no significant titers to T. gondii among several cows from the two affected herds examined. Collectively, these data would suggest that Sarcocystis is the etiologic agent in a few cases, and, Toxoplasma may have been present in at least one fetus (No. SO), but the etiology in the vast majority of cases is unknown.

Reports of multiple protozoal abortions in the cow are infrequent. Thilsted et al.32 reported recently on multiple protozoal abortions in dairy cows caused by a Neospora caninum-like organism.32 McCausland et al. reported multiple protozoal abortions in cows from several dairies, and the authors speculated that they were due to Sarcocystis infections.22 Multiple abortions were also seen in one dairy, associated with adult bovine sarcocystosis, although fetal infections were not demonstrated.2 In our study, multiple abortions were seen in 36 herds. In 12 of these herds, presumptive or


360 Barr et al.

confirmed protozoal fetal infection was diagnosed in multiple fetuses. No clinical signs were reported in the aborting cows. These clinical and pathologic findings closely resemble the reports by Thilsted et al.32 and McCausland et a1.,22 although our data demonstrate a markedly higher incidence of protozoal infections.

Protozoa were found most frequently in the youngest of the submitted fetuses (Fig. 1). Microscopically, in the majority of cases where multiple protozoa were found, the degree of inflammation in the brain was often mild. Vascular oriented, focal gliosis was the dominant inflammatory change, and necrotic foci were infrequent in these cases. This association between younger fetuses, more visible organisms, and less severe tissue inflammation may reflect a more poorly developed inflammatory or immune system in these younger fetuses.

The serologic results, from one of the two herds where multiple paired dam sera were examined, in- dicate that several cows in this herd were exposed to BVD virus. Two fetuses from this herd were diagnosed with presumptive protozoal infection and protozoa were found in a third fetus (Table 2, fetus No. 5). BVD was not isolated or demonstrated by fluorescent antibody tests in any of these fetuses, but given the sero- logical results, a possible interaction between BVD and fetal protozoal infections cannot be ruled-out in this particular herd. In conjunction with these findings, it is interesting to note that noncytopathogenic BVD has been isolated from an aborted calf infected with a Neo- spora caninurn-like organism."

The results of this retrospective study suggest that protozoal infections are a significant cause of abortion in California dairies. Further studies are necessary to define the etiology. Isolation of an organism is perhaps the first step in precisely defining the agent, its life cycle, and pathogenesis of the disease process.

Acknowledgements

The authors thank Dr. S. Hietala, M. Stillian, J. Goodbrod, and P. Chiu for their technical assistance and S. Arnold for assistance in preparing this manuscript. Supported in part with funding provided through Livestock Diseases Research Laboratory, School of Veterinary Medicine, University of California, Davis, CA.

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33 United States Department of Agriculture, National Vet- erinary Services Laboratory: Laboratory procedures for isolating, identifying and typing Brucella, pp. 23-25. USDA National Veterinary Services Laboratory, Ames, IA. 1985

299-302, 1980

Request reprints from Dr. B. C. Barr, California Veterinary Diagnostic Laboratory System, PO Box 1770, Davis, CA 95617 (USA).


Vet Pathol-1990-Barr-354-61

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