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 lynxPeer reviewe

Jaffar Ud Din

Khalid Hameed

Luca Rossi

Muhammad Ali Nawaz

Samer Angelone-Alasaad

Parasites & Vectors

PubMed

Springer - Publisher Connector

LETTER TO THE EDITOR Open Access
The threatening but unpredictable
Sarcoptes scabiei: first deadly outbreak in
the Himalayan lynx, Lynx lynx isabellinus,
from Pakistan
Khalid Hameed1,2, Samer Angelone-Alasaad3,4* , Jaffar Ud Din5,6, Muhammad Ali Nawaz7 and Luca Rossi8
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 intro-
duction 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 re-
port 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 con-
flict, loss of natural prey-base and loss of habitat to a
lesser extent [8].
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 immedi-
ately 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).
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 de-
tected (1309 mites/cm2 skin), with prevailing larval
stages. We considered two hypotheses, which could ex-
plain the origin of the outbreak.
* Correspondence: sameralasaad@hotmail.com
3Institute of Evolutionary Biology and Environmental Studies (IEU), University
of Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland
4Estación Biológica de Doñana, Consejo Superior de Investigaciones
Científicas (CSIC), Avda, Américo Vespucio s/n, 41092 Sevilla, Spain
Full list of author information is available at the end of the article
© 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Hameed et al. Parasites & Vectors  (2016) 9:402 
DOI 10.1186/s13071-016-1685-0
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 sam-
ples have been collected [11]. Similarly, a mange-like
condition was observed (though not laboratory con-
firmed) in a snow leopard captured near Skardu,
Gilgit-Baltistan [12]. In Scandinavia and Switzerland,
Fig. 1 Map of Pakistan showing the site where the mange-infested Himalayan lynx was found
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
Hameed et al. Parasites & Vectors  (2016) 9:402 Page 2 of 3
deadly sarcoptic mange in Eurasian lynx has been associ-
ated 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-emer-
gence, where Sarcoptes infestation was pre-existing, and
the new recognition is a result of increased detection op-
portunities [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.
Author details
1Department of Zoology, Mirpur University of Science & Technology (MUST),
Mirpur Azad Jammu & Kashmir, Pakistan. 2Department of Zoology, Arid
Agriculture University, Rawalpindi, Pakistan. 3Institute of Evolutionary Biology
and Environmental Studies (IEU), University of Zürich, Winterthurerstrasse
190, 8057 Zürich, Switzerland. 4Estación Biológica de Doñana, Consejo
Superior de Investigaciones Científicas (CSIC), Avda, Américo Vespucio s/n,
41092 Sevilla, Spain. 5Snow Leopard Foundation, Islamabad, Pakistan.
6Institute of Biological Sciences, Faculty of Science, University of Malaya,
50603 Kuala Lumpur, Malaysia. 7Department of Animal Sciences,
Quaid-I-Azam University, Islamabad, Pakistan. 8Dipartimento di Scienze
Veterinarie, Università degli Studi di Torino, Via Leonardo da Vinci 44, I-10095
Grugliasco, Italy.
Received: 7 June 2016 Accepted: 6 July 2016
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. 2nd ed. Iowa: Iowa State University Press, Ames; 2001. p. 107–19.
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;15:294–7.
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.
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.
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;185:359–63.
6. Walton SF, Holt DC, Currie BJ, Kemp DJ. Scabies: new future for a neglected
disease. Adv Parasitol. 2004;57:309–76.
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;8:232–43.
8. Din JU, Nawaz MA. Status of the Himalayan lynx in district Chitral, NWFP,
Pakistan. J Anim Plant Sci. 2010;20:17–22.
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;104:723–32.
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;143:1269–77.
11. McCarthy TM, Chapron G. Snow Leopard Survival Strategy, vol. 105. Seattle:
International Snow Leopard Trust and Snow Leopard Network; 2003.
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;38:228–32.
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.
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:
1327–9.
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Hameed et al. Parasites & Vectors  (2016) 9:402 Page 3 of 3


The threatening but unpredictable Sarcoptes scabiei: first deadly outbreak in the Himalayan lynx, Lynx lynx isabellinus, from Pakistan

Crossref

Rossi, L.

