Post on 16-Jan-2023
HAIR-LOSS EPIZOOTIC IN MOOSE (ALCES ALCES) ASSOCIATED
WITH MASSIVE DEER KED (LIPOPTENA CERVI) INFESTATION
Knut Madslien,1,5 Bjørnar Ytrehus,1 Turid Vikøren,1 Jonas Malmsten,2 Ketil Isaksen,3
Hans Olav Hygen,3 and Erling J. Solberg4
1 Section for Wildlife Diseases, National Veterinary Institute, Pb 750 Sentrum, N-0106 Oslo, Norway2 Department of Pathology and Wildlife Diseases, National Veterinary Institute, SVA, SE-751 89 Uppsala, Sweden3 Climatology Division, Norwegian Meteorological Institute, Niels Henrik Abels vei 40, N-0313 Oslo, Norway4 Norwegian Institute of Nature Research, NO-7485 Trondheim, Norway5 Corresponding author (email: knut.madslien@vetinst.no)
ABSTRACT: Deer keds (Lipoptena cervi) are blood-sucking flies in the family Hippoboscidae;moose (Alces alces) are their main host in Scandinavia. There are no detailed reports of thenegative impacts of deer keds on moose. In 2006 and 2007, hunters in southeastern Norway andmidwestern Sweden found several moose cadavers with severe alopecia; numerous moose hadextensive hair loss. Between February 2006 and June 2007, materials from 23 moose weresubmitted for laboratory examination and large numbers of deer keds were found in the coat ofmost animals. The body condition of the moose varied but was poor in animals with severealopecia. The findings of enormous numbers of deer keds in the coat of the majority of the affectedanimals and a consistent histologic image (acute to chronic, multifocal to coalescing, eosinophilic tolymphocytic dermatitis), concurrent with the absence of any other lesions, trace elementdeficiencies, or dermal infections which are known to cause alopecia, suggest that the hair-lossepizootic was linked to massive infestations with deer keds. The emergence of this hair-losssyndrome implies that the dynamics between parasite and host have been disrupted by a currentlyunknown environmental or ecological factor. A high moose density, combined with extraordinarilymild weather June 2006–June 2007 and a particularly long period with the absence of night-frost inautumn of 2006, may have been ideal for deer ked development, survival, and optimal hostacquisition.
Key words: Alces alces, climate, deer ked, dermatitis, hair loss, Lipoptena cervi, populationdensity, pathology.
INTRODUCTION
The deer ked (Lipoptena cervi) is ablood-feeding ectoparasite that infests sev-eral cervid host species (Hackman et al.,1983). Deer ked females are viviparous andproduce new prepupae throughout theyear. Fully developed pupae passively dropout of the coat to the ground where theydevelop into winged imagos in late summerand early autumn. When the imagos reachtheir hosts, they lose their wings andremain on the same host for the rest oftheir lives (Haarløv, 1964). Keds have beenpresent in continental Europe since thestone age (Gothe and Schol, 1994) andwere described in southern Sweden asearly as 1758 (Linne, 1758). This parasitehas expanded its distribution west andnorthward in Scandinavia over the lastfew decades and is now abundant insoutheastern Norway and central Sweden(Fig. 1) (Valimaki et al., 2010). Factors
contributing to the increase in deer keddistribution and abundance are not fullyelucidated, although increases in hostanimal populations and changes in climatehave been suggested (Valimaki et al., 2010).
The deer ked is not reported to causedisease in the host (Allan, 2001), althoughStrose (1916) blamed the parasite forcausing focal hair loss and eczema in reddeer (Cervus elaphus). Darling (1963)reported that red deer seemed not toreact strongly to the deer ked but arguedthat the effect on the host must beconsiderable, without further describingthe cases. Fatigue and growth retardationhave been seen in fallow deer (Damadama) experiencing massive infestations ofdeer keds (Ivanov, 1974). Laaksonen(2009) reported that semidomesticatedreindeer (Rangifer tarandus) showed pru-ritus and developed focal alopecia afterinfestation with deer keds.
Journal of Wildlife Diseases, 47(4), 2011, pp. 893–906# Wildlife Disease Association 2011
893
We describe the clinical and pathologicfindings associated with epizootic hair lossamong moose in areas of southeastern Nor-way and midwestern Sweden where the deerked is abundant. We discuss to what degreethe hair-loss syndrome was associated withdeer ked infestation and to what extent localmoose population densities and weatherconditions were factors in the outbreak.
MATERIALS AND METHODS
Study area
The study area was in southcentral Scandina-via (59u069–62u169N, 10u279–15u139E; Fig. 1).The elevation ranges from sea level in thesouthwest to about 600 m in the north, coveringboth the middle boreal, southern boreal, andboreonemoral vegetation zones (Moen, 1998).The landscape is undulating with forest-coveredhills and some farmland in intersecting valleys.Forests are dominated by Scots pine (Pinussylvestris) and Norway spruce (Picea abies) and,to some extent, birch (Betula spp.).
Affected population
The moose population of the study area ismainly limited (and regulated) by hunting.Predation by wolves (Canis lupus) and a few
brown bears (Ursus arctos) also may have someimpact on the population (Sand et al., 2008).
Body mass and reproductive rates of mooseare relatively high, but variable, throughout thestudy area. Observations by moose hunterssuggest a decline in body condition during thelast 15 yr, particularly in the north (Solberget al., 2010). The decline is associated withincreasing population density and is thought tobe caused by food limitation (Lavsund et al.,2003). Data from radio-collared moose indicatethat moose in this area are sedentary (Lavsundet al., 2003). Moose population density in thestudy area is higher than the average forScandinavia. On a regional (county) scale,hunters harvested, on average, about 0.3–0.6moose per km2 of forest and bogs in 2000–2007(Solberg et al., 2010). During the same period,we estimated the preharvest moose density wasabout 1.0–1.4 adult ($1 yr old) moose per km2
(E.J. Solberg, unpubl. data).
