Sarcoptic Mange in Free-ranging Raccoon Dogs (Nyctereutes Procyonoides) in Japan (Pages 177–182)

8/9/2019 Sarcoptic Mange in Free-ranging Raccoon Dogs (Nyctereutes Procyonoides) in Japan (Pages 177–182)

http://slidepdf.com/reader/full/sarcoptic-mange-in-free-ranging-raccoon-dogs-nyctereutes-procyonoides-in 1/6

© 2005 European Society of Veterinary Dermatology 177

Veterinary Dermatology 2005, 16, 177–182

BlackwellPublishing,Ltd.

Case Report

Sarcoptic mange in free-ranging raccoon dogs (Nyctereutes procyonoides

) in Japan

HIROYOSHI NINO MIYA* and MUNE TSUGU OGATA†

*Department of Laboratory Animal Science, and †Veterinary Teaching Hospital, School of Veterinary

Medicine, Azabu University, 1-17-71 Fuchinobe, Sagamihara, Kanagawa 229-8501, Japan

(

Received

10 February

2004; accepted

1 November

2004)

Abstract

Sarcoptes scabiei

infestation was diagnosed in three freshly dead free-ranging raccoon dogs (

Nyc-

tereutes procyonoides

) in Kanagawa Prefecture, Japan. The dogs presented with an alopecic pruritic skin disease,

with signs of alopecia on the ears, muzzle, around the eyes, elbow, thigh and the neck, and hyperpigmented and

crusted skin lesions, which had a severe malodour. Skin scrapings revealed the presence of the mite Sarcoptes

scabiei

. Histopathology of lesions demonstrated marked acanthosis, hyperkeratosis, parakeratosis and fungalelements, which were subsequently identified as Acremonium

sp., Alternaria

sp. and an unknown fungus. Mite

segments were located mainly in the stratum corneum and also in the stratum granulosum. Tunnels could be

observed in the hyperkeratotic stratum corneum. Scanning electron microscopy (SEM) revealed the tortoise-like

Sarcoptes scabiei

with four long bristles, suckers and blade-like claws on legs 1 and 2, cuticular spines, prominent

body striations and a terminal anus. SEM also revealed an adult female mite digging a tunnel with the head

wedged into the very end of the closed burrow. Tunnels filled with eggshells, corneocyte debris and faecal pellets

were also observed.

INTRODUCTION

Sarcoptic mange is one of the most frequently diag-

nosed infestations in a wide range of domestic and wild

mammals throughout the world. Among canids in

Japan, sarcoptic mange (infestation with Sarcoptes

scabiei

) has been reported in dogs (

Canis familiaris

),

1

foxes (

Vulpes vulpes

)

1

and raccoon dogs (

Nyctereutes

procyonoides

).

1,2

The prevalence of scabies in raccoon

dogs has been shown to be high in urban and suburban

areas over the past decade in Kanagawa Prefecture,

Japan.

1

Despite being a relatively common cutaneous

disease among raccoon dogs, descriptions of the his-

topathological changes associated with the infestationin raccoon dogs are limited. The female mite lives

within the stratum corneum and burrows down to the

stratum granulosum to feed on the tissue fluid oozing

from cells and cellular particles.

3

The aims of this case

report were to describe the lesions associated with

infestation by sarcoptic mange mites using routine

histopathology and scanning electron microscopy

(SEM) to provide a better understanding of the mite’s

habitat.

CLINICAL, HISTOPATHOLOGICAL

AND ULTRASTRUCTURALFINDINGS

Between September and December 2003, three free-

ranging raccoon dogs (adult male) were found dead next

to a dirt road in the suburban areas of Sagamihara City

(139

°

22

′

E, 35

°

34

′

N) in Kanagawa Prefecture, Japan.