Institutional Research Information System University of Turin

LETTER TO THE EDITOR Open AccessThe threatening but unpredictableSarcoptes scabiei: first deadly outbreak inthe Himalayan lynx, Lynx lynx isabellinus,from PakistanKhalid Hameed1,2, Samer Angelone-Alasaad3,4* , Jaffar Ud Din5,6, Muhammad Ali Nawaz7 and Luca Rossi8AbstractAlthough neglected, the mite Sarcoptes scabiei is an unpredictable emerging parasite, threatening human andanimal health globally. In this paper we report the first fatal outbreak of sarcoptic mange in the endangeredHimalayan lynx (Lynx lynx isabellinus) from Pakistan. A 10-year-old male Himalayan lynx was found in a miserablecondition with severe crusted lesions in Chitral District, and immediately died. Post-mortem examination determinedhigh S. scabiei density (1309 mites/cm2 skin). It is most probably a genuine emergence, resulting from a new incidencedue to the host-taxon derived or prey-to-predator cross-infestation hypotheses, and less probable to be apparentemergence resulting from increased infection in the Himalayan lynx population. This is an alarming situation for theconservation of this already threatened population, which demands surveillance for early detection and eventuallyrescue and treatment of the affected Himalayan lynx.Keywords: Sarcoptes scabiei, Lynx lynx isabellinus, Human-lynx conflict, Chitral District, Pakistan, Neglected parasite,Emerging diseaseLetter to the editorAlthough affecting more than 100 species of mammalsworldwide [1, 2], the epidemiology of Sarcoptes scabiei isstill not well understood, with differences betweenlocations and host species [3]. The emerging of S. scabieiis frightening, since it may entail devastating mortalityin wild and domestic animals, even only from the intro-duction of a single case [4, 5]. Sudden outbreaks of S.scabiei in human, wild and domestic populations havefrequently been reported [6]; nevertheless, there is no re-port of S. scabiei infestations in the Turkestan subspeciesof the Eurasian lynx, also named Himalayan lynx (Lynxlynx isabellinus).The Himalayan lynx in the Hindu Kush mountainrange of the District Chitral, Pakistan (Fig. 1), is highlythreatened. The last population assessment reportedsporadic occurrence with a minimum of six individuals[7]. The prime threats to the existence of the Himalayanlynx are retaliatory killing because of human-lynx con-flict, loss of natural prey-base and loss of habitat to alesser extent [8].On the 26th of March 2016, a 10-year-old maleHimalayan lynx was found by villagers of Karimabad,while in a miserable condition, with severe crustedlesions on the lower limbs (Fig. 2). Although immedi-ately transported by field staff of the Snow LeopardFoundation, to the Animal Hospital in Chitral City,the lynx died before treatment was started. Deep skinscrapings were collected and examined followingKOH clearing [9] (Fig. 3).This is the first report of fatal outbreak of sarcopticmange in the Himalayan lynx (Lynx lynx isabellinus)from Pakistan. A high Sarcoptes mite density was de-tected (1309 mites/cm2 skin), with prevailing larvalstages. We considered two hypotheses, which could ex-plain the origin of the outbreak.* Correspondence: sameralasaad@hotmail.com3Institute of Evolutionary Biology and Environmental Studies (IEU), Universityof Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland4Estación Biológica de Doñana, Consejo Superior de InvestigacionesCientíficas (CSIC), Avda, Américo Vespucio s/n, 41092 Sevilla, SpainFull list of author information is available at the end of the article© 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.Hameed et al. Parasites & Vectors  (2016) 9:402 DOI 10.1186/s13071-016-1685-0Hypothesis (i): The outbreak is ‘genuine’ emergence ofan infestation, which is new to the Himalayan lynxpopulation. Likely sources could be other carnivoressharing habitat with the Himalayan lynx, such as wolf,snow leopard, jackal, fox and leopard cat, according tothe host-taxon derived hypothesis [10]. While in nearbyCentral Karakhoram National Park, Gilgit-Baltistan, oneof the Authors (LR, unpublished) collected photo trapevidence that scabies was present among red foxes(Vulpes vulpes). In western Mongolia numerous reportshave been made of a debilitating mange-like affliction inthe snow leopard (Uncia uncia); however no skin sam-ples have been collected [11]. Similarly, a mange-likecondition was observed (though not laboratory con-firmed) in a snow leopard captured near Skardu,Gilgit-Baltistan [12]. In Scandinavia and Switzerland,Fig. 1 Map of Pakistan showing the site where the mange-infested Himalayan lynx was foundFig. 2 Carcass of the mange-infested Himalayan lynx showingsevere crusted lesionsFig. 