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Veterinary Dermatology 2003, 14, 339 344

Blackwell Publishing Ltd.

Notoedric mange in free-ranging masked palm civets


(Paguma larvata) in Japan
HIROYOSHI NINOMIYA*, MUNETSUGU OGATA and TAKASHI MAKINO
*Department of Laboratory Animal Science and Veterinary Teaching Hospital, School of Veterinary Medicine,
Azabu University, 1-17-71 Fuchinobe Sagamihara Kanagawa 229-8501, Japan
Kanagawa Prefecture Nature Preserving Center, 657 Nanasawa Atsugi, Kanagawa 243-0121, Japan
(Received 14 February 2003; accepted 4 June 2003)

Abstract Fifty-one masked palm civets (Paguma larvata) were trapped as part of a nuisance wildlife control
programme between July 2001 and August 2002 in Fujisawa City, Kanagawa Prefecture, Japan. Eleven civets had
characteristic mange lesions with marked alopecia and crusts, caused by the burrowing epidermal mite Notoedres
cati. The diagnosis was confirmed by histology and examination of mites obtained from skin scrapings of affected
civets. Histopathology of lesions demonstrated moderate hyperplastic epidermis, parakeratosis and acanthosis.
Occasionally microvascular angiogenesis was observed in the epidermis. Tunnels were excavated in the hair follicles, reaching the hair roots. The tunnels were located between the hair shaft and the inner root sheath. Female
mites, eggs and nymphs were demonstrated in their tunnels using scanning electron microscopy.
Keywords: mange, masked palm civet, Notoedres cati, Paguma larvata.

INTRODUCTION
Masked palm civets (Paguma larvata) are found throughout
most of Japan. They were initially imported as pets
from South-East Asian countries in the 1900s. Animals
escaped and the number of masked palm civets has since
increased. The civet population has especially increased
in urban and suburban areas over the past decade.
Masked palm civets cause a variety of problems including feeding on dog or cat food, feeding on trash in garbage
cans, establishing dens in attics or wall spaces, and/or
causing damage to vegetable gardens and fruit trees.
Notoedric mange is an epizootic cutaneous disease of
mammals and is caused by Notoedres cati, in felids,17
white-nosed coatis (Nasua narica)8 and ring-tails
(Bassariscus astutus).9 In a previous report, we described
an infection with N. cati in free-ranging North American
racoons (Procyon lotor) in Japan.10 This mite infestation
is rarely reported in the family Viverridae.11 This report
describes an outbreak of notoedric mange in a population of masked palm civets from the Kanagawa Prefecture
in Japan.

MATERIALS AND METHODS


As part of a programme of nuisance wildlife control,
between July 2001 and August 2002, 51 adult masked palm
civets were captured in residential areas of Fujisawa
Correspondence: H. Ninomiya, Department of Laboratory Animal
Science, School of Veterinary Medicine, Azabu University, 1-17-71
Fuchinobe Sagamihara Kanagawa 229-8501, Japan. E-mail:
ninomiya@azabu-u.ac.jp
2003 European Society of Veterinary Dermatology

City (13931E, 3525N), in the Kanagawa Prefecture,


Japan and euthanized with an overdose of pentobarbital
injected intraperitoneally. Eleven (five males, six females)
animals had clinical signs consistent with mite infestations. Carcasses were frozen and stored at the Nature
Preserving Center of the Kanagawa Prefecture until they
were transported to our laboratory at Azabu University
where they were thawed and necropsied as part of a
wildlife research programme. Skin specimens were
excised and fixed in neutral-buffered 10% formalin, and
later sectioned at 5 m and stained with haematoxylin
and eosin (H&E). Skin scrapings were treated with 10%
KOH and examined microscopically for mites. Mites
were examined as whole mounts in glycerin. For scanning
electron microscopy (SEM) examination, the skin was
fixed in 10% glutaraldehyde, and then immersed in 10%
KOH for 2 h to digest the cornified layer. The stratum
corneum and the surface layer of the epidermis were
removed by scraping or slicing with a scalpel to expose
the mites in the skin. After dehydration through graded
concentrations of ethanol, the tissue was critical-point
dried (CP 5A, Topcon, Tokyo, Japan) using liquid carbon
dioxide. Samples were mounted on aluminium stubs
using silver paste and sputtered with gold in an ion coater
(IB-3, Eiko Engineering, Tokyo, Japan). Handling and
use of the animals were regulated under the authority
of the Nature Preserving Center of the Kanagawa
Prefecture.

