Pathology in Practice

Alexandra Myers Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Lorelei Clarke Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Dana L. Ambrose Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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Elizabeth W. Howerth Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602.

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History

A 2-year-old spayed female English Setter that arrived in Atlanta on a flight from South Africa was boarded at a nearby quarantine facility. The day following its arrival, the dog appeared to be dead and was brought to the referring veterinarian. The dog's rectal temperature was 41.7°C (107°F) at that time, and cardiopulmonary resuscitation efforts were unsuccessful. No other external abnormalities were noted, and the body was submitted to the Athens Veterinary Diagnostic Laboratory at the University of Georgia for necropsy.

Clinical and Gross Findings

At necropsy, the dog weighed 14.5 kg (31.9 lb) with a body condition score of 3/5. On external examination, the mucous membranes were mildly cyanotic and there was fecal staining on the perineum. The intrathoracic, periaortic soft tissue was expanded by large amounts of blood (Figure 1). A 13-cm-long, shiny, gelatinous, loosely adhered thrombus occluded the descending aorta just cranial to the diaphragm. The aorta was dilated at this level with an irregularly thickened wall (aneurysm). The lungs were diffusely congested.

Figure 1—
Figure 1—

Photographs of the thoracic cavity (A) and opened aorta (B) of a 2-year-old English Setter that died soon after a flight from South Africa to the United States. Notice the hemorrhage and swelling along the aorta cranial to the diaphragm (white arrow). In the opened aorta, there is a thrombus loosely adhered to the intimal lining (T) where the lumen is markedly dilated and the wall thickened (Aa), compared with the more proximal portion of the aorta (Ao). Liver (L), diaphragm (D), and a portion of the lungs (Lu) are labeled for orientation.

Citation: Journal of the American Veterinary Medical Association 250, 11; 10.2460/javma.250.11.1255

Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→

Histopathologic and Parasitological Findings

Samples of all major organs and tissues including the aorta were fixed in neutral-buffered 10% formalin and prepared for histologic evaluation. Microscopically, the architecture of the aorta was severely altered (Figure 2). The tunica intima was irregularly thickened by fibrous tissue infiltrated with degenerate neutrophils, and the endothelium was eroded. The tunica media was disrupted and replaced by fibrovascular proliferation and pockets of degenerate neutrophils and fibrin. Severe fibrovascular proliferation with neutrophils and hemorrhage greatly thickened the adventitia, where many sections of a metazoan parasite were surrounded by serohemorrhagic fluid with neutrophils and necrosis. The perivascular connective and adipose tissues contained severe hemorrhage and large numbers of neutrophils as well as sections of metazoan parasites. The parasites were pseudocoelomic with a smooth cuticle, coelomyarian musculature, a large intestinal tract lined by columnar uninucleate cells with microvilli, large vacuolated lateral chords, a uterus, and eosinophilic fluid within the pseudocoelom. These characteristics were consistent with a nematode (Figure 3).

Figure 2—
Figure 2—

Photomicrograph of a section of the aorta from the dog in Figure 1. Notice the severe architectural alteration. The tunica intima (I) is irregularly thickened, the tunica media (TM) is disrupted with replacement by fibrosis, and the adventitia is greatly expanded by fibrovascular proliferation (FV) with neutrophilic infiltration and hemorrhage. Perivascular hemorrhage (H) is massive. Multiple sections of Spirocerca lupi (SL) are present in the adventitia surrounded by serohemorrhagic fluid and necrosis. H&E stain; bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 250, 11; 10.2460/javma.250.11.1255

Figure 3—
Figure 3—

Photomicrograph of a section of aorta with a higher magnification view of several S lupi within the adventitia of the aorta. These nematodes are characterized by a smooth cuticle, coelomyarian musculature (C), a large intestinal tract lined by columnar uninucleate cells with microvilli (In), large vacuolated lateral chords (L), and a uterus (U). H&E stain; bar = 200 μm.

Citation: Journal of the American Veterinary Medical Association 250, 11; 10.2460/javma.250.11.1255

The nematodes observed in the tissue sections were subsequently teased out of the aortic wall and examined. The organisms were identified as L4 and L5 larvae of Spirocerca lupi on the basis of their morphologic characteristics, namely size; lack of sexual organs; red color; presence of a mouth with no definite lips; a short, thick buccal cavity; and an esophagus with a short muscular anterior portion and a longer glandular posterior portion.

Morphologic Diagnosis and Case Summary

Morphologic diagnosis and case summary: intrathoracic aortic aneurysm with thrombosis, rupture, and periaortic hemorrhage attributed to S lupi infection in a dog.

