Introduction
Pox viruses cause disease in a wide range of mammals, birds and reptiles. The six genera of pox viruses known to infect mammals include: Orthopoxvirus (mouse pox, rabbit pox, horse pox, cow pox, elephant pox, many others); Parapoxvirus (contagious ecthyma, seal pox, red squirrel pox, others); Capripoxvirus (goat pox, others); Leporipoxvirus (hare fibroma, myxomatosis, squirrel fibroma, others); Suipoxvirus (pigs), Yatapoxvirus (primate tanapox); and Molluscipoxvirus (human molluscum contagiosum).6,8 A seventh genus contains several unassigned viruses including cetacean pox virus, gray kangaroo pox, molluscum-like virus of horses, mule deer pox and others.6,8 Marennikova, et al. (1976) described fatal pox virus infection in two giant anteaters with severe rash, vesicular dermatitis and pulmonary infection.4 The virus isolated from these anteaters was similar to cowpox virus (genus: Orthopoxvirus).4
Molluscum contagiosum is a disease of humans characterized by proliferative cutaneous lesions in children and adults. Children are infected by close contact or fomite inoculation. In adults, molluscum contagiosum is a sexually transmitted disease that is seen with increased incidence in immunosuppressed individuals (i.e., HIV infection or chemotherapy patients). Skin lesions due to molluscum contagiosum are clinically recognized as small slightly raised umbilicated lesions on the face, limbs or trunk. Histologically, the skin lesions are characterized by endophytic nodular hyperplasia of the epidermis. Large eosinophilic cytoplasmic inclusions (molluscum bodies) compress the nucleus to the periphery of infected keratinocytes. In this report, we describe cutaneous pox virus infection in two giant anteaters (Myrmecophaga tridactyla) with clinical and histopathologic lesions resembling those seen in molluscum contagiosum of humans.
Case Report
Anteater #1
An adult female giant anteater was treated over an 8-month period for cutaneous Mycobacterium sp. infection in the inguinal region. During one of the surgical procedures performed to treat the mycobacterial infection, an area of roughened and irregular skin was noted on the lateral cervical region cranial to the right shoulder. Two 4-mm punch biopsies from this region were submitted in 10% neutral buffered formalin for histopathologic examination. The anteater was euthanatized several weeks later due to uncontrolled spread of the mycobacterial infection. At necropsy, close examination of the previously biopsied site on the lateral cervical region revealed numerous small (2–4 mm diameter) slightly raised nodular lesions. In many areas the lesions were confluent with each other, giving the skin the roughened texture that was described clinically. Examination of the lesions under a 10x magnifying lamp revealed many of the lesions had a small umbilicated central region. Several lesions were placed in formalin for histopathologic examination.
Anteater #2
Following the diagnosis, treatment and euthanasia of the female anteater described above, an adult male anteater was immobilized for complete physical examination. Several raised cutaneous lesions were discovered on the caudal palmer surface of both right and left front feet. These lesions were pale tan in color and measured 2–3 mm in diameter. The lesions occurred individually or in small groups of 2–3 nodules. Punch biopsies of two lesions were submitted in formalin for histopathology. Examination of the submitted lesions under a 10x magnifying lamp revealed one of the two lesions had a small umbilicated central region. At the time of preparation of this abstract, numerous cutaneous lesions remain on the palmar surface of both front feet. Rare lesions are also present on the hind feet.
Microscopic Examination
The histopathologic characteristics in the skin lesions submitted at all time periods from both anteaters were similar. The epidermis was diffusely irregularly hyperplastic and was covered by a thick, dense layer of orthokeratotic keratin. In multifocal areas there was marked endophytic hyperplasia of the epidermis, forming a multilobular intradermal mass. The lobules comprising the mass were separated by thin bands of dermal collagen. The lobules of hyperplastic epidermis were characterized by a central core of enlarged (20–30-micron diameter) round to oval eosinophilic keratinocytes. This core of enlarged keratinocytes was surrounded by a rim of normal appearing keratinocytes resembling those of the stratum basale. Scattered hyperplastic lobules had a central core of keratin and degenerate keratinocytes. Keratinocytes comprising the center of hyperplastic lobules contained large (10–20-micron diameter) hypereosinophilic intracytoplasmic inclusions that occupied the majority of the cytoplasm and displaced the nucleus to the periphery of the cell. Similar inclusions were also present within degenerate keratinocytes intermixed with keratin at the center of hyperplastic lobules and on the epidermal surface. Dermal inflammation was present in any of the lesions examined.