RESULTS
Eleven of the 51 adult masked palm civets (Paguma larvata)
had extensive dermatitis involving the ears, skin over
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Figure 1. Severe notoedric mange in a masked palm civet, Paguma


larvata, including alopecia and scab formation over the whole body.

Figure 3. Scanning electron micrograph showing dorsal idiosoma of


an adult female Notoedres cati from a civet. Bar = 33.3 m. 1st, first
leg; 2nd, second leg.

Figure 2. Lesions of notoedric mange on the trunk of an infested


civet; note scrab and marked alopecia.

the dorsal aspect of the head, neck, thorax, ventral


trunk, legs or tail. The affected skin was devoid of hair,
had numerous nodules and was thickened, leathery and
wrinkled. In severely emaciated animals trapped in the
winter season, there was partial to complete alopecia,
thickened wrinkled skin with dense grey encrustations
over the whole body, especially on the face (Fig. 1). The
skin in the affected areas was markedly corrugated and
often was covered by large plaques of keratinous crusts,
resulting from self-inflicted trauma induced by pruritis
(Fig. 2).
Skin scrapings of lesions revealed all life stages of
culprit mites, from ovum to adult. The mites were oval
and tortoise-like. Female adult mites had suckers on
short legs l and 2, cuticular scales and prominent body
striations. The anus was located dorsally and was surrounded by several stout setae (Fig. 3). The mites were
identified as N. cati on the basis of these morphologic
features. N. cati resembles N. douglasi (centrifera) and
N. muris from which it may be distinguished by the
following features. The dorsal scale-like formations
present in N. cati are absent in N. douglasi and N. muris.12
The elongated setae differentiate N. cati from other
Notoedres (e.g. N. musculi, N. oudemansi) with scaly
patterns on the dorsum.9
Histologically, the affected skin was characterized by
extensive acanthosis, and hyperkertosis and parakeratosis

Figure 4. Section of skin from a masked palm civet showing


notoedric mites in the hair follicles, moderate hyperkeratosis and
acanthotic skin. H&E stain. Bar = 50 m. h, hair shaft; m, mite.

of the epidermis with numerous intraepidermal tunnels


containing mites.
Tunnels were burrowed in the hair follicles and
located between the hair shaft and the inner root sheath.
The epidermal tunnels were lined by flattened parakeratotic cells. Eggs, larvae, nymphs and adult females
were observed in some tunnels. Intraepidermal abscesses
were not present in skin sections of affected animals.
Moderate spongiosis was only present in epidermis
close to the mites. The inflammatory response was
slight and usually limited to the perivascular spaces in
the papillary layer of the dermis. Some of the epithelial
cells in the affected hair follicles showed marked
attenuation and parakeratosis. The affected hair follicles were completely disorganized, devoid of hair shafts
and filled with sloughed keratinocytes, accounting for
the alopecia. (Fig. 4). The dermal microvasculature
in the papillary layer was enlarged and prominent.
Neovascularization was sometimes observed in the
epidermis, close to the parakeratotic scales (Fig. 5).

European Society of Veterinary Dermatology, Veterinary Dermatology, 14, 339 344

Notoedric mange in masked palm civets

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Figure 5. Section of skin from a masked palm civet showing proliferating capillaries (arrows) in encrusted epidermis associated with the mite.
H&E stain. Bar = 50 m. epi: parakeratotic epithelial cells; m, mite.

Figure 7. An oviposition tunnel containing a female mite and an egg.


The tunnel is spacious and in good order. Bar = 66.6 m. e, egg; m, mite.

Figure 6. Scanning electron micrograph showing mites within


tunnels. The stratum corneum and the papillary layer of the dermis
were removed with a scalpel. Bar = 66.6 m. h, hair shaft; m, mite.