They had died due to vehicular collision. All three dogs

had skin lesions comprising moderate to severe alopecia

and extensive dermatitis over the ears, muzzle, around

the eyes, elbow, thigh and the neck, and had a severe

musty malodour (Fig. 1). The alopecic skin was markedly

corrugated, thickened and covered by greyish plaquesof keratinous crusts (Fig. 2). Skin scrapings collected

into 10% KOH revealed eggs, nymphs, larvae and oval-

shaped adult mites that had angular scales, thick spines

and prominent fine striations on the dorsal idiosoma,

features that were consistent with Sarcoptes scabiei

. To

allow detailed examination, mites were examined as

whole mounts in balsam (Fig. 3). The number of mites

including nymphs and larvae was up to 82/cm

2

in severely

infested areas of skin. Skin scales were also collected

for fungal culture and grown on potato dextrose agar

with added chloramphenicol and cycloheximide at

25 °

C. Fungi identified on the basis of morphological

appearance included Acremonium

sp., Alternaria

sp.and an unknown fungus.

Skin specimens were excised and fixed in neutral-

buffered 10% formalin, sectioned serially at 5 µ

m and

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: [email protected]



178 H Ninomiya and M Ogata

© 2005 European Society of Veterinary Dermatology, Veterinary Dermatology

, 16

, 177–182

stained with haematoxylin and eosin (H&E). Histo-

logically, the papillary dermis was thickened by coarse

collagen fibres. The most extensively involved areas

showed elongation of the dermal papillae. The over-

lying epidermis was hyperplastic and hyperkeratotic.Mites of all stages could be seen in tiers at the junction

between the stratum corneum and stratum granulosum

(Fig. 4a). The epidermal tunnels were lined by flattened

parakeratotic cells and contained adult mites, nymphs

in various stages, 4–7 eggs and faeces. Fungal colonies,

pyknotic neutrophils and vacuolated epithelial cells

were enmeshed in the parakeratotic scales (Fig. 4b).

The mouthparts of occasional mites in the tunnels

faced the stratum granulosum and/or stratum spinosum,

excavating tunnels beneath the stratum corneum

(Fig. 4c). Parakeratotic epidermal cells and much of

the tunnel containing eggs and faeces, but without mites,

were located in the superficial hyperkeratotic stratumcorneum due to continual outgrowth of the epidermis.

Moderate spongiotic vesiculation and intraepidermal

abscesses were sporadically found in the epidermis

close to the mites. In areas of severe hyperkeratosisand epidermal hyperplasia, epidermal pegs were formed

extending deep into the dermis. Fibroplasia of the

superficial dermis was also a prominent change and

was accompanied by a slight inflammatory infiltrate of

neutrophils, lymphocytes and fibroblasts. Moderate

oedema was present in the papillary layer of the dermis.

The deepest layers showed proliferation of fibroblasts,

and the skin was thickened and packed with dermal

connective tissue. Some of the epithelial cells in the

affected hair follicles showed marked attenuation and

parakeratosis. Affected hair follicles were completely

disorganized, devoid of hair shafts and filled withsloughed keratinocytes, which accounted for the

alopecia. The dermal microvasculature in the papillary

layer was enlarged and prominent. Sebaceous glands

were generally hyperplastic, and the acini of apocrine

sweat glands were moderately dilated in severe lesions.

For the SEM examination, skin was fixed in 10%

glutaraldehyde. The stratum corneum and the surface

layer of the epidermis were removed by scraping or

sectioning parallel to the skin surface with a scalpel to

expose the mites in the burrows. After dehydration

through graded concentrations of ethanol, the tissue

was critical-point dried (CP 5A, Topcon, Tokyo, Japan)

using liquid carbon dioxide. Samples were mountedonto aluminium stubs with silver paste, sputtered with

gold in an ion coater (IB-3, Eiko Engineering, Tokyo,

Japan) and observed with a SEM (ABT-32, Topcon).

Figure 1. Adult male raccoon dog (Nyctereutes procyonoides) from

Kanagawa Prefecture, Japan infected with sarcoptic mange on the

neck, shoulders and thighs.