Data collection
Nonconfirmed observations of alopecicmoose were based on phone and email corre-spondence with the National Veterinary Insti-tutes in Oslo, Norway (NVI) and Uppsala,Sweden (SVA). To estimate the prevalence ofalopecia in the moose population in Septemberand October 2007 and 2008, moose hunters infive Norwegian counties, representing areaswithin and outside the deer ked distributionrange, were asked to complete a questionnaireduring the moose hunting season. They wereasked to note if they had observed moose withhair loss and to classify the pattern of alopecia ona scale from 0 (no hair loss) to 5 (complete hairloss) according to a figure (Fig. 2). In March2007, two cows and one subadult with severehair loss were fitted with radio collars in Arjang,Sweden (Fig. 3a). The development of hair losswas monitored in these three animals; bloodsamples for hematology were drawn from thejugular vein at the time radio collars were fitted.
Specimen analysis
The patho-anatomical part of the study wasbased on an examination of material fromcarcasses and biopsy material from alopecicmoose submitted to NVI and SVA from thestudy area from February 2006–June 2007(Fig. 1, Table 1). In the laboratory, wholecarcasses were carefully inspected and de-scribed before the hide was removed andexamined. A full necropsy was performed andsamples of lung, heart, liver, kidney, brain,lymph nodes, thyroid gland, adrenal gland,and skin were collected and fixed in 10%neutral buffered formalin, dehydrated and
FIGURE 1. A map of southeastern Norway andmidwestern Sweden. Dark grey color representsmunicipalities with laboratory-confirmed cases ofalopecia caused by deer keds (Lipoptena cervi) inmoose (Alces alces), 2006–2007. Light grey repre-sents municipalities with observed severe alopecicmoose in the field. The known distribution of deerked in Norway is east of the dotted line.
894 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011
embedded in paraffin, sectioned at 5 mm, andstained with hematoxylin and eosin and vanGieson for histologic examination. Standardbacteriologic examination on calf blood agarplates was performed on samples from liver(n512), spleen (n59), and skin (n514). Theplates were incubated aerobically at 37 C andexamined after 24–48 hr. Biopsies from bothaffected and normal skin were collected forroutine parasitologic (n511) and mycologic(n515) examination. All visible deer keds andpupae in the coat of four animals werecollected and counted. Liver samples from
FIGURE 3. (A) Adult, female moose (Alces alces)with typical pattern of alopecia, radio collared inMarch 2007 in Varmland county, Sweden. (B) Thesame moose, in September 2007, showing regrowthof the coat on neck and withers. Photo: GunnarGloersen, Swedish Hunters Association.
r
FIGURE 2. Alopecia in moose (Alces alces), asassessed by hunters in the field during the 2007and 2008 hunting seasons in Norway and Sweden: 1)No visible hair-loss, 2) slight hair loss; spots ofalopecia affecting about 5 to 20%, especially thoraxand ventral neck, 3) moderate hair loss; about 30 to40% of coat lost and remaining coat sparse, 4) severehair loss, about 40 to 80% of coat lost, 5) nakedmoose; more than 80% hair loss. Figure inspired byfigure 1 in Samuel (1989).
MADSLIEN ET AL.—HAIR-LOSS EPIZOOTIC IN SCANDINAVIAN MOOSE 895
TA
BL
E1.
Ch
ron
olo
gic
list
ing
of
moose
(Alc
esal
ces)
rece
ived
for
lab
ora
tory
exa
min
atio
nd
uri
ng
anou
tbre
akof
alop
eci
ain
sou
theas
tern
Norw
ayan
dm
idw
est
ern
Sw
ed
en
in2006–2007.