On scanning electron microscopy, tunnels of N.


cati were burrowed vertically along the hair follicles
(Figs 610). Each tunnel was separate from the others
(Fig. 6). The tunnels reached the hair root where most
of the mites were located. Adult mites, eggs, larvae and
nymphs were in the tunnels. Adult female mites measured 137196 m long by 110158 m wide. The eggs
were oval and measured 8292 m by 4350 m. Based
on their structure and the mites they contained three
types of tunnels were observed; an oviposition tunnel
(Fig. 7), a common tunnel (Figs 8 and 9) and a moulting
tunnel (Fig. 10). The oviposition tunnel was spacious
with little contents such as faeces and epithelial cells
debris and contained a fertilized, egg-laying female.
The common tunnels were packed with faeces and
parakeratotic epithelial cells and were shared by one or
two female mites. Moulting tunnels contained nymphs
and shedding were occasionally observed. Most of the
mites in the tunnels were facing the deeper layer of the
hair follicles (Fig. 6).

Figure 8. A common tunnel in which mites stay most of their life.


The tunnel is packed with faeces and debris of parakeratotic
epithelial cells. Bar = 66.6 m. epi: parakeratotic epithelial cells; f,
faeces; m, mite.

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H. Ninomiya et al.
DISCUSSION

Figure 9. A mite in a common tunnel. Most of the mites heads are


toward the deeper layer of the epidermis but this mite is facing the skin
surface; probably in order to migrate onto the skin for mating. Note
the tunnel is closely associated with the hair follicle. Bar = 33.3 m.
ans, anus; h, hair shaft; m, mite.

Figure 10. A mite in a moulting tunnel just before casting off.


Sheddings (1st) of the first leg with a berst leg (1st) of the mite are
seen in the castoff covering (arrow). Bar = 33.3 m. 1st, first leg.

The masked palm civet population has increased


significantly over the past decade in most towns and
cities in the Kanagawa Prefecture. The animals live
within city limits, and feed on dog or cat food, refuse
or fruits on trees. During winter, when food resources
become limited, feral cats, racoons and masked palm
civets concentrate around garbage cans. Notoedric
mites may also live for a few days off the host and are
transmitted primarily by direct contact as in Sarcoptes
scabiei.13 Contact with infected individual bedding
or sites recently visited might also result in spread of
the disease. According to local veterinarians notoedric
mange in homeless cats is very prevalent and severe in
the area. Infected animals become an effective source
of mites for other animals. The gregarious nature of
masked palm civets probably favours spread of the
disease. The overall prevalence of notoedric mange
in masked palm civets was 21.6% (11 diseased animals/
51 trapped animals) in 2002, whereas in racoons it was
4% (2 diseased animals/50 trapped animals) in 2001.10
This shows wide occurrence of this mite in the two
species within the study sites in the Kanagawa Prefecture in Japan.
All 11 cases of notoedric mange included in this
study are consistent in their area of localization of
mites on the host, clinical manifestations and pathology
similar to racoons and domestic cats. Angiogenesis in
the epidermis in notoedric lesions contrasts with the
absence of capillaries in healthy epidermis. Proliferating, dilated capillaries were commonly observed in
the epidermis and the papillary layer of the dermis
adjacent to mites. The increased blood supply to the
tissue may favour the survival of the mites that feed on
live cells, including parakeratotic scales and crusts, or
tissue fluid oozing into the burrows. The avascular
epidermis has the capacity to regulate dermal angiogenesis and microvascular permeability by a paracrine
mechanism involving the secretion of vascular permeability factor/vascular endothelial growth factor
which induces angiogenesis and vasodilation.14 Similar
alterations have been described in lesional psoriatic
epidermis in humans.15
N. cati differs from S. scabiei, another burrowing
epidermal mite, in that they excavate vertical tunnels
along hair shafts where they inhabit deep layers of the
skin adjacent to hair roots. Tunnels of N. cati are
excavated in hair follicles and are separated from each
other, whereas those of S. scabiei are burrowed parallel
to the skin surface around the hair follicles.13 The tunnels
are located in the stratum corneum and the epidermis
and are connected to each other to form a honeycomb
network in the surface layer of the skin. This vertical
trend may make it more difficult to confirm notoedric
mange by skin scrapings. Also, histological sections of
biopsied tissue may not be helpful, the one exception
being animals with severe and chronic infestation as
suggested in sarcoptic mange.13,16 With no evidence of
mites, mite eggs or mite faeces on skin scrapings and in

