Fatal Sarcoptes scabiei Infection of Blue Sheep (Pseudois nayaur) in Pakistan Author(s): M. P. Dagleish, Qurban Ali, R. K. Powell, D. Butz, and M. H. Woodford Source: Journal of Wildlife Diseases, 43(3):512-517. Published By: Wildlife Disease Association URL: http://www.bioone.org/doi/full/10.7589/0090-3558-43.3.512

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Journal of Wildlife Diseases, 43(3), 2007, pp. 512–517 # Wildlife Disease Association 2007

Fatal Sarcoptes scabiei Infection of Blue Sheep (Pseudois nayaur) in Pakistan

M. P. Dagleish,1,6 Qurban Ali,2 R. K. Powell,3 D. Butz,4 and M. H. Woodford51Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, Near Edinburgh, EH26 OPZ Scotland, UK; 2 National Veterinary Laboratories, Park Road, Islamabad, Pakistan; 3 Great Bettws Farm, Great Bettws, Abergavenny NP7 7LG, Wales, UK; 4 Brock University, St Catharine’s, Ontario L2S 3A1, Canada; 5 Apdo, 1084, 8100 Loule, Algarve, Portugal; 6 Corresponding author (email: [email protected])

ABSTRACT: Sarcoptes scabiei was detected for Blue sheep (Pseudois nayaur) or ‘‘’’ the first time in skin scrapings, hair pluckings, inhabit the Tibetan plateau including and histologic sections from a blue sheep northeastern Pakistan, the high mountain (Pseudois nayaur) from the Shimshali Pamir in the Karakorum range of the western regions of China, northwestern Nepal, and Himalaya in Pakistan (36u289N, 75u369E). the border between India and China, at Local reports suggest many hundred altitudes of 2,400–6,000 m above sea level have been affected by a severe skin disease over (Wang and Hoffman, 1987). This species a 10-yr period, but the shy nature of this species is well-adapted to life in a high-altitude and the extreme climate that they inhabit mountainous environment in that it has meant only a single affected was avail- able for detailed evaluation. The severe skin physiological modifications in cardiopul- lesions were confined to the forelegs and monary hemodynamics, the ability to exist brisket, and many Sarcoptes scabiei mites were on a diet of sparse graminoids and herbs, present in all the samples examined. Histologic and exceptional agility on steep rocky preparations of the skin showed hyperkeratotic terrain (Wang and Hoffman, 1987; Sakai and parakeratotic hyperkeratosis of the epider- mis with a severe exudative dermatosis with et al., 2003; Mishra et al., 2004). Blue many polymorphonuclear neutrophils and sheep are classified as ‘‘Least Concern’’ in gram-positive cocci, yet no eosinophils. These the IUCN Red List of Threatened Species findings might suggest the lack of an appropri- (Harris, 2003) and are a primary source of ate immune response to the parasite or other prey for the snow leopard (Panthera coping strategies because there has been no abatement of the clinical signs in affected uncial; Fox et al., 1991). Western hunters animals over several years. Treatment options consider blue sheep to be trophy animals are limited due to the behavior of the species with their large horns and also because and its habitat. The blue sheep is a primary they reside in remote areas near pre- source of prey for the endangered snow leopard cipitous cliffs (which they can descend (Panthera uncia) and continued depletion rapidly when approached to avoid pre- could have serious consequences for the survival of the latter. dation), making them difficult to hunt. Key words: Blue sheep, Pseudois nayaur, They are important both in the conserva- Sarcoptes scabiei, scabies, skin disease. tion of the highly endangered snow leopard and as a potential source of Sarcoptic mange, or scabies, is a highly income through trophy hunting for local contagious parasitic skin disease caused by people, including the inhabitants of the Sarcoptes scabiei, a mite that infects Shimshali Pamir in the Karakorum range domestic and wild animals as well as of the western Himalaya (36u289N, humans (Fain, 1968, 1978). This species 75u369E). As such, they are not considered of mite has been divided into morpholog- to be unwanted competition for their 5,000 ically indistinguishable host-adapted vari- domestic sheep and plus the 1,000 eties which rarely cross-infect between , which share the same high altitude different species of animals, yet most will grazing during the summer months. parasitize humans. However, they fail to From 1996, Shimshali herders complete their life cycle when man is an reported finding increasing numbers of aberrant host (Yager and Scott, 1993). dead blue sheep in poor condition with