Electron Microscopy
Transmission electron microscopy revealed large numbers of brick-shaped pox virus particles within the cytoplasm of keratinocytes that contained eosinophilic intracytoplasmic inclusions on histopathology. These pox virus particles measured approximately 200 nm in length and contained the characteristic “hourglass” central core. The nucleus of infected cells was displaced to the periphery of the cell. Cellular changes associated with pox virus infection included mild vacuolization of the cytoplasm and swelling of the nuclear membrane.
Discussion
Benign cutaneous pox virus infection has not been previously reported in giant anteaters. The clinical presentation and pathologic lesions seen in these two giant anteaters differ greatly from a previous report of fatal systemic cowpox infection in two giant anteaters from the Moscow Zoo.4 In that report, cutaneous lesions of pox virus infection were described as a severe rash and a hemorrhagic vesicular dermatitis that was intensely pruritic. Cutaneous lesions in the two anteaters reported here consisted of small benign umbilicated nodules that were discovered as incidental findings during treatment for a separate disease process or during a routine physical examination. These nodules do not seem to cause any discomfort or pruritis in the currently infected anteater, and there was no evidence of systemic spread of the pox virus infection in the anteater that was necropsied following euthanasia for cutaneous mycobacterial infection. Efforts are underway to isolate and grow the pox virus responsible for the cutaneous lesions reported here. We believe the pox virus responsible for the lesions in these two anteaters is a different virus than the cowpox virus believed to be responsible for the deaths at the Moscow Zoo.
A unique finding in the lesions examined from these two anteaters was the consistent presence of endophytic hyperplasia of the epidermis associated with pox virus infection. In authors’ experience and in most reported cases, lesions associated with pox virus infection are nodular exophytic masses. The endophytic nature of the cutaneous pox lesions in these cases is similar to the lesions described in the human disease, molluscum contagiosum. Molluscum contagiosum has never been experimentally transmitted to animals and only a few cases of “molluscum contagiosum-like disease” have been reported.7,9 Reports of molluscum contagiosum-like disease include those from horses, chimpanzees and a red kangaroo.1,3,10 Cases of molluscum contagiosum-like disease were diagnosed in those species based on clinical signs and histopathologic lesions similar to the human disease. The pox virus responsible for molluscum contagiosum-like disease in horses has been demonstrated by in situ hybridization to be closely related to the human molluscum contagiosum virus and the possibility of cross-species transmission of molluscum contagiosum virus has been discussed.9
Molluscum contagiosum of adult humans and the molluscum contagiosum-like disease of adult horses are diseases that are often seen in association with immunosuppression.2,5,9 One of the two pox virus-infected anteaters (case #1) was concurrently infected with Mycobacterium fortuitum. It is suspected that the severe granulomatous inflammatory process present associated with the mycobacterial infection may have led to immunosuppression that predisposed this anteater to pox virus infection. An obvious predisposing condition has not been discovered for the infected male anteater (case #2), although the stress of captivity could play a minor immunosuppressive role.
In this report, we have described two cases of molluscum contagiosum-like disease in giant anteaters. Efforts to further characterize the virus by molecular methods are underway at this writing. Those molecular results will help us classify this disease as another report of molluscum contagiosum-like disease or as another example of possible cross species transmission of the molluscum contagiosum virus.
The prevalence of pox virus infection/disease in captive giant anteaters is unknown. Detailed examination of the skin may be required for diagnosis of this subtle disease. Definitive diagnosis is easily made by skin biopsy and histopathology. Treatment has not been attempted with the currently infected anteater.
Literature Cited
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