No
.C
oll
ect
ion
dat
eL
oca
tio
na
Sexb
Age
cE
uth
aniz
ed
Weig
htd
Am
ou
nt
of
deer
ked
seA
lop
eci
afG
ross
lesi
on
s
12/1
3/2
006
Mar
ker
FS
ub
adu
lt(1
,5)
Yes
210
Lar
ge
3N
on
e2
10/2
5/2
006
Røm
skog
FA
du
ltY
es
—L
arge
3N
on
e3
12/7
/2006
Røm
skog
FC
alf
(0,5
)N
o—
Lar
ge
3N
on
e4
12/1
5/2
006
Fil
ipst
adF
Ad
ult
Yes
—M
od
era
te3
Non
e5
12/2
0/2
006
Arj
ang
MS
ub
adu
lt(1
,5)
Yes
—L
arge
3N
on
e6
1/8
/2007
Røm
skog
FA
du
ltY
es
365
Lar
ge
(11,0
14)
4N
on
e7
1/2
2/2
007
Au
rskog-H
øla
nd
FA
du
lt(1
8)
Yes
290
Lar
ge
(16,4
96)
4S
oli
tary
fib
rop
apil
lom
as8
1/2
9/2
007
Røm
skog
FA
du
ltY
es
390
Lar
ge
(5,9
38)
3N
on
e9
2/1
2/2
007
Au
rskog-H
øla
nd
FS
ub
adu
lt(2
)Y
es
240
Lar
ge
3N
on
e10
2/1
2/2
007
Au
rskog-H
øla
nd
FA
du
ltY
es
350
Lar
ge
3S
oli
tary
kid
ney
cyst
s11
2/1
5/2
007
Ren
dal
en
MS
ub
adu
lt(2
)Y
es
—N
on
e3
Non
e12
2/2
6/2
007
Ren
dal
en
MS
ub
adu
lt(2
)Y
es
290
Non
e2
Non
e13
3/1
/2007
Au
rskog-H
øla
nd
FA
du
lt(5
)Y
es
330
Lar
ge
3N
on
e14
3/1
/2007
Au
rskog-H
øla
nd
FS
ub
adu
ltY
es
110
Lar
ge
(10,6
87)
1N
on
e15
3/2
/2007
Nan
nest
adF
Ad
ult
(9)
No
170
Non
e3
Non
e16
3/1
2/2
007
Eid
skog
FA
du
ltY
es
—L
arge
2N
on
e17
5/2
/2007
Au
rskog-H
øla
nd
MA
du
ltY
es
350
Mod
era
te3
Gen
era
lize
dfi
bro
pap
illo
mat
osi
s18
5/1
1/2
007
Au
rskog-H
øla
nd
FA
du
lt(1
2)
Yes
360
Sm
all
4F
ron
tle
gfr
actu
re(h
itb
yca
r)19
5/2
1/2
007
Nit
ted
alM
Su
bad
ult
(2)
Yes
180
Sm
all
4N
on
e20
5/2
1/2
007
Au
rskog-H
øla
nd
FA
du
lt(2
2)
Yes
275
Lar
ge
3M
alig
nan
tetm
oid
altu
mor
21
6/8
/2007
Fro
gn
MA
du
lt(1
0)
Yes
330
Non
e4
Peru
ke
antl
ers
22
6/2
0/2
007
Au
rskog-H
øla
nd
FA
du
ltY
es
325
Non
e3
Non
e23
6/2
8/2
007
Au
rskog-H
øla
nd
MA
du
lt(5
)Y
es
350
Non
e3
Soli
tary
fib
rop
apil
lom
as
aM
un
icip
alit
yin
No
rway
and
Sw
ed
en
.b
M5
mal
e;
F5
fem
ale.
cIn
bra
ckets
,est
imat
ed
age
bas
ed
on
den
tal
cem
en
tum
ann
uli
cou
nts
.d
Inkil
ogra
ms,
das
hin
dic
ates
weig
ht
was
no
tm
eas
ure
d.
eIn
bra
ckets
,to
tal
cou
nt
of
deer
ked
s.f
Degre
eo
fal
op
eci
ab
yra
nge;
1(n
orm
alco
ated
)to
5(n
aked
);se
eF
igu
re2
for
deta
ils.
896 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011
12 moose were frozen at 220 C prior tocarrying out trace element analysis for copper,selenium, and cobalt (Vikøren et al., 2005).
Meteorologic data collection
We used meteorologic data from Garder-moen (elevation: 202 m) weather station,which is representative for the inland areasof southeastern Norway and adjacent areas ofSweden. Gardermoen is an automated weath-er station that provides hourly measurementsof precipitation, temperature, humidity, wind,and pressure. Prior to 2009, these variableswere measured manually every 3–6 hr, de-pending on weather and time of day. Wewanted to elucidate factors that may influenceoff-host survival and development of deerkeds, as well as host acquisition of wingedkeds. Temperature influences deer ked devel-opment (Harkonen et al., 2010) and repeatedfreezing and thawing may be unfavorable forparasite survival (Davidson et al., 2008), withthe pupal stage on the ground being mostvulnerable. Hence, we looked at the depth andduration of snow cover and temperaturefluctuations around zero degrees C. Warmand sunny weather may facilitate host acqui-sition by winged keds, while frost is probablyless beneficial; therefore, we also includeddegree-days (daily mean temperature multi-plied by the number of days), length ofgrowing season (sum of days with daily meantemperature .5 C), precipitation, and firstfrost in the autumn.
RESULTS
Field observations
Earlier reports of alopecia in moose inthe study area are scarce. On February 13,2006, wildlife managers in Marker munic-ipality, Norway (Fig. 1), reported a sub-adult, female moose with severe hair loss,emaciation, and abnormal behavior. Theanimal was euthanized after seeking shel-ter in a farm building and submitted toNVI for necropsy (moose 1, Table 1). InOctober 2006, wildlife managers in theneighboring municipality of Rømskog(Fig. 1) reported that five of 60 huntedmoose had severe hair loss and thatmoose, in general, were severely infestedwith deer keds. Skin samples from one ofthe alopecic moose were submitted to NVI(moose 2, Table 1). In November and
December 2006, 11 alopecic moose werereported in the same area; three werefound dead and eight were euthanized (J.Moen, pers. comm.). In Sweden, betweenArjang and Filipstad (Fig. 1), hunterseuthanized 12 and observed another 50moose with severe hair loss during theautumn of 2006 and winter of 2007 (G.Gloersen, pers. comm.). From December2006 to June 2007, skin samples or wholecarcasses from an additional 21 moose(moose 3–23), representing seven differ-ent municipalities in the study area inNorway and two in Sweden, were submit-ted to NVI and SVA (Table 1). During thisperiod, wildlife managers and laymen alsoreported observations of alopecic moose inanother nine municipalities; two in Feb-ruary, one in March, three in April, andthree in May (Fig. 1). According to thereports, severely alopecic moose seemedto be in poor condition and did notrespond to human activity. Pruritus, how-ever, was not observed.
Necropsy findings
Seventeen whole carcasses and biopsymaterial from six animals were submittedto NVI (n521) and SVA (n52) from thestudy area from February 2006–June 2007(Fig. 1). Twenty of the animals wereeuthanized because of severe alopecia,two were found dead, and one (moose 14)was a normally coated calf, shot simulta-neously with a female alopecic moose.