512 SHORT COMMUNICATIONS 513 considerable numbers of skin lesions, brisket (Fig. 1). The affected skin con- especially on the forelegs and chest, and tained areas of excoriation, presumably live affected individuals that did not from self trauma, and deep fissures. No attempt to flee when approached. During gross abnormalities were found in the rest early summer 2000 an estimated ‘‘several of the organs examined. hundred’’ carcasses were present in the Many mites were present in both the area of the Shimshali Pamir used for deep skin scrapings and plucked hair summer grazing of local domestic stock. preparations, all of which were identified However, the disease appeared not to be as Sarcoptes scabiei by morphologic crite- seasonal and affected both sexes and all ria such as a globose body, eight short legs age groups of the blue sheep. In response (third and fourth pairs not projecting to this emerging problem, assistance was beyond the body margin), and dorsal requested to investigate these deaths. triangular scales (Fig. 1). Despite some Because it was not possible to transport freeze/thaw damage from storage in the an affected carcass to the village, a local glacier, histologic examination showed herder shot an affected animal (male, hyperkeratotic and parakeratotic hyper- approximately 3 yr old) showing the keratosis of the epidermis. A severe typically described lesions and buried it exudative dermatosis was present as de- in a glacier so it would be readily available noted by a large infiltration of polymor- for postmortem examination by veterinar- phonuclear neutrophils, many of which ians when they had completed the lengthy appeared degenerate (Fig. 2) and were and difficult journey to reach the plateau. frequently associated with multiple gram- Gross postmortem examination was per- positive cocci. Interstitial serum, mono- formed in the field after the carcass had nuclear inflammatory cells, and nuclear been dug out of the ice and thawed. Deep debris were also present. A similar mixed skin scrapings for ectoparasite investiga- inflammatory cell response was present in tion and full thickness skin samples were the dermis along with nuclear debris. taken for histopathology, and both were Multiple parasite profiles were present stored in 10% formal saline. Identification deep within the hyperplastic epidermis in of parasites was done by examination of pockets lined with parakeratotic stratum morphological characters (Soulsby, 1986) corneum. The parasite profiles were of after mounting skin scrapings on glass variable shape due to differing planes of microscope slides. Histologic examination section, yet the prominent triangular of skin samples was performed after scales characteristic of Sarcoptes scabiei routine processing; briefly, samples were were visible on one aspect of most profiles dehydrated through graded alcohols, em- (Fig. 2). A diagnosis of scabies was made bedded in paraffin-wax to enable 5-mm- on the basis of these findings. thick sections to be cut and mounted on We believe this is the first reported glass microscope slides, and stained with incidence of scabies in blue sheep. The either hematoxylin and eosin or Gram’s distribution and severity of the skin lesions stain. Plucked hairs from the formal- in this case were extreme and not typical of saline-fixed full thickness skin samples that described in domestic sheep, in which were also examined for ectoparasites after primarily the lips, nostrils, external surfaces mounting on glass microscope slides. of the pinnae, and occasionally the legs are Gross postmortem examination con- involved; in this case, the face appeared to firmed that the carcass was emaciated. have been spared, yet the whole antebra- Alopecia, marked lichenification, and chium and a large area of the brisket were a thick grey scaling crust was present on affected (Yager and Scott, 1993). In a severe the surface of both forelegs from the scabies outbreak affecting the free-ranging elbows to the carpi, both axillae, and the (Ammotragus lervia, a wild 514 JOURNAL OF WILDLIFE DISEASES, VOL. 43, NO. 3, JULY 2007

FIGURE 1. Forelegs and brisket of the affected blue sheep. Note alopecia, marked lichenification and grey scaling crust present on the surfaces of both forelegs from the elbows to the carpi, both axillae, and the brisket. Insert: mite recovered from plucked hair preparation with morphology typical of Sarcoptes scabiei. sheepadaptedtomountainterrainin on the forelegs and brisket and only one North Africa) following their introduction sheep had lesions on a hind limb (Gonza- to the Sierra Espun˜ a Regional Park in lez-Candela et al., 2004). However, gener- Spain, there was a total absence of lesions alized scabies lesions have been reported in SHORT COMMUNICATIONS 515