Comments

Spirocerca lupi is a spirurid nematode that affects canids in tropical and subtropical regions including the southern United States.1,2 This parasite is known for producing nodules in the wall of the esophagus that have the potential to transform into sarcomas.1–3 To acquire the parasite, dogs must eat the intermediate host (a coprophagic beetle) or paratenic hosts such as rodents, chickens, small reptiles, or amphibians.1,2 Larvae hatch in the stomach and migrate along gastric arteries to the aorta where they develop in the vessel wall for as long as 3 months.1,2 During this developmental phase, major damage of the aorta can occur, leading to aneurysm, mineralization, thrombosis, and potentially aortic rupture, as in the dog of the present report.1–3 After developing in the aorta, the worms migrate directly to the adjacent esophagus where they begin reproducing and laying eggs.1,2 Eggs are passed in the host's feces and consumed by coprophagic beetles, thereby completing the nematode's life cycle.

Many dogs will not have clinical signs of spirocercosis until esophageal nodules become large enough to obstruct food passage.1,2 The typical clinical signs of spirocercosis include regurgitation, vomiting, anorexia, weight loss, coughing, aspiration pneumonia, and other related signs.1–3 Sometimes, death occurs suddenly with no preceding signs owing to rupture of the wall of the aorta that has become weakened by the encysted nematodes.1,2 Other differential diagnoses for aortic aneurysms in dogs include hypertension, atherosclerosis, or spontaneous dissecting aneurysms, which has been reported to be a familial trait in Leonbergers.4 Spondylitis of thoracic vertebrae is a common finding in dogs with spirocercosis, but the vertebral column of the dog of the present report was not examined radiographically or microscopically.1,3,5 The pathogenesis of S lupi-associated spondylitis of thoracic vertebrae is unknown, but aberrant migration of larvae from the adjacent aorta is suspected.5 In a proportion of dogs, esophageal nodules undergo transformation into sarcomas, most often osteosarcomas or fibrosarcomas.3 Metastasis of these tumors, most often to the lungs, is common as is development of microcytic, hypochromic anemia as a result of chronic ulceration and bleeding of the tumor.3 Hypertrophic osteopathy is a condition that may develop in the long bones of dogs that have S lupi-associated sarcomas; when a diagnosis of hypertrophic osteopathy is made for a dog residing in an area in which S lupi is endemic, further testing for spirocercosis should be undertaken.1–3

Diagnosis of spirocercosis can be challenging. Eggs are sporadically shed in feces; hence, fecal flotation is not a sensitive test for this infection in dogs.1,2 Radiography is also considered insensitive for identification of S lupi-associated lesions.6 Results of a recent study6 indicated that CT is much more effective than radiography for detection of lesions in the aorta, and CT examination is less invasive than endoscopic examination. Endoscopy is still considered the most sensitive diagnostic test for diagnosis of spirocercosis because it allows direct visualization of esophageal nodules; however, unlike CT, it does not provide information about the extent of aortic damage.1–3,5,6 In the English Setter of the present report, aortic lesions were found in the absence of esophageal lesions; had the dog been examined for signs of spirocercosis prior to death, CT would have been the best diagnostic test option.

For several years, the recommended treatment protocol for nonneoplastic spirocercosis has involved SC administration of doramectin.2,7 In a recent study2 of experimentally infected dogs, a spot-on formulation of 10% imidacloprid and 2.5% moxidectin was successful in controlling the migrating and encapsulated forms of S lupi. This formulation is approved for use in prevention and treatment of S lupi infections in dogs in South Africa, where the parasite is endemic.2 Oral administration of milbemycin oxime has also proved successful in resolving S lupi-related esophageal lesions.7 No drug treatment, however, is able to resolve aortic lesions such as aneurysms and mineralization.2,7 Therefore, in endemic areas, prevention of spirocercosis is important. Prohibiting dogs from hunting and scavenging reduces the likelihood of infection, and administering preventative doses of macrocyclic lactones, although not approved for prevention of spirocercosis in the United States, has been shown to effectively limit infections.2,7 Once esophageal nodules have progressed to malignancy, surgery and chemotherapy may be attempted, but overall prognosis and survival time for affected dogs are poor.3

The dog in the present report had just arrived in the United States on a flight from South Africa, and it is possible the flight or associated stress could have precipitated the aortic aneurysm rupture. Spirocerca lupi is found worldwide, especially in tropical and subtropical regions.1,2,5,7 Clinicians in the southern United States should include spirocercosis as a differential diagnosis for dogs that die suddenly with no clinical signs, dogs that develop regurgitation and vomiting, or dogs with hypertrophic osteopathy; suspicion for S lupi infection should increase for dogs not routinely receiving macrocyclic lactones.

