Signalment:  

Adult cow bison, Bison bison.Placenta submitted from a bison cow that recently aborted in a capture facility in Yellowstone National Park.

Gross Description:  

The non-cotyledonary regions of the chorioallantois were diffusely opaque, edematous and white/pink. The cotyledons were tan and had scattered hemorrhage.

Histopathologic Description:

Placenta: Multifocally, the cotyledons of the chorioallantois are necrotic as characterized by loss of distinct villar architecture with replacement by a granular to fibrillar eosinophilic material containing karyorrhectic debris including necrotic leucocytes. Intracytoplasmic bacteria occur within trophoblasts. The deeper connective tissue is edematous with scattered infiltrates of neutrophils and fewer macrophages.

Morphologic Diagnosis:  

Placentitis, necrotizing, acute, multifocal, severe, with intracytoplasmic bacteria and severe edema, chorioallantois, placenta.

Lab Results:  

Brucella abortus biovar 1 was isolated from the placenta.

Condition:  

Brucella abortus

Contributor Comment:  

The primary consequences of brucellosis in domestic animal populations are economic losses due to decreased production. Infections also occur in wild populations and in the United States; bison and elk in the Greater Yellowstone Area (GYA) and wild/feral swine in other areas of the US are natural reservoirs hosts. The recent Brucella abortus outbreaks in cattle within the GYA are considered to be the result of transmission from infected elk herds. Disease management practices in bison herds of Yellowstone National Park have been controversial and polarizing for several decades. Permanent solutions for disease control or population management in the bison and elk herds of this region will be difficult to implement because of a multitude of factors including the following: large wild animal populations within a large geographic area; differing jurisdictional boundaries of governmental agencies; differing state and federal agency missions and mandates; na+�-�ve understanding and exaggerated fears of the disease by various groups and entities; the urbanization of the populace; and financial interests. Although brucellosis has been eradicated in domestic herds in some advanced countries, the disease is still significant in animals and humans throughout most of the world. The agents zoonotic potential also lead to the propagation and incorporation of the agent into national bio-warfare arsenals.

Brucellosis is caused by small gram-negative bacilli of the genus Brucella; these bacteria are facultative intracellular organisms. The organism lacks many of the typical virulence factors of pathogenic bacteria and how the organism resists phagocytic degradation and is able to replicate within professional and non-professional phagocytes is poorly understood. There are multiple species within the genus and include: B. abortus biovars 1-9 (cattle), B. sues biovars 1-5 (swine), B. obis (sheep), B. melitensis biovars 1-3 (sheep and goats), B. can is (dog), B. neotomae (rodents), and species that infect pinnipeds and cetaceans. B. abortus, B. sues and B. melitensis are further subdivided into biovars but contrary to the species name, these organisms can also cause disease in numerous other domestic and wild animal hosts and these are the common species infecting man. B. can is and marine Brucella species have also rarely been associated with disease in man, whereas B. obis and B. neotomae are recognized to only infect sheep and rodents, respectively.

Brucellosis in animals is characterized by third trimester abortion with necrotizing placentitis, retained placentas and metritis, weak calves, mastitis, arthritis/hygromas/bursitis, and in males, orchitis/epididymitis and seminal vesiculitis. The disease in susceptible domestic animal populations has significant economic consequences due to calf loss, infertility, decreased milk production and disease regulatory consequences. Infected animals can eventually become resistant but could still act as intermittent shedders that serve as a reservoir of infection within the herd. Transmission is usually through ingestion or contamination of mucous membranes after exposure to infected fetuses, fetal membranes or contaminated body fluids. Venereal transmission occurs with B. suis, B. obis and B.canis but is uncommon with B. abortus or B. melintensis. Abortions also can occur after vaccination of pregnant females with live vaccine strains.

Brucellosis in man has multiple synonyms such as undulant fever and Malta fever. In countries where the disease is common, infection in man is normally acquired by ingestion of contaminated dairy products or exposure to infected animal reproductive tissues and fluids. Infection can result from exposure to the agent after ingestion, inhalation, through open wounds, accidental injection when vaccinating animals, and congenitally from infected mothers. Effective animal disease control programs and pasteurization of dairy products are major contributors in the low rates of human infections in modern societies. Laboratory personnel, veterinarians and agricultural and slaughterhouse workers are at higher risk for acquiring infections. Laboratory personnel are extremely vulnerable and can readily be exposed if safety precautions are not utilized. Centers for Disease Control and Prevention Biosafety in Microbiological and Biomedical Laboratories (CDC BMBL) recommends strict adherence to BSL-3 safety practices in conjunction with sound laboratory techniques when culturing the organism. The infectious dose for man varies depending on the species. In man, only 1-10 CFU of B. melitensis can cause disease. Reported infectious doses for immune-competent people with the following species are: B. sues (1000-10,000 CFU), B. abortus (100,000 CFU) and B. can is (greater that 1,000,000 CFU).

Acute disease in man usually results in incapacitating flu-like illness, cyclic fevers, gastrointestinal upsets, epididymitis/orchitis, and in severe cases, CNS or endocardial disease. Chronic infections can manifest as chronic fatigue-like syndromes, depression, arthritis, endocarditis, hepatitis, cholecystitis, meningitis, uveitis, and osteomyelitis. Mortality rate is less than 5%. Treatment involves long term antibiotic therapy and currently, there is no human vaccine.

