History
A 2-year-old pregnant heifer aborted her first calf in the third trimester. She was housed on an outdoor pasture with other bred heifers. Third-trimester abortions had been a chronic problem in this herd for the past 7 years. The farm’s vaccination history was unknown.
Gross Findings
Postmortem examination of the fetus revealed a slightly edematous body with no obvious congenital abnormalities. There was pitting of both humeral heads with extensive loss (necrosis) of the articular cartilage (Figure 1). The right humeral head was replaced by friable fibrinonecrotic debris that also extended into the joint space. The lungs were diffusely congested and rubbery. The placenta was unavailable for examination, and the physical examination of the dam was unremarkable.
Photographs of the right (A) and left (B) opened shoulder joints and the humoral heads of a late-term fetus aborted from a first calf heifer. A—There is near complete destruction of the right humeral head, and the joint space is filled with abundant friable, tan, fibrinonecrotic debris. The remnants of the humeral head (H) and glenoid fossa (F) can barely be grossly discerned within the debris. The synovial lining is moderately thickened (asterisks). B—The articular surface of the humeral head (H) is irregular and roughened, with multifocal pitting of the cartilage and locally extensive complete cartilage loss (necrosis) to expose the underlying bone (black arrows). The synovial lining is mildly thickened (asterisks).
Citation: Journal of the American Veterinary Medical Association 261, 9; 10.2460/javma.23.04.0185
Histopathologic and Microbiological Findings
Tissue samples of the fetal humeral heads, eye, brain, and representative visceral organs were fixed in neutral-buffered 10% formalin and processed routinely for histologic examination. On histologic examination, the articular cartilage of the humerus had locally extensive multifocal areas of necrosis with fibrin and erosion and fibrillation of the articular cartilage (Figure 2). The surface of the remaining cartilage was roughened and had pockets of inflammatory cells. The inflammatory population was composed primarily of neutrophils and macrophages and was accompanied by moderate edema. Multifocally, fibrovascular tissue extended into the necrotic cartilage. The epiphyseal bone underlying the necrotic and erosive cartilage was locally, extensively destroyed.
Photomicrograph of the right humeral head. The articular cartilage is extensively eroded with multifocal areas of necrosis (viable cartilage [VC] and necrotic cartilage [NC] are visible). The necrotic aspect of the cartilage is thinned to lost and blends with the necrotic aspect of the underlying bone (viable bone [VB] and necrotic bone [NB] are visible). H&E stain; bar = 1 mm.
Citation: Journal of the American Veterinary Medical Association 261, 9; 10.2460/javma.23.04.0185
The alveolar septa of the pulmonary parenchyma were expanded by congestion and numerous inflammatory cells composed mostly of neutrophils and macrophages with lesser numbers of lymphocytes and plasma cells (Figure 3). Within the alveolar lumen, there were more neutrophils and macrophages as well as extracellular basophilic material. When fetal eye and periorbital tissues were examined, the conjunctiva had low numbers of lymphocytes.
Photomicrograph of the lungs. There are infiltrates of neutrophils and macrophages present within the alveolar lumen (long arrows) and expanding alveolar septa (arrowheads). The alveolar septa are also slightly expanded by congested capillaries. A terminal bronchus at the peripheral lower edge of the photomicrograph is similarly affected. H&E stain; bar = 50 µm.
Citation: Journal of the American Veterinary Medical Association 261, 9; 10.2460/javma.23.04.0185
Fresh samples of brain, lung, liver, and kidney were submitted for real-time PCR targeting bovine herpesvirus-1, bovine viral diarrhea virus, Leptospira spp, Neospora caninum, and Ureaplasma diversum. Synovial tissue from the affected joint was also submitted for real-time PCR targeting U diversum. The assays revealed very low cycle thresholds of 19.1 and 19.3 for U diversum in the pooled tissues and the synovium, respectively, and were negative for bovine herpesvirus-1, bovine viral diarrhea virus, Leptospira spp, and N caninum. Fresh samples of lung, liver, and abomasal contests were submitted for aerobic culture, including enrichment for Salmonella spp, and were negative.
Morphologic Diagnosis and Case Summary
Morphologic diagnoses: lungs: moderate, multifocal, subacute, neutrophilic bronchopneumonia; humerus: severe, multifocal, subacute, fibrinonecrotizing and erosive arthritis with subchondral bone necrosis
Case summary: bovine abortion with fetal pneumonia and arthritis, consistent with U diversum infection.
