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Brief Communication |
Correspondence: 1Corresponding Author: Julia H Wilson, Veterinary Population Medicine, 1365 Gortner Avenue, St. Paul, MN 55108
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Abstract |
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Key Words: Blastomycosis • horse • lungs • mammary gland • skin • thrombi
Blastomycosis is a severe fungal disease characterized by multisystemic pyogranulomatous lesions affecting humans and many animal species, particularly dogs, but rarely horses.7 The objective of this case report is to describe the clinical features and pathologic lesions in a broodmare and to increase veterinarians' index of suspicion for this disease in horses.
A 17-year-old Quarter horse mare was presented to the Veterinary Medical Center (VMC), University of Minnesota, College of Veterinary Medicine, for assessment of progressive weight loss, mastitis, and multifocal ulcerative cutaneous lesions of 6 months duration. The mare had foaled uneventfully in the spring. The owner noted swelling of the right side of the mammary gland at 3 months postpartum. The foal was weaned, and the mare was treated unsuccessfully for several weeks with systemic antibiotics by the initial veterinarian consulted. The right half of the mammary gland became ulcerated and discharged a seropurulent exudate. Intramammary antibiotics labeled for bovine use (dry cow treatment) were administered into the mammary gland to no effect. Two months after the onset of mammary gland swelling, the mare developed draining tracts in the pectoral area and was treated symptomatically with intravenous oxytetracycline and flunixin meglumine. By the next month, similar lesions had developed on the ventrum and hind leg of the mare, and subsequently a second veterinary practice was consulted. Swabs of the exudate yielded a diagnosis of cutaneous blastomycosis based on typical cytologic features of the organism. The mare was treated with griseofulvin orally and daily cleansing of the cutaneous lesions. No fever or respiratory difficulty was noted during the illness. Despite a good appetite, the mare progressively lost weight, and was referred to the University of Minnesota's VMC.
Physical examination observations at the VMC included slight tachycardia (48 bpm); normal rectal temperature and respiratory rate; poor body condition (2/9 Henneke scale15); and multiple cutaneous lesions with seropurulent drainage in the pectoral region, ventrum, caudal abdomen, inguinal region, medial and dorsal surfaces of the hind limbs, and mammary gland. Both rear legs were mildly swollen distally. Imaging of the thorax revealed ventral fluid accumulation, multiple foci of abnormal tissue echogenicity in the dorsal lung surface (ultrasound), and a cavitated mass-like lesion in the caudodorsal lung fields (radiography). A small amount of anechoic fluid was observed in the pericardial sac (ultrasound). Aspirates of pleural fluid were highly cellular, consisting predominately of mature neutrophils, but no microbes were seen. Smears of the cutaneous exudate revealed fungal organisms compatible with Blastomyces dermatitidis. The hematocrit of the mare was 29% (reference range, 27–43%), and plasma protein was mildly elevated at 8.2 g/dl (reference range, 6.1–7.9 g/dl). A clinical diagnosis of cutaneous and systemic blastomycosis was made. Based on the poor prognosis and expense of antifungal treatment, the horse was euthanized.
At necropsy, the skin of the inguinal and pectoral areas was extensively ulcerated and covered with a yellowish-orange exudative crust. In the inguinal subcutaneous tissues, multiple draining tracts filled with copious, malodorous, thick yellow pus were observed. The mammary gland was swollen, ulcerated, and indurated; sectioning revealed abundant fibrous connective tissue and coalescing pyogranulomas (Figs. 1, 2). Multifocal, pyogranulomatous pneumonia, accompanied by fibrous adhesions between the visceral pleura of the lung and the costal aspect of the parietal pleura ventrally, was noted in the thoracic cavity (Fig. 3). The ventral mediastinum and pericardium contained multiple firm, cream-colored nodules of variable sizes (Fig. 4). Multiple thrombi were present in the lungs, along with cream-colored nodules ranging from 0.1 to 3.0 cm in diameter (Fig. 5). A large mural thrombus was found in the right atrium, and a smaller one was found in the trunk of the pulmonary artery. Thrombi were also identified in the saphenous vein of the right hind limb and veins of the left thigh. The tracheobronchial and superficial inguinal lymph nodes were firm, markedly enlarged, and contained coalescing tan and cream-colored foci on cut section.
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Mild inflammatory infiltrates, predominately lymphocytes and plasma cells, were identified in perivascular sites of 1 kidney, portal tracts of the liver, and in multiple foci of 1 adrenal gland; however, no fungal organisms were noted in these tissues. The spleen contained many neutrophils and the femoral diaphyseal bone marrow cellularity was high, with an estimated myeloid:erythroid ratio of 10 : 1. No significant pathologic changes were observed in the heart, thyroid glands, trachea, esophagus, stomach, intestines, uterus, ovaries, urinary bladder, brain, or eyes.
Aerobic bacterial cultures of the inguinal abscess, lung, lymph nodes, and mammary gland were negative. Fungal cultures of the inguinal abscess, lung, lymph node, and mammary gland grew B. dermatitidis-like colonies. Deoxyribonucleic acid (DNA) probe analysis at the Minnesota Department of Health confirmed the fungus as B. dermatitidis. The mare's foal was seronegative by agar gel immunodiffusion testing for antibodies to B. dermatitidis at 11 months of age and remains healthy at 22 months.