The necropsy of the index case (moose1, Table 1) revealed severe, bilateralalopecia and moderate, crusting dermatitisinvolving the cheeks, ventral neck, lateralthorax, abdomen, and haunch. A largenumber of deer keds were observed onthe carcass, most in areas that were stillcovered with hair. The lymph nodes of thebody were generally enlarged, but noother specific gross lesions were noted.Histologic examination of alopecic areasrevealed moderate and diffuse orthoker-atotic hyperkeratosis and diffuse, moder-ate hyperplasia of the epidermis, withmoderate formation of rete ridges (Fig. 4).
MADSLIEN ET AL.—HAIR-LOSS EPIZOOTIC IN SCANDINAVIAN MOOSE 897
The hair follicles showed moderate kera-tosis, with the infundibulum of the major-ity of the follicles dilated with keratinplugs of exfoliated corneum and debris.The hair bulbs had the appearance of‘‘flame follicles’’ (i.e., follicles morpholog-ically characterized by excessive trichilem-
mal keratinization, giving the impressionof a flickering flame). Sebaceous andsweat glands appeared relatively normalbut had prominent, thickened basal mem-branes. The dermis showed increasedcellularity consisting of diffuse, mild tomoderate infiltrates of eosinophilic granu-
FIGURE 4. Skin histology of alopecic moose (Alces alces). (a) Sparse coat; inflammatory infiltrates indermis, flame follicles, and follicular keratosis. (b) Sparse coat; perivascular infiltration of eosinophils,macrophages, and plasma cells. (c) Alopecic skin, orthokeratotic hyperkeratosis, acanthosis, intracornealpustule, and follicular keratosis. (d) Sparse coat; orthokeratotic hyperkeratosis, perivascular infiltration ofeosinophils, macrophages, and plasma cells and a follicle filled with these cells. (e) Alopecic skin; acanthosis,dermal fibrosis, and perivascular infiltration of macrophages and lymphocytes. (f) Sparse coat; acanthosis, andfibrosis. a, b, c5moose 6 (see Table 1), d5moose 16, e5moose 18, f5moose 20. All are hematoxylin andeosin-stained sections, except for f, which is van Gieson stained. Bar5100 mm in all sections.
898 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011
locytes, macrophages, plasma cells, andlymphocytes. A diffuse, mild edema and adiffuse, moderate increase in the amountof regularly organized connective tissue inthe dermis were also observed. The vesselsof the dermis appeared contorted andwere characterized by hypertrophic endo-thelium with prominent nuclei and athickened basal membrane. In areaswhere some hair was still present, the skinwas characterized by mild, diffuse ortho-keratotic hyperkeratosis, a mild focalhyperplasia of the epidermis, and occa-sional intraepidermal pustules. The chang-es in the dermis were similar to those inalopecic areas, but the increase in con-nective tissue was less prominent andcharacterized by irregularly organizedfibers.
The macroscopic changes in animalnumbers 2–23 showed large similaritieswith each other and with the casedescribed above. The general pattern wasbilateral, fairly symmetric alopecia on theventral neck, sides, and abdomen whilethe dorsal neck, back, and limbs showedless-prominent hair loss. Moose 14 did notshow alopecia but had skin changes asdescribed below. In the alopecic animals,the naked skin showed varying degrees ofhyperpigmentation (increasing with daylength) and was diffusely thickened andcovered by light, removable crusts butappeared otherwise relatively smooth anddid not show obvious papules, erythema,or erosive ulcerative lesions. Althoughsingle hairs were broken, the generalimpression was that hairs were eitherpresent at full length or not present. Selftrauma, consistent with scratching, wasnot a common finding. The remaining haircoat appeared dull and the hairs wereeasily epilated. Ked infestation was con-firmed in the majority of cases (17 of 23;Table 1). Keds were distributed through-out the animal, except distally on thelimbs, but only a few specimens werefound in alopecic areas. The keds aggre-gated in the axillae, neck, groin, andperineal region. In fresh carcasses, the
insects were located on the surface of theskin, their head oriented towards the skin,while they crawled out on the protectivehairs as the carcass cooled. The woolenhairs of severely infested animals weresmeared with a reddish-brown, dust-likematerial, probably deer ked feces mixedwith moose blood. The infestation inten-sity was highest in the animals examined inDecember–February (2006–2007), whilefew deer keds were found in May andJune 2007. The body condition of themoose varied, although it was poor in theanimals with severe alopecia, and therewere no consistent changes in the internalorgans.
Histologic presentation varied depend-ing on the month of examination. Ingeneral, histologic examination of theskin revealed a mild to moderate diffuseorthokeratotic hyperkeratosis and mild tomoderate multifocal to diffuse hyperplasiaof the epidermis (acanthosis). In somecases, affected epidermis showed multifo-cal small ulcerations, micropustules, andserocellular crusts. The dermis was charac-terized by multifocal to coalescing, mild tomoderate infiltrates of inflammatory cells.The infiltrates had a perivascular distributionand were found in both the superficial andthe deep dermis. During the first half of theepizootic, they were dominated by eosino-philic granulocytes while lymphocytes, mac-rophages, and plasma cells were moreprominent in the spring and early summer.Blood vessels adjacent to inflammatoryinfiltrates were contorted and showed endo-thelial hypertrophy. Inflammatory changeswere most severe and acute in areas with aremaining coat, while alopecic areas wereoften characterized by milder, mononuclearinfiltrates. Increased amounts of irregularlyorganized connective tissue (fibrosis) weremost pronounced in chronic cases (i.e., in latewinter and spring) and in denuded areas.During autumn, winter, and early spring thehair follicles appeared as flame follicles.However, in May–June, a gradual shift toanagen follicles was observed (Table 2). Thedensity of follicles and dermal papillae did
MADSLIEN ET AL.—HAIR-LOSS EPIZOOTIC IN SCANDINAVIAN MOOSE 899
TA
BL
E2.