Figure 2. Lesions of sarcoptic mange on the neck. The dermatitis

is characterized by warty, cobblestone-like hyperkeratosis and

alopecia.

Figure 3. Photomicrograph of an adult female Sarcoptes scabiei

mite containing an egg from a skin scraping of a parasitized raccoon

dog in the study. Bar = 60 µm.




, 16

, 177–182

Sarcoptic mange in raccoon dogs 179

SEM revealed that the adult female mite was the stagemost commonly seen. Adult female mites were 320–

534 µ

m long and 229–378 µ

m wide (Fig. 5a). The

unsegmented pedicels of legs 1 and 2 of females had

suckers, and legs 3 and 4 ended in long trailing bristles

(Fig. 5b). The oviporus was on the ventral idiosoma

and showed a transversal cleft (Fig. 5b). The tarsi of

all legs had two blade-like claws. Large spines were

present on the central part of the dorsum and body

striations were prominent. The anus was located at the

posterior end of the body and was surrounded by

several short stout setae (Figs 6 and 7). Males were

smaller and had similar suckers on legs 1 and 2. Eggs

were oval and measured 107–115 µ

m by 78–80 µ

m.Some eggs had ridges running longitudinally on the

eggshell surface. Eggs were bundled together and fixed

to the burrow floor of an oviposition tunnel by fine

threads (Fig. 8). The mites were identified as S. scabiei

on the basis of these morphological features.

DISCUSSION

The epidermal histological findings in lesions of

sarcoptic mange were severe hyperkeratosis with par-

akeratotic crusting and thickening of the epidermis,

acanthosis, vesiculation and mites in the stratum cor-

neum. Dermal changes consisted of intradermal pro-

liferation of connective tissue, oedema in the papillary

layer and severe degenerative and necrotic changes of

the hair follicles. These histological aspects of sarcopticmange in raccoon dogs correspond to the classic

description of sarcoptic mange in dogs,

4

wild

5,6

and

domestic animals.

7

The marked atrophic hair follicles

Figure 4. Photomicrograph of skin section. (a) Low magnification showing hyperkeratotic epidermis, burrows with mites, acanthosis anddisorganized hair follicles devoid of hair shafts. H&E stain. Bar = 300 µm. Arrow head: mite. (b) Low magnification showing hyperkeratotic

epidermis with fungal colonies (outlined). H&E stain. Bar = 200 µm. Arrow head: mite. Inset: enlargement of outlined area revealing fungal

colonies. H&E stain. Bar = 15 µm. (c) Higher magnification of (a) showing a mite excavating a burrow. Note the capitulum, head (arrow) wedges

into the stratum granulosum. H&E stain. Bar = 30 µm. Arrow head: mite.

Figure 5. Scanning electron micrograph of an

adult female Sarcoptes scabiei mite. (a) Dorsal

idiosoma. Bar = 50 µm. ans: anus. (b) Ventral

idiosoma. The transverse cleft called the

tocostoma is seen going across the abdomen

(arrow). The tocostoma opens and widens as

two or three eggs are extruded each day.14

Bar = 50 µm.





, 16

, 177–182

accounting for the alopecia seen in these raccoon dogs

parallels the dermal changes reported from the domestic

and wild mammals with severe hyperkeratotic sarcopticmange. Skerratt et al.

suggested that the thick crusts

prevent hair regrowth.

8

The nutritional supply required

to meet proliferation of epidermal cells and fibroplasia

of the superficial dermis and exudation from fissures in

the skin must be large. This may change the haemody-

namics in the lesion, draining much more blood towards

the superficial dermis rather than hair follicles, causing

atrophy of the follicular sheath and follicular bulb,

resulting in hair loss. The accumulation of parakera-

totic cells in sarcoptic lesions in raccoon dogs parallels

that seen in domestic and wild mammals with severe

hyperkeratotic sarcoptic mange. Parakeratotic scales

in the stratum corneum corresponded to the previouspassage of scabies mites through the incompletely

differentiated layers of the epidermis.