References

  • 1. van der Merwe LL, Kirberger RM, Clift S, et al. Spirocerca lupi infection in the dog: a review. Vet J 2008; 176: 294309.

  • 2. Austin CM, Kok DJ, Crafford D, et al. The efficacy of a topically applied imidacloprid 10%/moxidectin 2.5% formulation (Advocate(R), Advantage(R) Multi, Bayer) against immature and adult Spirocerca lupi worms in experimentally infected dogs. Parasitol Res 2013; 112(suppl 1):91108.

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  • 3. Ranen E, Lavy E, Aizenberg I, et al. Spirocercosis-associated esophageal sarcomas in dogs. A retrospective study of 17 cases (1997–2003). Vet Parasitol 2004; 119: 209221.

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  • 4. Chetboul V, Tessier D, Borenstein N, et al. Familial aortic aneurysm in Leonberg dogs. J Am Vet Med Assoc 2003; 223: 11591162.

  • 5. Kirberger RM, Clift SJ, van Wilpe E, et al. Spirocerca lupi-associated vertebral changes: a radiologic-pathologic study. Vet Parasitol 2013; 195: 8794.

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    • Export Citation
  • 6. Kirberger RM, Stander N, Cassel N, et al. Computed tomographic and radiographic characteristics of aortic lesions in 42 dogs with spirocercosis. Vet Radiol Ultrasound 2013; 54: 212222.

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    • Search Google Scholar
    • Export Citation
  • 7. Kok DJ, Schenker R, Archer NJ, et al. The efficacy of milbemycin oxime against pre-adult Spirocerca lupi in experimentally infected dogs. Vet Parasitol 2011; 177: 111118.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Figure 1—

    Photographs of the thoracic cavity (A) and opened aorta (B) of a 2-year-old English Setter that died soon after a flight from South Africa to the United States. Notice the hemorrhage and swelling along the aorta cranial to the diaphragm (white arrow). In the opened aorta, there is a thrombus loosely adhered to the intimal lining (T) where the lumen is markedly dilated and the wall thickened (Aa), compared with the more proximal portion of the aorta (Ao). Liver (L), diaphragm (D), and a portion of the lungs (Lu) are labeled for orientation.

  • Figure 2—

    Photomicrograph of a section of the aorta from the dog in Figure 1. Notice the severe architectural alteration. The tunica intima (I) is irregularly thickened, the tunica media (TM) is disrupted with replacement by fibrosis, and the adventitia is greatly expanded by fibrovascular proliferation (FV) with neutrophilic infiltration and hemorrhage. Perivascular hemorrhage (H) is massive. Multiple sections of Spirocerca lupi (SL) are present in the adventitia surrounded by serohemorrhagic fluid and necrosis. H&E stain; bar = 100 μm.

  • Figure 3—

    Photomicrograph of a section of aorta with a higher magnification view of several S lupi within the adventitia of the aorta. These nematodes are characterized by a smooth cuticle, coelomyarian musculature (C), a large intestinal tract lined by columnar uninucleate cells with microvilli (In), large vacuolated lateral chords (L), and a uterus (U). H&E stain; bar = 200 μm.

  • 1. van der Merwe LL, Kirberger RM, Clift S, et al. Spirocerca lupi infection in the dog: a review. Vet J 2008; 176: 294309.

  • 2. Austin CM, Kok DJ, Crafford D, et al. The efficacy of a topically applied imidacloprid 10%/moxidectin 2.5% formulation (Advocate(R), Advantage(R) Multi, Bayer) against immature and adult Spirocerca lupi worms in experimentally infected dogs. Parasitol Res 2013; 112(suppl 1):91108.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Ranen E, Lavy E, Aizenberg I, et al. Spirocercosis-associated esophageal sarcomas in dogs. A retrospective study of 17 cases (1997–2003). Vet Parasitol 2004; 119: 209221.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Chetboul V, Tessier D, Borenstein N, et al. Familial aortic aneurysm in Leonberg dogs. J Am Vet Med Assoc 2003; 223: 11591162.

  • 5. Kirberger RM, Clift SJ, van Wilpe E, et al. Spirocerca lupi-associated vertebral changes: a radiologic-pathologic study. Vet Parasitol 2013; 195: 8794.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Kirberger RM, Stander N, Cassel N, et al. Computed tomographic and radiographic characteristics of aortic lesions in 42 dogs with spirocercosis. Vet Radiol Ultrasound 2013; 54: 212222.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Kok DJ, Schenker R, Archer NJ, et al. The efficacy of milbemycin oxime against pre-adult Spirocerca lupi in experimentally infected dogs. Vet Parasitol 2011; 177: 111118.

    • Crossref
    • Search Google Scholar
    • Export Citation

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