Su
mm
ary
of
his
tolo
gic
eva
luat
ion
of
skin
sam
ple
sfr
om
moose
(Alc
esal
ces)
rece
ived
for
lab
ora
tory
exa
min
atio
nd
uri
ng
anou
tbre
akof
alop
eci
ain
sou
theas
tern
Norw
ayan
dm
idw
est
ern
Sw
ed
en
in2006–2007.
No
.
Ep
iderm
isD
erm
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Hai
rfo
llicl
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tosi
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sis
Fib
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s
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rity
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min
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1D
iffu
se,
mod
cD
iffu
se,
mod
cM
od
cM
ult
ifoca
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coal
esc
ing
Mild
tom
odc
Eosi
nop
hil
s,m
acro
ph
ages,
lym
ph
ocy
tes,
pla
sma
cell
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lam
e
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mod
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ild
Mu
ltif
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lto
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Mild
tom
odc
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ph
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lym
ph
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sma
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e
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ifoca
l,m
ild
Mil
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l,p
eri
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ula
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ild
Eos
inop
hlis
,mac
rophag
es,p
lasm
ace
llsF
lam
e4
Dif
fuse
,m
ild
No
Mil
dM
ult
ifoca
l,p
eri
vasc
ula
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ild
Eos
inop
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,mac
rophag
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od
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ild
Multifoc
alto
coal
esci
ng,
per
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od
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,mac
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lam
e6
Dif
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ild
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ng,
per
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od
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ild
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ng,
per
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od
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ild
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ace
llsF
lam
e9
Dif
fuse
,se
vere
Dif
fuse
,m
ild
Mil
dM
ultifoc
alto
coal
esci
ng,
per
ivas
cula
rM
od
Lym
ph
ocy
tes,
pla
sma
cell
sF
lam
e10
Dif
fuse
,m
od
cD
iffu
se,
mil
dM
ild
Multifoc
alto
coal
esci
ng,
per
ivas
cula
rM
od
Lym
ph
ocy
tes,
pla
sma
cell
sF
lam
e11
Dif
fuse
,m
od
cM
ult
ifoca
l,m
ild
Mil
dIn
sign
ific
ant
inflam
mat
ory
infiltra
tion
Fla
me
12
Dif
fuse
,m
od
cM
ult
ifoca
l,m
od
cM
ild
Insi
gnific
ant
inflam
mat
ory
infiltra
tion
Fla
me
13
Dif
fuse
,m
od
cM
ult
ifoca
l,m
od
cM
od
cM
ultifoc
alto
coal
esci
ng,
per
ivas
cula
rM
ild
Lym
ph
ocy
tes,
pla
sma
cell
sF
lam
e14
Dif
fuse
,m
od
cM
ult
ifoca
l,m
od
cM
ild
Mu
ltif
oca
lto
coal
esc
ing
Mod
Eosi
nop
hil
sF
lam
e15
Dif
fuse
,m
ild
Mu
ltif
oca
l,m
ild
No
Insi
gnific
ant
inflam
mat
ory
infiltra
tion
Fla
me
16
Dif
fuse
,m
od
cM
ult
ifoca
l,m
od
cM
ild
Mu
ltif
oca
lto
coal
esc
ing
Mod
Eos
inop
hils
,mac
rophag
es,p
lasm
ace
llsF
lam
e17
Dif
fuse
,m
ild
Dif
fuse
,m
ild
Mod
cM
ult
ifoca
l,p
eri
vasc
ula
rM
ild
Mac
rophag
es,l
ymphoc
ytes
,pla
smac
ells
Fla
me
and
anag
en18
Dif
fuse
,m
ild
Dif
fuse
,m
od
cM
od
cM
ult
ifoca
l,p
eri
vasc
ula
rM
od
Mac
rophag
es,l
ypm
hoc
ytes
,pla
smac
ells
Fla
me
and
anag
en19
Dif
fuse
,m
ild
Dif
fuse
,m
od
cM
od
cM
ult
ifoca
l,p
eri
vasc
ula
rM
ild
Lym
phoc
ytes
,pla
sma
cells
,neu
trop
hils
Fla
me
and
anag
en20
Dif
fuse
,m
od
cM
ult
ifoca
l,m
ild
Mil
dM
ult
ifoca
l,p
eri
vasc
ula
rM
ild
Lym
ph
ocy
tes,
pla
sma
cell
sF
lam
ean
dan
agen
21
No
Dif
fuse
,m
od
cM
od
cM
ult
ifoca
l,p
eri
vasc
ula
rM
ild
Lym
phoc
ytes
,pla
sma
cells
,neu
trop
hils
An
agen
22
No
Dif
fuse
,m
od
cM
ild
Mu
ltif
oca
l,p
eri
vasc
ula
rM
od
Lym
phoc
ytes
,pla
sma
cells
,neu
trop
hils
An
agen
23
No
Dif
fuse
,m
od
cM
ild
Mu
ltif
oca
l,p
eri
vasc
ula
rM
ild
Lym
phoc
ytes
,pla
sma
cells
,neu
trop
hils
An
agen
aO
rth
okera
toti
ch
yperk
era
tosi
s.b
Do
min
atin
gh
air
cycl
est
age
inco
nto
ur
hai
rs.
cM
od
5m
od
era
te.