9

Epidermal cells

surrounding this initial epidermolytic focus finally

underwent disturbed terminal differentiation and

appeared as parakeratotic cells. Hyperplastic sebaceous

glands and dilation of the acini of apocrine sweat

glands seen in raccoon dogs have been reported in pigs

with sarcoptic mange.

7

The gland openings may be

plugged by the hyperkeratotic crusts, causing dilation

of the glands. Bacterial infections in the dermis, which

occur following fissuring associated with crusting, allow

bacteria to infect internal organs.

8

Secondary bacterial

infections have been reported in humans,

11

wombats

8

and rabbits

10

with scabies. Bacterial infections associ-ated with exudates in the dermis may cause severe skin

malodour. It has been suggested that a great degree of

epidermal hyperplasia and infiltration of eosinophils

and neutrophils may be more characteristic of sarcoptic

mange than other pruritic ectoparasitisms. However, in

this series, we were not able to demonstrate increased

numbers of eosinophils. Morris suggested that the role

of tissue eosinophils in mediating immune responses

against parasites is less clear in sarcoptic mange.

4

In

many dermatological diseases, immunofluorescence can

demonstrate extensive deposition of eosinophil granule

proteins in tissues devoid of intense eosinophilic infil-trates.

12

With no evidence of mites, mite eggs or mite

faeces in histological sections, sarcoptic mange may be

confused with other dermatoses with pruritus, inflam-

mation and/or alopecia.

The host–parasite relationship in sarcoptic mange is

worth noting. To maintain survival in an epidermal

burrow, the female mite endures a conflict between

burrow construction and the shedding of the stratum

corneum.

13

Deposited eggs need 3–4 days to hatch, and

sexual maturation of the larvae and nymph take a further

6 days.

3

Acting against this is the epidermal turnover,

which normally occurs every 2 weeks. Thus, the female

mite digs her tunnel in the vertical plane with the mouthparts dipping into the stratum granulosum against the

outward flow of the stratum corneum.

9,13

Numerous

cuticular spines and scales extending post-laterally on

Figure 6. Scanning electron micrograph showing an adult female

mite depositing eggs (e) in the burrow behind her. The stratum

corneum was removed with a scalpel. Bar = 50 µm. ans: anus; epi:

epidermis; h: hair shaft; k: keratinocytes.

Figure 7. Scanning electron micrograph showing adult female mites

with their mouthparts directed to the end of the closed burrow.

Bar = 50 µm. ans: anus; k: keratinocytes.

Figure 8. Scanning electron micrograph showing eggs tied to each

other and on the burrow floor with fine thread. Various shrinkage on

the eggshell may represent the hatching process. Bar = 50 µm. epi:

epidermis; k: keratinocytes.




, 16

, 177–182

Sarcoptic mange in raccoon dogs 181

the dorsal idiosoma may play a role in preventing mites

from being pushed back by the epidermal outward flow.

The female mite digs her burrows by physically forcing

her way between the corneocytes, rather than chewing

a passage in termite fashion.

13,14

She ploughs with two

sets of powerful hind legs, and forward progress is

aided by the jaws and two cutting blade-like claws onthe elbows of the first two pairs of legs, similar to a

mole.

13,14

Scabiei eggs in the burrow are glued to each

other and on the burrow floor by a cement-like sub-

stance secreted by the ‘glue gland’ along the oviduct.

13

In addition, they are tied with fine threads to the bur-

row floor, presumably so as not to be dispersed.

This SEM study has clearly shown the mite and its

habitat and these ultrastructural observations will shed

light on the outlines seen under the light microscope by

clinicians. Description of the disease as it occurred in

the raccoon dog is very similar to what would corre-

spond to an epizootic of sarcoptic mange in humans,

9,10

dogs,

4

foxes,

5

ibex,

6

pigs

7

and wombats.

