Abstract
Introduction
Many captive animals show forms of pelage loss that are absent in wild or free-living conspecifics, which result from grooming or plucking behavior directed at themselves or at other individuals. For instance, dorsal hair loss in primates results from excessive hair-pulling or over-grooming by cage-mates. Occasionally this behavior appears to be associated with stress;8 however, captive non-human primates frequently suffer from sarcoptic mange,5 psorergatic mange (caused by Psoralgidae mites), and pulmonary acariasis due to lung mites (Pneumonyssus spp.).4,9,10 The pathogenesis and concordant clinical symptoms of mange might depend on the immune status of the host. Naïve, immunocompromised, or anergic animals that are unable to evoke hypersensitivity responses might develop an extensive epidermal hyperkeratosis with a chronic dermal inflammation.2 The following case reports describe an unusual dermatologic disease and its regression in two hand-reared, young chimpanzees (Pan troglodytes) at Parco Natura Viva, Garda Zoological Park, Italy.
Case Report
Over a period of the last 2 years, two young hand-reared chimpanzees (one male and one female) showed a particular form of complete pruriginous alopecia spread over the whole body. The female is an 8-year-old female chimpanzee. She was hand-reared in a human family context for the first year of her life and after that period she was housed alone for 2 years in the chimpanzee enclosure at Parco Natura Viva, Garda Zoological Park, Italy. When she was 3 years old, her brother was housed with her in the same enclosure for 1 year, and then two other young hand-reared chimpanzees were put in the enclosure.
The chimpanzee enclosure had two different areas: an outside area and an inside one with four different cages. The small group of four young chimpanzees was housed in the biggest round cage, whereas the adult group was housed in the other three cages and the outside area. The juvenile chimpanzees were allowed into the outside area for a few hours each day while the adults were kept inside.
Over the first 3 years, the female had no clinical problems, and her development was normal except for a localized dermatitis on hands and feet which was resolved with antimycotics (itraconazole). However, when she was 4 years old, she developed a pruriginous dermatitis on her back that spread rapidly over her whole body. Initially the problem was thought to be a parasitic infection of a simple food allergy and was treated with ivermectin PO and antihistamine at the human dose. No clinical improvement was seen. During this time, her brother started to present with similar pruritus and dermatologic problems. In September 2003, the skin condition worsened in both chimpanzees. Clinical signs progressed to depigmentation, depilations, round erosions/ulcers, crusty keratin flakes and papules. Antibiotic treatment (Clavamox 25 mg/kg) for a pyodermatitis was initiated but was ineffective. Corticosteroids were also prescribed and seemed to improve the pruritus. After 3 months, treatment was discontinued, and the chimpanzees started to scratch again.
Herpetiform dermatitis caused by a food allergy to gluten was considered as a differential diagnosis as it has been reported in humans.13 Gluten was removed from the diet for 1 month, but no clinical improvement was seen. Repeated skin scrapings and fecal examinations were negative throughout the treatment period.
In January 2004, treatment with doramectin (Dectomax®) PO once per week for 2 months was initiated. In January 2004, the chimpanzees were anesthetized, and blood was collected for viral and hematologic tests and skin biopsies performed. All results were within normal limits. Tests were negative for the simian T-lymphotropic virus (STLV), SIV and Herpesvirus. Moreover, serologic examination for Leishmania was negative.
The biopsy results were dermatitis perivascular superficial comprising eosinophilic granulocyte associated to hyperkeratosis of the epidermis. Since the contact allergy could not be ruled out by the biopsy the straw was removed from the inner enclosure from the beginning of July 2004. In August 2004, we performed a second biopsy on all four chimpanzees in the group: that revealed for two of them (the brother and sister described here) chronic hyperplastic and hyperkeratotic perivascular dermatitis with focal band like/interface dermatitis in the female and with minimal eosinophilic infiltration in the male. It is important to underline that even if mites and/or eosinophilic infiltration were not found in the biopsy, scabies could not totally be ruled out.
The following differential diagnoses had to be considered: atopy, psychogenic dermatitis, food allergy, drug reaction. In October 2004 the chimpanzees were anesthetized for the third time in order to perform serologic RAST test and PRICK test to check any food, inhalation and contact allergy. The RAST test is an allergen-specific IgE antigen test to screen for an allergy (a type I hypersensitivity) to a specific substance or substances. The PRICK test is used to identify the causative allergens in an atopic individual. The test depends on the introduction of allergen extract into the dermis resulting in an IgE-mediated response that looks like a local erythema and skin swelling. A skin culture was also performed. The female was positive for Staphylococcus aureus and a hemolytic bacillus whereas the male was positive for Klebsiella pneumoniae; both were negative for mycotic culture and Enterobacteriacae. The Prick allergic test revealed a high reaction to milk and milk byproducts and RAST test showed sensitivity to some vegetables (pineapple, tomato, apricot, peer, grapefruit), peanuts, nuts, almonds and also rice, bread and milk. According to these results the diet of the two young chimpanzees was changed and the above food items were avoided. Anti-inflammatory or antihistaminic drugs were given when serious episodes of pruritus occurred. Even with these treatments, the clinical picture did not improve. In spring 2005 the two chimpanzees and two other young chimpanzees were introduced into the group of eight adult individuals. The introduction of the two chimpanzees was slow especially because they had already exhibited some stereotypic behaviors (finger sucking, rocking, etc.) related to problems with their earlier care. After that, they developed a strong bond with one of the keepers who was with them for the last 4 years. In general, hand-reared chimpanzees form a strong bond with their human caregiver that substitutes for the natural mother.7 Once the introduction was complete, the pruritis and other clinical symptoms decreased and then disappeared. The skin lesions resolved as well. Currently, the alopecia has completely regressed, and the two chimpanzees are fully haired.
Discussion
This case report demonstrates the possibility that factors other than the traditional parasitic causes can be involved in severe, chronic pruritus and alopecia in chimpanzees. Once introduced into the group of adults, not only were the other chimpanzees not infected, but also the disease of the two chimpanzees disappeared. The facts strongly suggest the existence of factors (prior or concurrent to mite infestation) that predisposed these chimpanzees to scabies and allowed the progression of the disease. Predisposing factors in children include neurologic and immunologic disorders, psoriasis, and various diseases (including parasitoses) that result in immunosuppression, (i.e., measles, pneumocystosis, candidiasis).1,2,11 Furthermore, in immunocompetent and immunocompromised children, topical therapy usually fails to cure crusted scabies.6,11 As young chimpanzees are highly social, the experience of abandon and isolation had made the chimpanzees’ psychologic development complicated and difficult. This is supported by the fact that their disease was solved only when they were introduced into the group of adults in a social context. In conclusion, our data suggest that alopecia in chimpanzees could be a highly complex multifactorial disorder.
Acknowledgments
We thank Donata Grassi and Caterina Spiezio for providing their expertise in chimpanzees behaviour; Maria and Ruth for their dedication to the chimpanzees and for telling us Camilla and Tommy’s story.
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