900 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011
not show any obvious association withalopecia, deer ked infestation, or time of year.
Parasitologic examination
Seven of the 11 skin samples examinedfor ectoparasites other than deer keds werenegative, while low numbers of Chorioptesspp. were found in four animals.
Microbiologic culture results
Most skin samples had negative bacterialcultures, although Staphylococcus aureus(n56), Streptococcus agalactiae (n52),Pasteurella multocida multocida (n51)and Clostridium perfringens (n51) wereisolated from some skin samples. Mycolo-gic examinations were negative except forone moose on which Scopulariopsis brevi-caulis was isolated.
Trace elements
Liver concentrations (mg/g wet weight)of trace elements were (mean6SEM):cobalt 0.1160.01, selenium 0.9760.20,and copper 74.867.98.
Observations and blood analysis ofcaptured moose
Hemoglobin values from the capturedanimals in March 2007 were 124, 144, and145 g/l (normal range: mean6SD 125.5 6
9.9; Adolfsson, 1993). In September 2007,both radio-collared cows were observedand appeared healthy with a coat, al-though slightly sparse, covering formerdenuded areas (Fig. 3b).
Observations during hunting seasons 2007and 2008
In Norway, 16,845 moose were ob-served and reported in the questionnaireanswered by moose hunters in autumn2007. Twenty (0.12%) animals had alope-cia (nine adult females, eight adult males,two calves, and one animal with ageunclassified). Of these, 15 were scored ashaving grade 2 alopecia while the remain-ing five were scored as grade 3. In 2008,only one (subadult female) of 15,136(0.007%) was alopecic (grade 2).
Weather
Weather conditions for winter 2005–2006 were fairly normal, but summer andautumn 2006 were milder than normal(Table 3). The 365-day running mean airtemperature for the period from 11 June2006–10 June 2007 was by far the highestsince records at Gardermoen began in 1940(Fig. 5a). The temperature was threestandard deviations above the correspond-ing mean temperature of the normal period(1961–1990). Furthermore, autumn 2006was characterized by an extraordinarily latearrival of the first frost night after August 1(87 days, average is 47; Fig. 5b).
DISCUSSION
Based on the pathologic skin changes ofalopecic moose, the massive deer kedinfestation in affected animals, and theabsence of findings indicative of any otherconsistent factor (other ectoparasites, in-fectious agents, endocrine disorders, ordeficiencies) that could be a plausiblecause of such a condition, we concludethat severe deer ked infestation was a keyfactor in the current outbreak. However,deer keds were not found on two alopecicbulls from Rendalen, north of the deerked distribution range (Fig. 1) nor on four(one in March, three in June) alopecicanimals inside the deer ked area. Youngmoose bulls can disperse considerabledistances (up to 250 km) from their birtharea before they establish a more perma-nent home range (Hundertmark, 2007).Hence, the two bulls from Rendalen mayhave been born within the deer ked rangeand may have experienced massive deerked infestation as calves before dispersal.The hair loss in these two animals may, assuch, represent chronic, partially healedlesions. The absence of the parasite in thelast three cases may be explained by thedeer ked life cycle; the adult ectoparasitesare thought to die during spring andsummer (Haarløv, 1964).
In Canada, premature winter hair lossin moose associated with the presence of
MADSLIEN ET AL.—HAIR-LOSS EPIZOOTIC IN SCANDINAVIAN MOOSE 901
TA
BL
E3.
Sele
cted
mete
oro
logic
dat
afo
r2000–2010
from
Gar
derm
oen
weat
her
stat
ion
(ele
vati
on
:202
m),
Norw
ay,
rep
rese
nta
tive
for
the
inla
nd
areas
of
sou
theas
tern
Norw
ayan
dad
jace
nt
areas
of
Sw
ed
en
.T
he
autu
mn
of
2006
(bold
typ
e)
was
char
acte
rize
db
yh
igh
nu
mb
ers
of
deer
ked
sin
the
stu
dy
area.
Year
Pre
vio
us
win
tera
—p
up
alsu
rviv
alS
um
merb
—p
up
ald
eve
lop
men
tA
utu
mn
c—
swar
min
go
fad
ult
s
Day
sw
ith
sno
wfa
lld
Sn
ow
sum
e
Melt
ing–
freezi
ng
ep
iso
des
Len
gth
of
gro
wth
seas
on
f
Mean
tem
pera
ture
ingro
wth
seas
on
Degre
e-d
aysg
ingro
wth
seas
on
Degre
e-d
ays
abo
ve5
Cin
gro
wth
seas
on
Mean
tem
pera
ture
inau
tum
nD
egre
e-d
ays
inau
tum
n
Degre
e-d
ays
abo
ve5
Cin
autu
mn
Pre
cip
itat
ion
hD
ays
befo
refr
ost
i
2000
17
1,0
68
72
209
13.0
1,5
46.2
951.2
9.9
1,0
56.9
535.5
455.9
123
2001
27
3,1
51
57
179
13.1
1,5
08.0
933.5
9.3
998.6
543.5
320.7
56
2002
20
1,6
41
64
174
13.9
1,7
14.3
1,1
00.4
8.7
928.8
636.3
193.5
54
2003
32
5,0
70
58
181
13.5
1,6
55.1
1,0
57.6
8.6
920.9
535.4
176.4
33
2004
61,5
86
63
200
12.8
1,6
62.2
1,0
16.0
9.8
1,0
48.2
580.2
273.9
62
2005
11
819
73
188
12.3
1,5
67.0
940.0
10.0
1,0
45.0
585.1
307.8
48
2006
22
3,8
71
64
185
14.6
1,6
78.2
1,1
06.1
10.7
1,1
40.7
703.3
392.3
87
2007
20
1,1
68
71
217
12.1
1,7
17.7
1,0
36.0
8.8
945.5
511.1
161.3
47
2008
22
751
78
192
13.6
1,6
33.4
1,0
36.9
8.4
901.3
462.4
318.6
61
2009
25
3,8
16
60
173
12.9
1,6
41.3
1,0
07.7
8.3
889.4
500.2
265.5
60
2010
NA
jN
Aj
43
167
13.4
1,5
00.9
950.5
8.0
857.5
469.9
250.5
59
Norm
alk
27
5,9
70
63
170
13.0
1,4
38.9
890.0
8.0
860.3
453.9
298.0
46.9
SD
l8
3,0
22
15
17
1.0
105.0
90.5
0.9
95.4
63.7
106.5
11
aF
rom
No
vem
ber
(year
befo
re)
toA
pri
l.b
Fro
mo
nse
to
fgro
wth
seas
on
to1
5A
ugu
st.