3 Adult Sarcoptes mite taken from the skin scraping of the deadHimalayan lynxHameed et al. Parasites & Vectors  (2016) 9:402 Page 2 of 3deadly sarcoptic mange in Eurasian lynx has been associ-ated to epidemic or endemic disease in the sympatricabundant red fox populations [13]. Other putative sourcesare infested domestic animals, through prey-to-predatorcross-infestation [14]. Livestock, especially lambs and kids,are major victims of lynx attacks [8]. Most households ofthe community hold small herds composed of one or twocattle and ten to fifteen sheep and goats. During summerdomestic animals are taken to alpine pastures for grazing,and are more vulnerable to predation by lynx. Sarcopticmange is widespread amongst small domestic ruminantsin Pakistan [15].Hypothesis (ii): It is ‘apparent’ emergence/re-emer-gence, where Sarcoptes infestation was pre-existing, andthe new recognition is a result of increased detection op-portunities [7].This is the first Sarcoptes mite infection case report inthe Himalayan lynx population from Pakistan. This is analarming situation for the conservation of the alreadythreatened population of this species, which demandssurveillance for early detection and eventually rescueand treatment of the affected animals.AbbreviationsNot applicable.AcknowledgementsWe would like to thank Snow leopard Foundation (Pakistan) InternationalResearch Support Initiative Program (IRSIP), and Higher Education Commission(Pakistan) for their support.FundingNot applicable.Availability of data and materialNot applicable.Authors’ contributionsKH, JUD & MAN performed the fieldwork. KH, SAA, JUD, MAN and LRdiscussed and wrote the paper. All authors read and approved the finalversion of the manuscript.Competing interestsThe authors declare that they have no competing interests.Consent for publicationNot applicable.Ethics approvalNot applicable.Author details1Department of Zoology, Mirpur University of Science & Technology (MUST),Mirpur Azad Jammu & Kashmir, Pakistan. 2Department of Zoology, AridAgriculture University, Rawalpindi, Pakistan. 3Institute of Evolutionary Biologyand Environmental Studies (IEU), University of Zürich, Winterthurerstrasse190, 8057 Zürich, Switzerland. 4Estación Biológica de Doñana, ConsejoSuperior de Investigaciones Científicas (CSIC), Avda, Américo Vespucio s/n,41092 Sevilla, Spain. 5Snow Leopard Foundation, Islamabad, Pakistan.6Institute of Biological Sciences, Faculty of Science, University of Malaya,50603 Kuala Lumpur, Malaysia. 7Department of Animal Sciences,Quaid-I-Azam University, Islamabad, Pakistan. 8Dipartimento di ScienzeVeterinarie, Università degli Studi di Torino, Via Leonardo da Vinci 44, I-10095Grugliasco, Italy.Received: 7 June 2016 Accepted: 6 July 2016References1. Bornstein S, Mörner T, Samuel WM. Sarcoptes scabiei and sarcoptic mange.In: Samuel WM, Pybus MJ, Kocan AA, editors. Parasitic diseases of wildmammals. 2nd ed. Iowa: Iowa State University Press, Ames; 2001. p. 107–19.2. Alasaad S, Walton S, Rossi L, Bornstein S, Abu-Madi M, Soriguer RC, et al.Sarcoptes-World Molecular Network (Sarcoptes-WMN): integrating researchon scabies. Int J Infect Dis. 2011;15:294–7.3. 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 casestudy. Parasit Vectors. 2014;7:e16.4. Bates P. Sarcoptic mange (Sarcoptes scabiei var. vulpes) in a red fox (Vulpesvulpes) population in north-west Surrey. Vet Rec. 2003;152:112–4.5. Alasaad S, Ndeereh D, Rossi L, Bornstein S, Permunian R, Soriguer RC, et al.The opportunistic Sarcoptes scabiei: a new episode from giraffe in thedrought-suffering Kenya. Vet Parasitol. 2012;185:359–63.6. Walton SF, Holt DC, Currie BJ, Kemp DJ. Scabies: new future for a neglecteddisease. Adv Parasitol. 2004;57:309–76.7. Din JU, Zimmermann F, Ali M, Ali Shah K, Ayub M, Khan S, et al. Populationassessment of Himalayan lynx (Lynx lynx isabellinus) and conflict withhumans in the Hindu Kush mountain range of District Chitral, Pakistan(Malay). Integr Zool. 2013;8:232–43.8. Din JU, Nawaz MA. Status of the Himalayan lynx in district Chitral, NWFP,Pakistan. J Anim Plant Sci. 2010;20:17–22.9. 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 theneglected parasite. Parasitol Res. 2009;104:723–32.10. Rasero R, Rossi L, Soglia D, Maione S, Sacchi P, Rambozzi L, et al. Hosttaxon-derived Sarcoptes mite in European wild animals revealed bymicrosatellite markers. Biol Conserv. 2010;143:1269–77.11. McCarthy TM, Chapron G. Snow Leopard Survival Strategy, vol. 105. Seattle:International Snow Leopard Trust and Snow Leopard Network; 2003.12. 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;38:228–32.14. Gakuya F, Rossi L, Ombui J, Maingi N, Muchemi G, Ogara W, et al. The curseof the prey: Sarcoptes mite molecular analysis reveals potential prey-to-predator parasitic infestation in wild animals from Masai Mara, Kenya.Parasit Vectors. 2011;4:1e93.15. Aziz F, Tasawar Z, Lashari MH. Prevalence of Sarcoptes scabiei var. caprae inGoats of Dera Ghazi Khan, Punjab, Pakistan. Int J Curr Eng Technol. 2013;3:1327–9.•  We accept pre-submission inquiries •  Our selector tool helps you to find the most relevant journal•  We provide round the clock customer support •  Convenient online submission•  Thorough peer review•  Inclusion in PubMed and all major indexing services •  Maximum visibility for your researchSubmit your manuscript atwww.biomedcentral.com/submitSubmit your next manuscript to BioMed Central and we will help you at every step:Hameed et al. Parasites & Vectors  (2016) 9:402 Page 3 of 3

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The threatening but unpredictable Sarcoptes scabiei: First deadly outbreak in the Himalayan lynx, Lynx lynx isabellinus, from Pakistan

Hammed, Khalid

Alasaad, Samer

Ud Din, Jaffar

Nawaz, Muhammad Ali

Rossi, Luca

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The threatening but unpredictable Sarcoptes scabiei: first deadly outbreak in the Himalayan lynx, Lynx lynx isabellinus, from Pakistan

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