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Notoedric mange in masked palm civets


histological sections, notoedric acariasis may be confused with other dermatoses with pruritus, inflammation
and/or alopecia.
N. cati tunnels seem to vary between host species. In
racoon, tunnels are relatively shallow, and are located
between hair follicles,11 whereas tunnels in masked
palm civets are located closely to the hair shafts and
excavated along the hair follicles where the mites
inhabit deep in the hair root, similarly to Demodex spp.
mites.17 There is no significant difference in the dermal
and epidermal composition in these two mammal species. Further investigations concerning relationships
between mites and host species should be fruitful.
Some larvae of N. cati migrate from their tunnels
made by the females and others reside in these tunnels.6
Adult male notoedric mites move on the skin and
die after copulation.6 Only fertilized females burrow
tunnels and reside in them.6 The females may segregate
their niches for oviposition, moulting and common
life, similar to S. scabiei.13 The oviposition tunnels where
fertilized female mites lay eggs are roomy and tidy, in
contrast to other tunnels which are packed with faeces
and debris of keratinocytes. Clean and spacious oviposition tunnels may give hatching larvae optimal feeding
conditions.

REFERENCES
1. Maehr, D.S., Greiner, E.C., Lanier, J.E. et al. Notoedric
mange in the Florida panther (Felis concolor coryi).
Journal of Wildlife Diseases 1995; 31: 251 4.
2. Pence, D.B., Tewes, M.E., Shindle, D.B. et al. Notoedric
mange in an ocelot (Felis pardalis) from southern Texas.
Journal of Wildlife Diseases 1995; 31: 558 62.
3. Pence, D.B., Matthews, F.D., Windberg, L.A. Notoedric
mange in the bobcat, Felis rufus, from southern Texas.
Journal of Wildlife Diseases 1982; 18: 47 50.
4. Fletcher, K.C. Notoedric mange in a litter of snow
leopards. Journal of the American Veterinary Medical
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5. Scott, D.W., Miller, W.H., Griffin, C.E. Parasitic skin


diseases. In: Muller and Kirks Small Animal Dermatology, 6th edn. Philadelphia: WB Saunders, 2001:
4834.
6. Foley, R.H. A notoedric mange epizootic in an islands
cat population. Feline Practice 1991; 19: 810.
7. Young, E., Zumpt, F., Whyte, I.J. Notoedres cati (Hering,
1883) infestation of the cheetah: preliminary report.
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1972; 43: 205.
8. Valenzuela, D., Ceballos, G., Garcia, A. Mange epizootic
in white-nosed coatis in western Mexico. Journal of Wildlife
Diseases 2000; 36: 5663.
9. Klompen, H. Phylogenetic relationships in the mite
family Sarcoptidae (Acari: Astigmata). Miscellaneous
Publications Museum of Zoology, University of Michigan
1992; 180: 1159.
10. Ninomiya, H., Ogata, M. Notoedric mange in two
free-ranging North American racoons (Procyon lotor)
in Japan. Veterinary Dermatology 2002; 13: 11921.
11. Webb, J.W. Parasites of small Indian mongoose on St.
Croix, Virgin Islands. Journal of Parasitology 1980; 66:
1768.
12. Lavoipierre, M.M. Mange mites of the genus Notoedres
(Acari. Sarcoptidae) with descriptions of two new
species and remarks on Notoedric mange in the squirrel
and the vole. Journal of Medical Entomology 1964; 1 (1):
517.
13. Bornstein, S., Mrner, T., Samuel, M. Sarcoptes scabiei and
sarcoptic mange. In: Parasitic Disease of Wild Mammals.
Ames: Iowa State University Press, 2001: 10719.
14. Detmar, M., Yeo, K.T., Nagy, J.A. et al. Keratinocytederived vascular permeability factor (vascular endothelial
growth factor) is a potent mitogen for dermal microvascular
endothelial cells. Journal of Investigative Dermatology
1995; 105: 4450.
15. Elder, J.T., Fisher, G.J., Lindquist, P.B. et al. Overexpression of transforming growth factor alpha in psoriatic
epidermis. Science 1989; 10: 243 (4892): 8114.
16. Paterson, S., Pike, R., Boydell, P. Norwegian scabies in
a dog. Veterinary Record 1995; 136: 3934.
17. Hamir, A.N., Snyder, D.E., Hanlon, C.A. et al. First report
of a Demodex sp. in racoons. (Procycon lotor). Journal of
Wildlife Diseases 1993; 29: 13941.