c1
Au
gu
st–
15
No
vem
ber.
dS
no
wfa
ll5
bo
thin
creas
ed
sno
wd
ep
than
dp
reci
pit
atio
nth
esa
me
day
.e
Sn
ow
sum
5d
aily
sno
wd
ep
thm
ult
ipli
ed
by
day
s(e
.g.,
10
cmsn
ow
dep
thfo
r1
0d
ays5
10
0-c
md
ays)
.f
Gro
wth
seas
on
5su
mo
fd
ays
wit
hd
aily
mean
tem
pera
ture
.5
C.
gD
egre
e-d
ays5
the
dai
lym
ean
tem
pera
ture
mu
ltip
lied
by
day
s(e
.g.,
10
Cfo
r1
0d
ays5
10
0-d
egre
ed
ays)
.h
Pre
cip
itat
ion
5d
aily
pre
cip
itat
ion
inm
illi
mete
rs.
iD
ays
fro
m1
Au
gu
stto
firs
tep
iso
de
wit
hte
mp
era
ture
belo
w0
C.
jN
A5
no
tav
aila
ble
.k
Mean
valu
ein
the
no
rmal
peri
od
19
61
–1
99
0.
lS
D5
stan
dar
dd
evi
atio
n.
902 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011
the winter tick (Dermacentor albipictus)has been described (McLaughlin andAddison, 1986). The winter tick wasreported once in Norway, found on animported horse from the USA, but theparasite is currently not present (Lillehauget al., 2002).
Chorioptes spp. may cause skin lesionsin the outer ear canal of moose (Hestvik etal., 2007) and have also been associatedwith single cases of generalized alopecia inmoose in Norway and Sweden. Histolog-ically, the ear skin lesions caused by this
mite seem quite similar to those seen inour study. However, moose with massiveChorioptes infestation typically show apatchy pattern of alopecia, compared tothe confluent pattern seen in the currentoutbreak. Also, Chorioptes was not foundin the majority of our cases. Otherectoparasites known to cause alopecia incervids, including chewing lice (Cervicolasp.; Bildfell et al., 2004), sarcoptic mange(Sarcoptes scabiei; Bornstein et al., 2001),and mites of the genus Demodex (Genteset al., 2007) were not found in our study.
Several endocrine dermatopathiescause alopecia in cattle, among themhypovitaminosis A and hypothyroidism(Ginn et al., 2007). Blood plasma levelsof vitamin A and thyroxin were notexamined in our material, but the histo-logic changes were not consistent with anendocrine dermatopathy. Deficiencies ofcopper (Frank, 1998) and cobalt (Kennedyet al., 1997), and selenium intoxication(Kaur et al., 2003), are reported to beassociated with alopecia in animals. In ourstudy, these trace elements were not attoxic or deficient levels based on the NVI’scriteria set for cattle.
In Belarus, Ivanov (1974) reported thatall moose hunted during the autumnharbored deer keds in their coat with anaverage of about 1,000 keds per moose. InFinland, average numbers of keds innormally coated cows and calves were3,549 and 1,730, respectively (Paakkonenet al., 2010). We found 16,496, 11,014,and 5,938 keds in the coats of three cowswith severe hair loss and 10,687 in the coatof a calf with a normal coat (Table 1). Weconsider these numbers to be very high,taking into account that keds preferhabitats with hair-covered skin (Haarløv,1964), and it can be presumed that amajor proportion of the initial ked popu-lation may have been lost together withthe hair. Consequently, perhaps the highdensity of deer keds, biting and feeding15 to 20 times per day (Ivanov, 1974),exceeded a threshold of what moose skincould tolerate, thus triggering a cascade of
FIGURE 5. Meteorologic data from the Garder-moen weather station (elevation: 202 m), which isrepresentative for inland areas of eastern Norwayand midwestern Sweden (see www.met.no). Thethick black line and the thin grey lines display,respectively, the mean and 30-yr standard deviationsfor the normal period 1961–1990. (a) Series of 365-day running mean air temperature for 1990–2009.The black arrow marks the maximum 365-day meantemperature in the series corresponding to theperiod 6 November 2006 to 6 October 2007. (b)Number of days after 1 August before the minimumtemperature drops below 0 C for 1990–2008. Theblack-filled circle marks the year 2006.