Comments
Ureaplasma diversum is a member of the family Mycoplasmataceae, which is frequently found on the mucous membranes of the nasal passages, vulva, and vagina of the cow and the prepuce of bulls, associated with both sick and asymptomatic animals.1,2 While generally considered a commensal organism, U diversum is associated with granular vulvovaginitis, endometritis, infertility, and abortions.1,2 Ureaplasma abortion outbreaks in dairy herds typically present as clusters of several to many abortions, with most being in the third trimester. Notably, abortion outbreaks can happen in heifer-only groups and in groups of older cows. In addition to abortion, Ureaplasma infection can also be responsible for stillborn and weak calves.3
In addition to ascending infection of the uterus from the vulva or vagina, U diversum can be delivered to the uterus via semen or embryo transfer fluid. In fact, one of the ways U diversum presents a unique challenge in the dairy industry is the tenacity of the pathogen during embryo transfer and in vitro fertilization. The organism can be picked up as contamination from embryo or ova collection and readily adheres to the zona pellucida during in vitro exposure. Washing procedures recommended by the International Embryo Transfer Society frequently fail to remove the organism, allowing for potential transfer with the embryo to the recipient dam. Additionally, freezing the embryo transfer fluids appears to have relatively little effect.3 Ureaplasma has also been isolated in frozen semen for artificial inseminations, although, to the author’s knowledge, no report of Ureaplasma infection from artificial insemination has been reported in veterinary species to date.4
The placenta should always be evaluated in abortion workups, whenever possible. In classic cases of Ureaplasma, macroscopic examination of the placenta will reveal an amnionitis. This presents as increased redness of the amnion in acute cases and yellow thickenings of the amnion, the cotyledons, and the intercotyledonary spaces of the chorioallantois in chronic cases. The chronic presentation of Ureaplasma placentitis can mimic the macroscopic presentation of fungal or select bacterial abortions that affect cotyledons and intercotyledonary spaces, including Brucella abortus, Coxiella burnetti, and Chlamydia abortus.2
Oftentimes, fetal lesions will include a bronchopneumonia and may have enlarged bronchus-associated lymphoid tissues. Other causes of fetal bronchopneumonia in cattle include, but are not limited to, Brucella spp, Salmonella spp, Mannheimia spp, Pasteurella spp, Histophilus somni, and Tritrichomonas fetus.2 Interestingly, while many members of the family Mycoplasmataceae (especially Mycoplasma spp) are reported in arthritis in juvenile calves,2 only U diversum infection in cattle is a reported etiologic cause of infectious fetal osteoarthritis.5
In short, Ureaplasma is likely a more significant cause of abortion in cattle than originally hypothesized. Affected samples of the lung and the synovium of affected joints should be included in tissue pools for PCR testing for causes of abortion, and U diversum should be included in the list of organisms tested. (Liver is reported to be a good tissue for PCR detection of U diversum as well.1) Because this organism is difficult to culture, molecular methods are preferred for identification.
Acknowledgments
The authors have nothing to disclose.
References
- 1.↑
Díaz JM, Prieto A, López G, et al. Association of Ureaplasma diversum with reproductive disease in cattle. N Z Vet J. 2019;67(5):249-256. doi:10.1080/00480169.2019.1623733
- 2.↑
Foster RA. Female reproductive system and mammae. In: Zachary JF, ed. Pathologic Basis of Veterinary Disease. 7th ed. Elsevier; 2022:1267, 1279, 1285, 1287, 1293-1294, 1296, 1301, 1332.
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Crane MB, Hughes CA. Can Ureaplasma diversum be transmitted from donor to recipient through the embryo? Two case reports outlining U. diversum losses in bovine embryo pregnancies. Can Vet J. 2018;59(1):43-46.
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Marques LM, Buzinhani M, Neto RL, et al. Detection of Ureaplasma diversum in bovine semen straws for artificial insemination. Vet Rec. 2009;165(19):572-573. doi:10.1136/vr.165.19.572
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Himsworth CG, Hill JE, Huang Y, Waters EH, Wobeser GA. Destructive polyarthropathy in aborted bovine fetuses: a possible association with Ureaplasma diversum infection? Vet Pathol. 2009;46(2):269-272. doi:10.1354/vp.46-2-269