Rsum Cinquante et une civettes (Paguma larvata) ont t captures dans le cadre d'un programme de contrle
des animaux nuisibles entre juillet 2001 et aot 2002 Fujisawa au Japon. Onze animaux prsentaient des lsions
typiques de gale, avec une alopcie marque et des crotes, dues l'acarien Notoedres cati. Le diagnostic a t
confirm par histologie et par l'examen microscopique de raclages cutans mettant en vidence les parasites. Les
lsions microscopiques regoupaient la prsence d'une hyperplasie pidermique modre, d'une parakratose et
d'une acanthose. Occasionellement, une angiognse microvasculaire a t observe dans l'piderme. Des tunnels
ont t nots dans les follicules pileux, pntrant jusqu'aux gaines folliculaires. Ils taient localiss entre ke oiuk
et la gaine folliculaire interne. Des acariens femelles, des oeufs et des nymphes ont t identifis dans ces tunnels
par microscopie lectronique balayage.
Resumen Cincuenta y una pagumas (Paguma larvata) fueron cazadas mediante trampas dentro del programa
de control de la fauna salvaje llevado a cabo entre Julio del 2001 y agosto del 2002 en la ciudad de Fujisawa,
Prefactura de Kanagawa, Japn. Once pagumas mostraron lesiones caractersticas de sarna con alopecia y costras
extensas, causadas por la formacin de tneles epidrmicos por parte del caro Notoedres cati. El diagnstico
fue confirmado por histologa y estudio de los caros obtenidos por raspados cutneos de pagumas afectadas.
La histopatologa de las lesiones mostraron una epidermis moderadamente hiperplsica, paraqueratosis y
acantosis. Ocasionalmente se observ angiognesis microvascular en la epidermis. Los tneles estaban excavados
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H. Ninomiya et al.
en los folculos pilosos, alcanzando las races del pelo. stos de localizaban entre el pelo y la vaina interna de
la raz. La microscopa electrnica de barrido permiti demostrar la presencia en los tneles de caros hembra,
huevos y ninfas.
Zusammenfassung Einundfnfzig Civets (masked palm civets, Paguma larvata) wurden im Rahmen eines
Wildtierschdlings-Kontrollprogramms im Zeitraum von Juli 2001 bis August 2002 in Fujisawa City, Kanagawa
Prfektur, Japan gefangen. Elf Civets hatten typische Rudevernderungen mit deutlicher Alopezie und Krusten,
hervorgerufen durch die epidermale Grabmilbe Notoedres cati. Die Diagnose wurde durch Histologie und den
Nachweis der Milben im Hautgeschabsel befallener Civets besttigt. Die Histopathologie der Lsionen zeigte
eine moderat hyperplastische Epidermis, Parakeratose und Akanthose. Gelegentlich konnte mikrovaskulre
Angiogenese in der Epidermis beobachtet werden. In den Haarfollikeln waren Tunnel gegraben worden, die
bis an die Haarwurzeln heranreichten. Die Tunnel waren zwischen Haarschaft und innerer Wurzelscheide
lokalisiert. Weibliche Milben, Eier und Nymphen konnten durch Rasterelektronenmikroskopie in ihren Tunneln
nachgewiesen werden.

European Society of Veterinary Dermatology, Veterinary Dermatology, 14, 339 344