Signalment:  

13-year-old male, castrated, warmblooded horse (Equus caballus).The owner noted two masses on the inside of the prepuce that have been present for two months and are rapidly growing.


Gross Description:  

There are two pieces of non-haired skin that are disrupted by a central tan, firm, nodule, measuring 2 x 1.5 x 1 cm in one piece, and 11 x 11 x 8 mm in the other.


Histopathologic Description:

Prepuce: The dermis is markedly expanded by large, dense, nodular aggregates of lymphocytes and plasma cells containing multiple smaller dense aggregates of epithelioid macrophages and multinucleated giant cells, with fewer scattered eosinophils. Multifocally within the inflammatory aggregates and frequently surrounded by macrophages and giant cells are cross-sections of nematodes, ranging up to 15 μm in diameter. These have a very thin cuticle, with low, indistinct platymyarian-meromyerian musculature, a pointed tail, numerous deeply basophilic 2-3 μm internal structures, and an esophagus with a prominent corpus, isthmus, and bulb (rhabditiform esophagus). There are moderate numbers of lymphocytes and plasma cells and fewer eosinophils scattered throughout the dermis surrounding the nodule. There is marked epidermal hyperplasia with compact hyperkeratosis overlying the nodule.


Morphologic Diagnosis:  

Posthitis, lymphoplasmacytic, eosinophilic, and granulomatous, severe, chronic, multifocal, with intralesional rhabditiform nematodes


Condition:  

Posthitis, granulomatous


Contributor Comment:  

Halicephalobus gingivalis (formerly known as Micronema deletrix or Halicephalobus delatrix) is a free-living rhabditiform nematode. Infections in horses are infrequently reported; when found, organisms typically infiltrate the central nervous system,(2,3) but have also been reported in the prepuce,(4,10) kidney,(1,15) eye,(11) bone,(5) and one case of systemic infection.(13) In addition to Halicephalobus, other free-living rhabditoid nematotes, such as the genus Cephalobus (6) and Pelodera,(12) have been reported to cause skin infections in horses, and cannot be ruled out in this case. In addition to horses, other equids, such as zebras, have also been reported to be infected.(8)

To date, only female Halicephalobus have been found in tissue samples.(10) While the route of infection and pathogenesis of disease are poorly understood, it is suspected that the organism gains entry via existing wounds. In some cases, viable Halicephalobus organisms have been detected in sperm and urine;(9) while no transmission via this route has been proven, it is another possible source of infection. Organisms access the central nervous system via blood vessels, and cause necrosis and inflammation due to migration through the tissue.

Under light microscopy, adult females are typically approximately 20 μm in diameter and 350 μm long, with a thin, smooth cuticle and tapered, pointed tail. They have platymyarian-meromyarian musculature, a rhabditiform esophagus, and an intestine lined by low cuboidal cells. Larvae are approximately 10 μm in diameter, with tapered, pointed tails. Typically, tissue sections have numerous parasites; this may be explained by the fact that females are parthenogenetic and thus can produce offspring in the absence of males.

Other rule outs for rhabditoid parasites in tissue sections include Cephalobus spp., Strongyloides westeri, and Pelodera strongyloides.(12) Cephalobus spp. can be differentiated from Halicephalobus spp. by examination of the tail, which is blunt in Cephalobus.(6) Strongyloides westeri have alae, which Halicephalobus spp. lack.(6) Pelodera strongyloides also have two lateral alae, as well as two lateral cords noted by two densi nuclei.(7)


JPC Diagnosis:  

Glabrous skin, prepuce: Posthitis, granulomatous and eosinophilic, focally extensive, marked with rhabditiform nematode adults, larvae and eggs, etiology consistent with Halicephalobus gingivalis.


Conference Comment:  

The contributor provides an excellent overview of halicephalobiasis in the horse. Most conference participants correctly identified the nematode as H. gingivalis, though some participants identified the tissue as gingiva rather than skin from the prepuce. As H. gingivalis causes granulomatous inflammation at both anatomic locations, tissue identification is important. Upon closer examination of the tissue sample, all participants subsequently identified scattered sebaceous and apocrine glands, and some sections contain rare hair follicles, consistent with glabrous skin. Conference participants also reviewed the differential diagnosis for this lesion, which the contributor discusses in detail. In addition to the morphologic features provided by the contributor, the moderator commented that a unique anatomic feature of H. gingivalis is the presence of a dorsally reflexed ovary, which is often difficult to appreciate on routine histologic examination, but when present is diagnostic.