8

Sarcoptic

mange mites from different species tend to be morpho-

logically indistinguishable

3

and transmission of S. scabiei

var. canis

to raccoon dogs has been suggested.

1,2

Hence,

it is possible that the mites examined in this study could

be S. scabiei

var. canis

. Further investigations regard-

ing ‘variability’ of the mite among hosts are indicated.

REFERENCES

1. Ishihara T, Hirotani H. Problems caused by wild animals.

In: Mammals. Tokyo: Yurindo, 2003: 113–16 (in Japanese).

2. Takahasi M, Nogami S, Misumi H et al. Mange causedby Sarcoptes scabiei

(Acari: Sarcoptidae) in wild raccoon

dogs, Nyctereutes procyonoides

, in Kanagawa prefecture,

Japan. Journal of Veterinary Medical Science 2001; 63:

457–60.

3. Bornstein S, Mörner T, Samuel WM. Sarcoptes scabiei

and

sarcoptic mange. In: Pybus J & Kocan AA eds. Parasitic

Diseases of Wild Mammals, 3rd edn. Ames: Iowa State

University Press, 2001: 107–19.

4. Morris DO. A histomorphological study of sarcoptic

acariasis in the dog: 19 cases. Journal of the American

Animal Hospital Association 1996; 32: 119–24.

5. Little SE, Davidson WR, Rakich PM et al. Responses of red foxes to first and second infection with Sarcoptes sca-

biei

. Journal of Wildlife Diseases 1998; 34: 600–11.

6. León-Vizcaíno L, Ruíz de Ybáñez MR, Cubero MJ et al.

Sarcoptic mange in Spanish ibex from Spain. Journal of

Wildlife Diseases 1999; 35: 647–59.

7. Sheahan BJ. Pathology of Sarcoptes scabiei

infection in

pigs. Journal of Comparative Pathology 1975; 85: 87–95.

8. Skerratt LF, Middleton D, Beveridge L. Distribution of

life cycle stages of Sarcoptes scabiei

var wombati

and

effects of severe mange on common wombats in Victoria.

Journal of Wildlife Diseases 1999; 35: 633–46.

9. Van Neste D, Lachapelle JM. Host–parasite relationships

in hyperkeratotic (Norwegian) scabies: pathological andimmunological findings. British Journal of Dermatology

1981; 105: 667–78.

10. Arlian LG, Bruner RH, Stuhlaman RA et al. Histo-

pathology in hosts parasitized by Sarcoptes scabiei

. Journal

of Parasitology 1990; 76: 889– 94.

11. Burgess I. Sarcoptes scabiei

and scabies. Advances in

Parasitology 1994; 33: 234–92.

12. Leiferman KM. A current perspective on the role of

eosinophils in dermatologic diseases. Journal of the

American Academy of Dermatology 1991; 24: 1101–12.

13. Shelly WB, Shelly ED. Scanning electron microscopy of

the scabies burrow and its contents, with special reference

to the Sarcoptes scabiei

egg. Journal of the American

Academy of Dermatology 1983; 9: 673–79.14. Mellanby K. Biology of the parasite. In: Otkin M,

Maibach HI, Patish LC & Schwartzmann RM eds.

Scabies and Pediculosis. Philadelphia: J.B. Lippincott Co.,

1977: 8–16.

Résumé

Une infestation par Sarcoptes scabiei a été diagnostiquée chez trois raccoon (

Nyctereutes procyonoides

)

à la préfecture de Kanagawa, Japon. Les chiens présentaient une dermatose prurigineuse et alopéciante, avec une

alopécie des oreilles, du chanfrein, autour des yeux, sur les coudes et le cou, et des lésions croûteuses hyperpig-

mentées et malodorantes. Les ralages cutanés ont montré la présence de Sarcoptes scabiei

. L’Histopathologie

des lésions a montré une acanthose marquée, une hyperkératose, une parakératose et des éléments fongiques qui

ont été identifiés comme des Acremonium

sp., Alternaria

sp. et une espèce non connue. Des segments d’acariens

étaient localisés dans le stratum corneum et dans le stratum granulosum. Des tunnels ont été observés dans le

stratum corneum hyperkératosique. Une microscopie électronique (SEM) a montré un Sarcoptes scabiei

avec quatre

longs poils, des ventouses et des griffes sur les pattes 1 et 2, des épines cuticulaires, des stries proéminentes et un

anus terminal. En outre, la SEM a montré une femelle adulte creusant un tunnel avec la tête dirigée en profondeur.

