Abstract
Although neglected, the mite Sarcoptes scabiei is an unpredictable emerging parasite, threatening human and animal health globally. In this paper we report the first fatal outbreak of sarcoptic mange in the endangered Himalayan lynx (Lynx lynx isabellinus) from Pakistan. A 10-year-old male Himalayan lynx was found in a miserable condition with severe crusted lesions in Chitral District, and immediately died. Post-mortem examination determined high S. scabiei density (1309 mites/cm2 skin). It is most probably a genuine emergence, resulting from a new incidence due to the host-taxon derived or prey-to-predator cross-infestation hypotheses, and less probable to be apparent emergence resulting from increased infection in the Himalayan lynx population. This is an alarming situation for the conservation of this already threatened population, which demands surveillance for early detection and eventually rescue and treatment of the affected Himalayan lynx.
Keywords: Sarcoptes scabiei, Lynx lynx isabellinus, Human-lynx conflict, Chitral District, Pakistan, Neglected parasite, Emerging disease
Letter to the editor
Although affecting more than 100 species of mammals worldwide [1, 2], the epidemiology of Sarcoptes scabiei is still not well understood, with differences between locations and host species [3]. The emerging of S. scabiei is frightening, since it may entail devastating mortality in wild and domestic animals, even only from the introduction of a single case [4, 5]. Sudden outbreaks of S. scabiei in human, wild and domestic populations have frequently been reported [6]; nevertheless, there is no report of S. scabiei infestations in the Turkestan subspecies of the Eurasian lynx, also named Himalayan lynx (Lynx lynx isabellinus).
The Himalayan lynx in the Hindu Kush mountain range of the District Chitral, Pakistan (Fig. 1), is highly threatened. The last population assessment reported sporadic occurrence with a minimum of six individuals [7]. The prime threats to the existence of the Himalayan lynx are retaliatory killing because of human-lynx conflict, loss of natural prey-base and loss of habitat to a lesser extent [8].
Fig. 1.

Map of Pakistan showing the site where the mange-infested Himalayan lynx was found
On the 26th of March 2016, a 10-year-old male Himalayan lynx was found by villagers of Karimabad, while in a miserable condition, with severe crusted lesions on the lower limbs (Fig. 2). Although immediately transported by field staff of the Snow Leopard Foundation, to the Animal Hospital in Chitral City, the lynx died before treatment was started. Deep skin scrapings were collected and examined following KOH clearing [9] (Fig. 3).
Fig. 2.

Carcass of the mange-infested Himalayan lynx showing severe crusted lesions
Fig. 3.