In addition to the histomorphologic differences among the various nematodes, clinicopathologic presentation may assist with differentiating them. Although H. gingivalis dermatitis may occur anywhere on the skin of horses, it generally localizes near or on the prepuce; lesions tend to be papules or nodules that are well circumscribed, measure 0.5 cm to 8 cm in diameter, and are often ulcerated.(14) In contrast, Pelodera dermatitis is characterized by papules, pustules, ulcers, crusts, alopecia, and scales on areas of the skin that typically have contact with damp soil and decaying organic matter, such as the limbs, ventral thorax, and abdomen;(14) pruritis is usually moderate to intense.

We thank Dr. Christopher Gardiner, Consulting Parasitologist for the AFIPs Department of Veterinary Pathology, for his study and diagnostic commentary for this case.


References:

1. Akagami M, Shibahara T, Yoshiga T, et al. Granulomatous nephritis and meningoencephalomyelitis caused by Halicephalobus gingivalis in a pony gelding. J Vet Med Sci 2007;69:1187-1190
2. Bryant U, Lyons E, Bain F, Hong C. Halicephalobus gingivalis-associated meningoencephalitis in a Thoroughbred foal. J Vet Diagn Invest. 2006;18:612-615.
3. Br+â-¦jer J, Parsons D, Linder K, Peregrine A, Dobson H. Halicephalobus gingivalis encephalomyelitis in a horse. Can Vet J. 2000;41:559-561.
4. Dunn D, Gardiner C, Dralle K, Thilsted J. Nodular granulomatous posthitis caused by Halicephalobus (syn. Micronema) sp. in a horse. Vet Pathol. 1993;30:207-208.
5. Ferguson R, van Dreumel T, Keystone J, et al. Unsuccessful treatment of a horse with mandibular granulomatous osteomyelitis due to Halicephalobus gingivalis. Can Vet J. 2008;49:1099-1103.
6. Greiner E, Mays M, Smart GJ, Weisbrode S. Verminous mastitis in a mare caused by a free-living nematode. J Parasitol. 1991;77:320-322.
7. Gutierrez Y. Diagnostic Pathology of Parasitic Infections with Clinical Correlations. 2nd ed. New York, NY: Oxford University Press; 2000:307.
8. Isaza R, Schiller C, Stover J, Smith P, Greiner E. Halicephalobus gingivalis (Nematoda) infection in a Grevy's zebra (Equus grevyi). J Zoo Wildl Med. 2000;31:77-81.
9. Kinde H, Mathews M, Ash L, St Leger J. Halicephalobus gingivalis (H. deletrix) infection in two horses in southern California. J Vet Diagn Invest. 2000;12:162-165.
10.Muller S, Grzybowski M, Sager H, Bornand V, Brehm W. A nodular granulomatous posthitis caused by Halicephalobus spp. in a horse. Vet Dermatol. 2008;19:44-48.
11.Rames D, Miller D, Barthel R, et al. Ocular Halicephalobus (syn. Micronema) deletrix in a horse. Vet Pathol. 1995;32:540-542.
12.Rashmir-Raven A, Black S, Rickard L, Akin M. Papillomatous pastern dermatitis with spirochetes and Pelodera strongyloides in a Tennessee Walking Horse. J Vet Diagn Invest. 2000;12:287-291.
13.Ruggles A, Beech J, Gillette D, Midla L, Reef V, Freeman D. Disseminated Halicephalobus deletrix infection in a horse. J Am Vet Med Assoc. 1993;203:550-552.
14.Scott DW, Miller WH, Jr. Equine Dermatology. St. Louis, MO: Elsevier Ltd; 2003:366-369.
15.Shibahara T, Takai H, Shimizu C, Ishikawa Y, Kadota K. Equine renal granuloma caused by Halicephalobus species. Vet Rec. 2002;151:672-674.


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2-1. Glabrous skin, prepuce


2-2 . Glabrous skin, prepuce



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