March 2018 Case of the Month

Description of the aspirate:

The sample was highly cellular and contained predominantly large aggregates of monomorphic mesenchymal cells that formed sheet-like structures that occasionally had a distinct whirling appearance. The cytoplasm of the cells was variable in tincture, ranging from light blue to more gray-purple. Nuclei were elongated to cigar shaped. Anisocytosis and anisokaryosis were mild. There was a distinct fibrillar appearance in some areas. This is most evident in Figure 2. Of note, small clusters of hepatocytes laden with lipofuscin pigment were found in close association with the mesenchymal cells (Figure 4). Cells with morphology consistent with the respiratory tract were not found. The background was bloody.

Given that the aspirate was submitted as a pulmonary mass, a diaphragmatic hernia was considered a leading differential. This would explain finding liver in the chest cavity. However, the mesenchymal cells were perplexing, particularly in light of how cellular the sample was. Given that the cells were incredibly monomorphic, a benign lesion was favored. If associated with the liver, a leiomyoma was considered. Primary hepatic leiomyomas have been documented in a number of species, while documentation of these lesions in the respiratory tract of companion animals is lacking. Extrusion of a primary hepatic leiomyosma through the diaphragm was strongly considered. Alternatively, a smooth muscle tumor could have been originating from the vasculature within the thoracic cavity. A gastrointestinal stromal cell tumor that had traversed the diaphragm was also considered.

Case follow-up:

Additional information was acquired from the submitting veterinarian. There was no imaging evidence of a diaphragmatic hernia. However, the pulmonary mass was reportedly difficult to aspirate and was only visible via transhepatic ultrasound. Thus, the mass was sampled by passing the collection needle through the liver, diaphragm, and presumptively into the pulmonary mass. This method of collection explained the hepatocytes found in the sample, and the large swaths of cells initially thought to be smooth muscle were likely the skeletal muscle of the diaphragm. Interestingly, this skeletal muscle is a little divergent from the rest of the skeletal muscle in the body in terms of its innervation and appearance.

Additional information on leiomyomas:

Smooth muscle tumors are most common in the gastrointestinal and genitourinary tract across all species. In companion animals, the gastrointestinal tract is the most common site due in part to the high rate of spays. However, the smooth muscle cells that comprises the vascular wall of all blood vessels, smooth muscle fibers in the capsules or trabeculae of organs, and ducts that have contractile function, can all give rise to neoplasms. This includes the biliary tract. In the primary literature, leiomyomas have been documented as space-occupying lesions in the pelvic canal, jugular vein, esophagus, and the third eyelid in dogs.1,2,3,4 Primary hepatic leiomyomas have been reported in people and affected patients are typically asymptomatic.5,6 Hepatic leiomyomas have rarely been reported in cattle.7 Leiomyomas originating from the round ligament of the liver have been rarely reported in people.8

In dogs, immunohistochemistry can be employed to differentiated between leiomyomas/sarcomas and gastrointestinal stromal tumors (GIST). This category of tumor can be difficult to classify, with variants in human pathology occasionally termed STUMP lesions (smooth muscle tumor with uncertain malignant potential).9 This aspirate certainly stumped me the first go around!

A more insidious counterpart to benign leiomyomas, disseminated leiomyomatosis, has been documented in the peritoneum of a dog and mare.  Despite the diffuse nature of this variant, the seeded tumors maintain a benign phenotype.10,11 In people, hormonal alterations are thought to contribute to the development of these lesions. Continued growth of the primary or secondary lesions can lead to clinical signs that can ultimately lead to the demise of the affected animal.

Diaphragm is derived from the Greek words “dia” meaning in between, and “phragma” meaning fence. I certainly sat on this fence writing up this report. This is a beautiful example of why it is important to provide pathologists with the most accurate information pertaining to sample, collection methods, and clinical history. We do not, and should not, operate in a black box. This sample did provide a wonderful opportunity to delve into smooth muscle tumors.

Author: Dr. Erica Behling-Kelly

References:

  1. Katamoto H, Kumagai D, Kouzai N, Takigami S, Kuwamura M, Yamate J, et al. Space-occupying leiomyoma in the pelvic canal of a dog. J Small Anim Pract. England; 2003 Jun;44(6):277–9.
  2. Mathes RL, Noble SJ, Ellis AE. Leiomyoma of the third eyelid in a dog. Vol. 19, Veterinary ophthalmology. England; 2016. p. 347–54.
  3. Robin EM, Pey PB, de Fornel-Thibaud P, Moissonnier PHM, Freiche V. Esophageal leiomyoma in a dog causing esophageal distension and treated by transcardial placement of a self-expanding, covered, nitinol esophageal stent. J Am Vet Med Assoc. United States; 2018 Feb;252(3):330–5.
  4. Pierini A, Cinti F, Binanti D, Pisani G. Primary leiomyosarcoma of the jugular vein in a dog. Open Vet J. Libya; 2017;7(1):61–4.
  5. Vyas S, Psica A, Watkins J, Yu D, Davidson B. Primary hepatic leiomyoma: unusual cause of an intrahepatic mass. Ann Transl Med. China; 2015 Apr;3(5):73.
  6. Navarro C, Hamidian Jahromi A, Donato M, Caliri N, Tempra A, Sangster G. Primary Leiomyoma of the Liver: Case Report and Review of the Literature. J La State Med Soc. United States; 2015;167(3):129–33.
  7. Esmaeilzadeh S, Rezaei A, Mazaheri Y. Hepatic leiomyoma in a cow. Vet Rec. 2007;161(12):423–4.
  8. Matito-Diaz MJ, Blanco-Fernandez G, Fernandez-Perez J, Lopez-Guerra D. Leiomyoma of the round ligament of the liver: report of one case. Vol. 107, Revista espanola de enfermedades digestivas : organo oficial de la Sociedad Espanola de Patologia Digestiva. Spain; 2015. p. 644–6.
  9. Tabrizi AD, Ghojazadeh M, Anvar HT, Vahedi A, Naji S, Mostafidi E, et al. Immunohistochemical profile of uterine leiomyoma with bizarre nuclei; Comparison with conventional leiomyoma, smooth muscle tumors of uncertain malignant potential and leiomyosarcoma. Adv Pharm Bull [Internet]. 2015;5(Suppl 1):683–7. Available from: http://dx.doi.org/10.15171/apb.2015.093
  10. Isaac ML, Spaulding KA, Goodrich ZJ. Imaging diagnosis–disseminated peritoneal leiomyomatosis in a dog. Vet Radiol ultrasound Off J Am Coll  Vet Radiol Int Vet Radiol Assoc. England; 2015;56(3):E25-30.
  11. Johnson PJ, Wilson DA, Turk JR, Pace LW, Campbell-Beggs C, Johnson GC. Disseminated peritoneal leiomyomatosis in a horse. J Am Vet Med Assoc 1994;205: 725–728.
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