Adult Sarcoptes mite taken from the skin scraping of the dead Himalayan lynx
This is the first report of fatal outbreak of sarcoptic mange in the Himalayan lynx (Lynx lynx isabellinus) from Pakistan. A high Sarcoptes mite density was detected (1309 mites/cm2 skin), with prevailing larval stages. We considered two hypotheses, which could explain the origin of the outbreak.
Hypothesis (i): The outbreak is ‘genuine’ emergence of an infestation, which is new to the Himalayan lynx population. Likely sources could be other carnivores sharing habitat with the Himalayan lynx, such as wolf, snow leopard, jackal, fox and leopard cat, according to the host-taxon derived hypothesis [10]. While in nearby Central Karakhoram National Park, Gilgit-Baltistan, one of the Authors (LR, unpublished) collected photo trap evidence that scabies was present among red foxes (Vulpes vulpes). In western Mongolia numerous reports have been made of a debilitating mange-like affliction in the snow leopard (Uncia uncia); however no skin samples have been collected [11]. Similarly, a mange-like condition was observed (though not laboratory confirmed) in a snow leopard captured near Skardu, Gilgit-Baltistan [12]. In Scandinavia and Switzerland, deadly sarcoptic mange in Eurasian lynx has been associated to epidemic or endemic disease in the sympatric abundant red fox populations [13]. Other putative sources are infested domestic animals, through prey-to-predator cross-infestation [14]. Livestock, especially lambs and kids, are major victims of lynx attacks [8]. Most households of the community hold small herds composed of one or two cattle and ten to fifteen sheep and goats. During summer domestic animals are taken to alpine pastures for grazing, and are more vulnerable to predation by lynx. Sarcoptic mange is widespread amongst small domestic ruminants in Pakistan [15].
Hypothesis (ii): It is ‘apparent’ emergence/re-emergence, where Sarcoptes infestation was pre-existing, and the new recognition is a result of increased detection opportunities [7].
This is the first Sarcoptes mite infection case report in the Himalayan lynx population from Pakistan. This is an alarming situation for the conservation of the already threatened population of this species, which demands surveillance for early detection and eventually rescue and treatment of the affected animals.
Abbreviations
Not applicable.
Acknowledgements
We would like to thank Snow leopard Foundation (Pakistan) International Research Support Initiative Program (IRSIP), and Higher Education Commission (Pakistan) for their support.
Funding
Not applicable.
Availability of data and material
Not applicable.
Authors’ contributions
KH, JUD & MAN performed the fieldwork. KH, SAA, JUD, MAN and LR discussed and wrote the paper. All authors read and approved the final version of the manuscript.
Competing interests
The authors declare that they have no competing interests.
Consent for publication
Not applicable.
Ethics approval
Not applicable.
Contributor Information
Khalid Hameed, Email: khalid.zoology@must.edu.pk.
Samer Angelone-Alasaad, Email: sameralasaad@hotmail.com.
Jaffar Ud Din, Email: jaffar@slf.org.pk.
Muhammad Ali Nawaz, Email: nawazma@gmail.com.
Luca Rossi, Email: luca.rossi@unito.it.
References
- 1.Bornstein S, Mörner T, Samuel WM. Sarcoptes scabiei and sarcoptic mange. In: Samuel WM, Pybus MJ, Kocan AA, editors. Parasitic diseases of wild mammals. 2. Iowa: Iowa State University Press, Ames; 2001. pp. 107–119. [Google Scholar]
- 2.Alasaad S, Walton S, Rossi L, Bornstein S, Abu-Madi M, Soriguer RC, et al. Sarcoptes-World Molecular Network (Sarcoptes-WMN): integrating research on scabies. Int J Infect Dis. 2011;15:294–297. doi: 10.1016/j.ijid.2011.01.012. [DOI] [PubMed] [Google Scholar]
- 3.Alasaad S, Sarasa M, Heukelbach J, Mijele D, Soriguer CS, Zhu XQ, et al. Advances in studies of disease-navigating webs: Sarcoptes scabiei as a case study. Parasit Vectors. 2014;7:e16. doi: 10.1186/1756-3305-7-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Bates P. Sarcoptic mange (Sarcoptes scabiei var. vulpes) in a red fox (Vulpes vulpes) population in north-west Surrey. Vet Rec. 2003;152:112–4. [DOI] [PubMed]
- 5.Alasaad S, Ndeereh D, Rossi L, Bornstein S, Permunian R, Soriguer RC, et al. The opportunistic Sarcoptes scabiei: a new episode from giraffe in the drought-suffering Kenya. Vet Parasitol. 2012;185:359–363. doi: 10.1016/j.vetpar.2011.10.039. [DOI] [PubMed] [Google Scholar]
- 6.Walton SF, Holt DC, Currie BJ, Kemp DJ. Scabies: new future for a neglected disease. Adv Parasitol. 2004;57:309–376. doi: 10.1016/S0065-308X(04)57005-7. [DOI] [PubMed] [Google Scholar]
- 7.Din JU, Zimmermann F, Ali M, Ali Shah K, Ayub M, Khan S, et al. Population assessment of Himalayan lynx (Lynx lynx isabellinus) and conflict with humans in the Hindu Kush mountain range of District Chitral, Pakistan (Malay) Integr Zool. 2013;8:232–243. doi: 10.1111/1749-4877.12017. [DOI] [PubMed] [Google Scholar]
- 8.Din JU, Nawaz MA. Status of the Himalayan lynx in district Chitral, NWFP, Pakistan. J Anim Plant Sci. 2010;20:17–22. [Google Scholar]
- 9.Alasaad S, Rossi L, Soriguer RC, Rambozzi L, Soglia D, Pérez JM, et al. Sarcoptes mite from collection to DNA extraction: the lost realm of the neglected parasite. Parasitol Res. 2009;104:723–732. doi: 10.1007/s00436-009-1333-0. [DOI] [PubMed] [Google Scholar]
- 10.Rasero R, Rossi L, Soglia D, Maione S, Sacchi P, Rambozzi L, et al. Host taxon-derived Sarcoptes mite in European wild animals revealed by microsatellite markers. Biol Conserv. 2010;143:1269–1277. doi: 10.1016/j.biocon.2010.03.001. [DOI] [Google Scholar]
- 11.McCarthy TM, Chapron G. Snow Leopard Survival Strategy. Seattle: International Snow Leopard Trust and Snow Leopard Network; 2003. [Google Scholar]
- 12.https://pamirtimes.wordpress.com/2011/02/27/sick-snow-leopard-captured-by-villagers-in-skardu-dies/.
- 13.Ryser-Degiorgis MP, Ryser A, Bacciarini LN, Angst C, Gottstein B, Janovsky M, et al. Notoedric and sarcoptic mange in free-ranging lynx from Switzerland. J Wildl Dis. 2002;38:228–232. doi: 10.7589/0090-3558-38.1.228. [DOI] [PubMed] [Google Scholar]
- 14.Gakuya F, Rossi L, Ombui J, Maingi N, Muchemi G, Ogara W, et al. The curse of the prey: Sarcoptes mite molecular analysis reveals potential prey-to-predator parasitic infestation in wild animals from Masai Mara, Kenya. Parasit Vectors. 2011;4:1e93. doi: 10.1186/1756-3305-4-193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Aziz F, Tasawar Z, Lashari MH. Prevalence of Sarcoptes scabiei var. caprae in Goats of Dera Ghazi Khan, Punjab, Pakistan. Int J Curr Eng Technol. 2013;3:1327–1329. [Google Scholar]