MADSLIEN ET AL.—HAIR-LOSS EPIZOOTIC IN SCANDINAVIAN MOOSE 903
skin inflammatory reactions as seen inthe majority of our skin samples. Why thisinflammatory reaction should induce hairloss without causing simultaneous pruritusis not clear. In experiments with sheep,Nelson (1963) suggested that the skininflammatory response to the sheep keds(Melophagus ovinus) resulted in reduceddermal blood supply. Hence, it is possiblethat changes in blood supply, induced bydeer ked bites, could affect the hairpapillae and thereby cause hair loss.Further research is needed.
The prevalence and extent of the hairloss in the moose population in 2006–2007is difficult to estimate due to the lack ofsurveillance data. Finding diseased ordead animals is the most direct evidencethat disease is occurring in an area orpopulation, but this technique has limitedapplication and, invariably, results in anunderestimation of the occurrence ofdisease (Wobeser, 2006). The number ofsubmitted and reported animals is, there-fore, not a good measurement of preva-lence of disease. However, during theattempt to immobilize moose in March2007, three of 15 moose (20%) observedfrom a helicopter had severe hair loss(Gunnar Gloersen, pers. comm.). Also,based on the pattern and severity of thealopecia seen in the moose and theassumption that the hair loss was progres-sive, it is plausible that a major proportionof the population experienced significant,but not clinically obvious, hair loss and,therefore, were not observed. We found alow prevalence of alopecia among moosein autumn 2007 (0.12%) and 2008(0.007%), indicating a termination of thehair loss epizootic in spring 2007. Wecannot rule out cases of deer ked-relatedhair loss prior to 2006, given the potentiallylow detection rate for the condition and thefact that moose alopecia was not of publicconcern prior to the hair-loss epizootic.
Deer keds have been established in thestudy area for 15–20 yr (Valimaki et al.,2010). It is curious that hair-loss epidem-ics have not occurred previously. Gener-
ally, parasite abundance increases withincreasing host population density (Arne-berg et al., 1998). Balashov (1996) report-ed a strong correlation between highdensity of moose populations and abun-dance of deer keds. Moose populationdensity in the study area is high and, thus,favorable for deer ked survival and repro-duction. However, high density alonecannot explain the epizootic in 2006–2007, as moose density has been high andstable in the study area for the last decade.
Balashov (1996) argues that mild anddry summers are important for the devel-opment of pupae and winged keds. On theother hand, Kadulski (1974) proposes thata long, severe winter with heavy snowfall islinked to high deer ked infestation inten-sity on cervids the following autumn andwinter, due to weakening of the host. Analternative explanation for Kadulski’s ob-servations might be that frequent snow-falls will rapidly cover the pupae andprotect them from potential predators(birds and rodents), thus creating stablestorage conditions ideal for pupal survivalduring winter (Harkonen et al., 2010).
We consider the extraordinarily highsummer and autumn temperatures in2006 to be the most important factor formaximum pupal development and surviv-al. Additionally, in 2006, the first frostnight occurred late in autumn (Fig. 5b),possibly enabling winged keds to searchfor a host during a longer window of timethan normal. Therefore, more swarmingdeer keds might have managed to find ahost, causing unusually high deer keddensities on the moose in 2006–2007.
Independent of the cause of alopecia,moose lacking large proportions of haircoat will need to increase their metabolicrate to maintain body temperature(McLaughlin and Addison, 1986). Not-withstanding metabolic and behavioraladaptations, the basic metabolic energyrequirements of a moose losing 30% ofits winter coat may double at ambienttemperatures of 220 C (McLaughlin andAddison, 1986). Hence, hypothermia or
904 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011
starvation might have been the proximatecause of the winter mortality of alopecicmoose in the study area in 2006–2007.Additionally, a transient negative effect ofblood loss cannot be excluded, even thoughhemoglobin levels from the alopecic cap-tured animals were normal and postmor-tems were not consistent with anemia. Nodecrease in moose population density orrecruitment rates were reported from thestudy area in 2007 compared to theprevious years, indicating that the outbreakdid not have substantial effects on the localmoose population (Solberg et al., 2010).There is still insufficient knowledge of theeffects of deer ked harassment and infes-tation on the health and fitness of wildlife.
ACKNOWLEDGMENTS
We thank Marthe Opland, Nina BrekkeTvedt, and Oddgeir Rissa Jacobsen at NVI forthe excellent technical assistance in the labora-tory. We are grateful to Rebecca K. Davidson,NVI, Professor Jon Teige, Norwegian School ofVeterinary Science and Preben Ottesen, andThe Norwegian Institute of Public Health forhelpful comments and Kjell Handeland, NVI,and Karin Bernodt, SVA, for performing someof the necropsies. Attila Tarpai, NVI, kindlyprepared the maps. We thank Jørn Daltorp,wildlife manager, for the excellent work withthe hair-loss questionnaire. We also thankGunnar Gloersen (Swedish Hunters Associa-tion), John Sigmund Moen (wildlife manager inRømskog), Atle Løvland (Indre Østfold Foodand Animal Health Authority), and all the otherhelpful wildlife managers and hunters forproviding important field reports and picturesof alopecic moose, submitting moose, andreporting alopecia. This work was supportedby the municipalities of Aurskog-Høland,Eidsberg, Eidskog, Elverum, Grue, Halden,Kongsvinger, Lørenskog, Marker, Nannestad,Sør-Odal, Trøgstad, Vestby, and Amot, theCounty Governor of Hedmark, the NorwegianForest Owners’ Federation, the NorwegianDirectorate for Nature Management, and theNational Health Surveillance Program forCervids (HOP) in Norway.
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Submitted for publication 23 December 2010.Accepted 9 April 2011.
906 JOURNAL OF WILDLIFE DISEASES, VOL. 47, NO. 4, OCTOBER 2011