FIGURE 2. Severe scabies infestation in the skin. Note the disruption to the normal architecture of the epidermis and the inflammatory infiltrate in both the epidermis (arrow heads) and scattered throughout the dermis (arrow). Insert: higher magnification of same field showing parasite profiles (arrow heads) deep within the hyperplastic epidermis in pockets. Hematoxylin and eosin. the more hairy desert sheep of the Sudan nourished or those with debilitating co- (Ibrahim and Abu-Samra, 1987) and also in existing disease (Yager and Scott, 1993). goats, although the head is still the pre- However, because this species has not ferred site (Yager and Scott, 1993). This been thoroughly studied, there might be apparent anomaly in lesion distribution differences in the patterns of cellular might partly be due to the evolutionary infiltration compared with domestic sheep misclassification of blue sheep. Most recent and goats. In addition, the bacterial in- studies, including behavioral, genetic, and fection and the presence of neutrophils biochemical evidence, now consider the might represent a time frame dominated blue sheep is probably a primitive with by the bacterial aspect of the complex. some convergent sheep-like characteristics We were unable to find any apparent (Schaller, 1977). concurrent disease in the animal available The presence of large numbers of mites for study to explain the pattern of the in the skin scrapings and plucked hair lesions, although introduction of a novel samples, the severe crusting dermatosis, disease into any naı¨ve population might deep fissures, extent of the lesions, and result in severe lesions and a high mortal- absence of any eosinophils in the tissue ity rate similar to that of the scabies samples suggests the possibility of a weak outbreak in the Barbary sheep (Gonza- or nonexistent hypersensitivity response to lez-Candela et al., 2004). Furthermore, the parasite. In domestic animals this form free-living animals in an extreme climate, of scabies is characteristic of the poorly such as the high Tibetan plateau, where 516 JOURNAL OF WILDLIFE DISEASES, VOL. 43, NO. 3, JULY 2007 food is sparse might be in constant threat former suffered a population decrease of of nutritional deficit. Protein/calorie mal- 86% over a 5-yr period (Gonzalez-Candela nutrition has been repeatedly shown to et al., 2004). In this case it is perhaps adversely affect how sheep react to pertinent that the sheep had been in- parasite challenge (Coop and Kyriazakis, troduced into a foreign habitat within 1999) and could be a significant factor in a fenced nature reserve with a limited food the clinical presentation of scabies in blue supply. Prior to the scabies epidemic, the sheep. To compound this, as intense Barbary sheep population had increased pruritus develops, animals spend less time steadily over a 17-yr period to a level that feeding, which can further exacerbate any was probably unsustainable. nutritional shortfall. From an evolutionary Whatever the original source of the perspective it is unlikely that herbivorous scabies infection in the blue sheep 10 yr animals, adapted to an extreme cold after the initial reports of dead animals, the environment with very low relative hu- consequences appear to be severe, not only midity such as that of the rock- and snow- for the survival of the species itself but covered high Tibetan plateau, would have potentially also for other species such as the been exposed to the common ecto- and snow leopard, which relies on them as their endoparasites we associate with domestic primary food source. Treatment options for in temperate and tropical cli- the blue sheep are somewhat limited due to mates. As such, they might not have their shy nature, dispersal over a huge evolved immunologic or other strategies, range which crosses several international such as partitioning of limited nutritional boundaries, and lack of any effective resources (Coop and Kyriazakis, 1999), to vaccine against Sarcoptes scabiei (Tarigan effectively deal with such a challenge. and Huntley, 2004). There appears to have The source of the initial infection in the been little, if any, obvious host adaptation blue sheep remains uncertain because no to the parasite over the period of the clinical signs of scabies were observed in outbreak or selection of animals that are local domestic animals at the time of this more tolerant, but further investigation is investigation. More recent observations of required to confirm this and the extent of local domestic stock suggests the presence the change in the population plus its intra- of low-grade scabies, and detailed ques- and interspecies dynamics. tioning of the older shepherds suggests this The authors would like to thank Inayat might have been present prior to 1996 Ali, Idabat Ali, the Shimshal Nature Trust, when affected blue sheep were first noticed and the Aga Khan Rural Support Project (M. H. Woodford and R. K. Powell, pers. (AKRSP) for their assistance gaining obs.). However, the gregarious social be- access to the affected blue sheep and havior of blue sheep, with individuals and Clare Underwood (Moredun Research groups constantly varying between two to Institute) for preparation of plucked hair 400 animals (Wang and Hoffman, 1987) samples and histologic sections. We are moving across the Tibetan Plateau irre- also grateful to Frank Jackson and David spective of national boundaries, is likely to Buxton for their constructive criticism of be significant in the spread of the disease. this manuscript. This study was generously We believe the most likely source of the supported by the Wildlife Conservation infection would have been from domestic Society, New York and the Bill Jordan livestock from any one of the several Foundation for Wildlife. countries having territory within the Tibet- an Plateau. This might be a similar situation LITERATURE CITED to the scabies epidemic in free-ranging COOP, R. L., AND I. KYRIAZAKIS. 1999. Nutrition- Barbary sheep where the infection was parasite interaction. Veterinary Parasitology 84: from local domestic goats in which the 187–204. SHORT COMMUNICATIONS 517

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