Les tunnels étaient remplis d’oeufs, de débris de cornéocytes et de déjections fécales.

Resumen

Se diagnosticó una infestación por Sarcoptes en tres mapaches (Nyctereutes procyonoides) de

muerte reciente, de vida libre en la prefectura de Kanagawa, Japón. Los mapaches presentaban una enfermedad

prurítica y alopécica, con alopecia en los oídos, hocico, alrededor de los ojos, codo, muslo y cuello, y lesiones

hiperpigmentadas y costrosas con un fuerte olor. Los raspados cutáneos revelaron la presencia del ácaro

Sarcoptes scabiei

. La histopatología mostró acantosis marcada, hiperqueratosis, paraqueratosis, y elementos

fúngicos que fueron identificados posteriormente como sp. de Acremonium, Alternaria y un hongo desconocido.

Los segmentos de ácaro se situaban principalmente en el estrato córneo y también en el granuloso. Los túnelesse podían observar en el estrato córneo hiperqueratótico. La microscopía electrónica de barrido (SEM) reveló

un ácaro de Sarcoptes

en forma de tortuga, con cuatro cerdas largas, chupadores y garras en forma de cuchilla

en las patas 1 y 2, las espinas dorsales cuticulares, estriaciones prominentes del cuerpo, y un ano terminal.





, 16

, 177–182

Además, la SEM reveló un adulto hembra de ácaro cavando un túnel con la cabeza apostada al final del mismo.

Se observaron túneles llenos de las cáscaras de huevo, restos de corneocitos y heces.

Zusammenfassung Sarcoptes scabiei Infestation wurde bei drei kürzlich verstorbenen Marderhunden

(Nyctereutes procyonoides) in der Präfektur Kanagawa, Japan diagnostiziert. Die Marderhunde zeigten alopezische,

juckende Hauterkrankung mit Anzeichen von Alopezie im Bereich der Ohren, Schnauze, Augen, Ellbogen,

Oberschenkel und des Halses und hyperpigmentierte und verkrustete Hautläsionen, die einen starken Geruch

aufwiesen. Hautgeschabsel offenbarten das Vorhandensein von Sarcoptes scabiei -Milben. Histopathologie

der Läsionen zeigten deutliche Akanthose, Hyperkeratose, Parakeratose und Pilzelemente, die nachfolgend als

Acremonium sp., Alternaria sp und als eine unbekannte Pilzart identifiziert wurden. Milbensegmente waren

hauptsächlich im Stratum corneum lokalisiert wie auch im Stratum granulosum. Im hyperkeratotischen Stratum

corneum konnten Tunnel beobachtet werden. Rasterelektronenmikroskopie (SEM) zeigte Schildkröten-ähnliche

Sarcoptes scabiei mit vier langen Borsten, Saugwerkzeugen und schaufel-ähnlichen Klauen an den Beinen 1und

2, kutikulären Dornen, prominenter Körperstreifenbildung und einen terminalen Anus. Zusätzlich zeigte SEM

eine adulte weibliche Milbe, die einen Tunnel grub und dabei mit dem Kopf ganz am Ende einer geschlossenen

Höhle eingezwängt war. Die Tunnel warem mit Eischalen, Debris von Korneozyten und Kotkügelchen angefüllt.

Documents

Sarcoptic Mange in Free-ranging Raccoon Dogs (Nyctereutes Procyonoides) in Japan (Pages 177–182)