Blastomycosis is a fungal disease of multiple mammalian species, but is best documented in humans and dogs.1,8 Despite a likely high exposure rate in endemic areas, blastomycosis is a very rare disease in horses and may present as either a cutaneous or systemic illness.6,24,25 Blastomycosis has been a reportable disease in Wisconsin since 1984, where it is the most prevalent systemic fungal infection, averaging 99 human cases/year. At the time of diagnosis, the horse in this case report resided in one of the highest ranking counties (Washburn) with 12.1 human cases/100,000 residents from 2000–2004 (JR Archer, unpublished data 2005). A cluster of canine cases was also identified in this county.2
Inhalation is considered the primary route of infection in human8 and canine9 systemic blastomycosis cases and is likely a route of infection for horses. Epidemiologic investigations into clusters of human cases in this region have identified point sources of spores in locations where organically rich soil has been disturbed, such as an old woodpile.3 In dogs in Wisconsin and Louisiana, the odds of living within 400 m of a body of water was 10 times greater for blastomycosis cases than control dogs.1,4 Within northern Wisconsin, a higher risk of blastomycosis has been similarly demonstrated in humans and dogs living near lower elevation waterways or on sandy soils prone to drought.2,5 One explanation for this water link is that wet Blastomyces conidiophores readily release conidia that can become aerosolized with rooting and sniffing behavior, with subsequent inhalation.1 Sandy soil was reported on the horse owner's property but no waterways were adjacent to the mare's pasture; however, the mare was housed near a lake until just after foaling. If this area were the source of infection, the organism would have been introduced into the mare most likely by the aerosol route at least 3 months before the observation of clinical abnormalities. This seems plausible, as the incubation period in human cases originating from an inhaled point source has ranged from just under 2 weeks to almost 15 weeks.11
Alternatively, based on the initial signs of mammary gland lesions in this mare and the late onset of systemic signs, the fungal infection may have begun cutaneously, after introduction of the organism to the mammary gland. In humans, primary cutaneous blastomycosis is uncommonly observed, as most cases with skin lesions are associated with hematogenous spread from lung foci, particularly to areas of devitalized tissue (e.g., sites of trauma).12,14 A review of 22 published cases in humans describes half of the exposures as occupational self injury in laboratory or morgue settings.14 Cutaneous or osseous blastomycosis without the involvement of other organs has been reported in humans in association with direct inoculation of the organism via animal bites or scratches or other traumatic penetrating injuries.14 There have also been several case reports of localized osseous blastomycosis in dogs, but this manifestation is much less common.18,23
Mammary gland infection, as evidenced by this equine case, is comparatively unusual, but has been documented previously in a case of equine blastomycosis.6 The initial lesions, however, were observed in the perineal region with subsequent extension to the mammary gland; the results of a full necropsy were not reported. The mare had lost a colt and had mastitis 3 years previously, and it was hypothesized that the mammary gland may have been injured, predisposing it to infection.6 Most canine cases exhibit multisystemic signs attributable to lesions in the respiratory system, lymphatics, eyes, and skin. Only 3% of dogs in a retrospective study from Louisiana had mammary gland involvement.1 Similarly, few cases of blastomycosis involving the breast have been reported in the human literature.13,22
The chronology of this case suggests the mare may have become infected during pregnancy. In recent years, blastomycosis has become increasingly recognized as a serious infection in immunocompromised hosts.20 Pregnancy is considered a condition with partial immunosuppression, potentially predisposing patients to opportunistic infections such as blastomycosis.10,17,21 A recent review cited 19 human cases of blastomycosis infections during pregnancy, with 2 newborn deaths attributed to congenital blastomycosis.21 Previous case reports of equine blastomycosis have not been associated with pregnancy. Assessment of the immunologic status of this mare was not done, and the role of pregnancy in the horse's susceptibility to and/or ability to mount an effective immune response against the fungal organisms is speculative.
Thrombosis has not been described in previous cases of blastomycosis in the horse; however, thrombophlebitis has been reported as an uncommon complication of blastomycosis in 3 dogs.16,19,26 One dog had blastomycosis involving the hilar lymph node with erosion through the left atrial wall leading to thrombosis,26 another dog had a granuloma of the cranial vena cava resulting in chylothorax and cranial vena caval syndrome,16 whereas in the third dog it was hypothesized that inflammatory events secondary to blastomycosis and granulomatous inflammation likely resulted in endothelial damage and subsequent disseminated intravascular coagulation.19 Disseminated intravascular coagulation or a possible localized inflammatory effect on vascular integrity in close proximity to severe fungal lesions was suggested in this case, given the presence of multiple thrombi in the lungs, heart, and veins of the hind limbs; however, there was no evidence of inflammation or erosion into blood vessels, and no coagulation studies were done.
Although blastomycosis appears to be an uncommon infection in horses, systemic mycotic infections should be included in the list of differential diagnoses for horses with chronic infections, including cases of mastitis and dermatitis refractory to antibiotic therapy. A higher index of suspicion should be maintained for horses in endemic areas.
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