JPC Diagnosis:  

Chorioallantois: Placentitis, necrotizing, multifocal to coalescing, moderate, with marked edema, diffuse vasculitis, and with numerous intratrophoblastic bacilli.

Conference Comment:  

Transmission of brucellosis is by contact with infected tissues, secretions or excretions, such as milk, urine, and fetal and placental tissues. The bacteria penetrate the mucosa and migrate to local and regional lymph nodes after being engulfed by local macrophages or dendritic cells, within which the bacteria grow and replicate. The bacteria kill the phagocytes and incite a pyogranulomatous lymphadenitis due to the lipopolysaccharide composition of the bacterial cell wall. The bacteria are systemically disseminated via leukocyte trafficking, enabling them to infect the mammary glands, reproductive organs, placenta and fetus. Chorionic epithelial cells naturally produce erythritol around the fifth month of gestation, which is a carbohydrate growth promoter for Brucella abortus, and the bacteria multiply in the rough endoplasmic reticulum of chorionic trophoblasts. Other intratrophoblastic bacterial agents causing abortion include Leptospira interrogans, Coxiella burnetti, Listeria monocytogenes, Campylobacter fetus and C. jejuni, and Chlamydophila abortus and C. decorum; intratrophoblastic protozoa include Toxoplasma gondii, Neospora caninum, and Sarcocystis spp., although protozoal cysts are more commonly found in other tissues, especially in the central nervous system.(11)

Fetal death and abortion are attributed to placental disruption and endotoxemia; fibrinous bronchopneumonia, pleuritis and pericarditis are seen in the fetus. In addition to Arcanobacterium pyogenes, B. abortus is the most common cause of bacterial fetal pneumonia. The bacterial infection induces hypoxia through placental inflammation, and this disruption of the placenta induces a breathing response in the fetus, and death is due to aspiration of the amniotic fluid.(3,5,14) Typical gross placental lesions include extensive cotyledonary necrosis; intercotyledonary edema with a tough, yellow to gray, leathery surface; necrosis and inflammation of the placental arcades; and inflammation of the maternal septa, leading to placental interlocking and retained placenta.(5) Brucella abortus is also commonly associated with bursitis in horses, known colloquially as poll evil and fistulous withers.(13)

References:

1. August K, Rovid-Spickler A, et al. Brucellosis. Available at http://www.cfsph.iastate.edu/Factsheets/pdfs/brucellosis.pdf. 2009
2. Beja-Pereira A, Bricker B, et al. DNA genotyping suggests that recent brucellosis outbreak in Greater Yellowstone Area originated from elk. J Wild Dis. 2009;45:1174-1177.
3. Foster RA. Female reproductive system and mammary gland. In: Zachary JF, McGavin MD, eds. Pathologic Basis for Veterinary Disease. 5th ed. St. Louis, MO: Elsevier Mosby; 2011:531.
4. Kreeger TJ, Cook WE, et al. Brucellosis in captive Rocky Mountain bighorn sheep (Ovis canadensis) caused by Brucella abortus biovar 4. J Wild Dis. 2004;40:311-315.
5. Lopez A. Respiratory system, mediastinum, and pleurae. In: Zachary JF, McGavin MD, eds. Pathologic Basis for Veterinary Disease. 5th ed. St. Louis, MO: Elsevier Mosby; 2011:1113.
6. Meyer M, Meagher M. Brucellosis in free ranging bison (Bison bison) in Yellowstone, Grand Teton and Wood Buffalo National Parks: a review. Letter to editor. J Wild Dis. 1997;31:579-598.
7. Olsen SC, Holland SD. Safety of revaccination of pregnant bison with Brucella abortus strain RB51. J Wild Dis. 2003;39:824-829.
8. Rhyan JC, Gidlewski T, et al. Pathology of brucellosis in bison from Yellowstone National Park. J Wild Dis. 2001;37:101-109.
9. Rhyan JC, Holland SD, et al. Seminal vesiculitis and orchitis caused by Brucella abortus biovar 1 in young bison bulls from South Dakota. J Vet Diagn Invest. 1997;9:368-374.
10. Rhyan JC, Quinn WJ, et al. Abortion caused by Brucella abortus biovar 1 in free ranging bison (Bison bison) from Yellowstone National Park. J Wild Dis. 1994;30:445-446.
11. Schlafer DH, Miller RB. Female genital system. In: Maxie MG, ed. Jubb, Kennedy, and Palmers Pathology of Domestic Animals. 5th ed. Vol 3. Philadelphia, PA: Saunders Elsevier; 2007:484-9, 490-516. 
12. Tessaro SV, Forbes LB. Experimental Brucella abortus infection in wolves. J Wild Dis. 2004;40:60-65.
13. Thompson K. Bones and joints. In: Maxie MG, ed. Jubb, Kennedy, and Palmers Pathology of Domestic Animals. 5th ed. Vol 1. Philadelphia, PA: Saunders Elsevier; 2007:172-3.
14. Zachary JF. Mechanisms of microbial infection. In: Zachary JF, McGavin MD, eds. Pathologic Basis for Veterinary Disease. 5th ed. St. Louis, MO: Elsevier Mosby; 2011:189-90, 198.

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2-1. Placenta

2-2. Placenta

2-3. Placenta

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