PREVALENCE OF ANTIBODY TO MALIGNANT

CATARRHAL FEVER VIRUS IN WILD AND DOMESTIC

RUMINANTS BY COMPETITIVE-INHIBITION ELISA

Authors: Li, Hong, Shen, David T., Jessup, David A., Knowles, Donald
P., Gorham, John R., et al.
Source: Journal of Wildlife Diseases, 32(3) : 437-443
Published By: Wildlife Disease Association
URL: https://doi.org/10.7589/0090-3558-32.3.437

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 J( f % i1(I1i/t l)t%5,’ 33 199b 4:u7-443

PREVALENCE OF ANTIBODY TO MALIGNANT CATARRHAL FEVER

VIRUS IN WILD AND DOMESTIC RUMINANTS BY
COMPETITIVE-INHIBITION ELISA

Hong Li,1 David T. Shen,1 David A. Jessup,2 Donald P. Knowles,1 John R. Gorham,1
Tom Thorne,3 Donal O’Toole,4 and Timothy B. Crawford5
Animal Disease Research Unit, U. S. Department of Agriculture, Agricultural Research Service,
Pullman, Washington 99164, USA
2 California Department of Fish and Game, Rancho Cordova, Califomia 95670, USA
Wyoming Game and Fish Department, Veterinary Section, Laramie Laboratory,
Laramie, Wyoming 82070, USA
Wyoming State Vetennary Laboratory, University of Wyoming, Laramie, Wyoming 82070, USA
Department of Veterinary Microbiology and Pathology, Washington State University,
Pullman, Washington 99164, USA

ABSTRACT: A competitive-inhibition ELISA (CI-ELISA), based on a nuonochonal antibody to an

epitope comiserved amomig muualignamit catarrhal fever virus (MCFV) straimis of botlu wildebeest amid
sheep origimi, was used to determuiimue the prevalence of antibody to MCFV in selected doniestic
amid wild mumimiamits, both free-ramiging amid captive, fromn the USA. \Ve evaluated 2528 sera from
14 species betweemi 1990 and 1995, including 80 prongliorn antelope (Antilocapra americana),
:3:39 bighuorn slice1) (Ovi.s cana(Iensis), 103 bisoui (Bison bison), 17 black-tailed deer (Odocoileu.s
Iu(’,nzon us co/u mbzanus), 395 domestic cattle (Bo.s taurus), 291 domestic goats (Capra Ii ircu,s),
680 (lomuestic sheep (Ovis ammon), :32:3elk (Cervu.s elap/umis), 41 llamas (Lame ,glama), 21 mouflon
sheep (Ovis inusimon), 54 miuouumitaimi goats (Oreamnos amencanu.s), 101 mule (leer (Odocoileus
Iu’inzonu.s), 20 muuskox (Ovibos mosc/.atus), and 63 while-tailed (leer (Odocoileus uirgznzanus). A
high seroprevalence (37 to 62%) was observed in domestic sheep, doniestic goats, muiskox, and
some bighorn sheep popuulations. Seroprevalemice in these species was generally age-related: a
verv low seroprevalence was present imuthese animsuals under one year of age. A low seroprevalence
(2% to 1:3%) was fouumud imi clinically-susceptible species suich as (loluiestic cattle, (leer, elk and
bison, smmpportimig the concept that sigmiificamut miiuuiubers of non-lethial infections occur among clin-
ical lv smisceptil)le ruiniimiamuts.
Ket, words: M alignamut catarrhal fever, gani miiahierpesviruus, ruiminamits, wildlife, antibody prey-
alemice, competitive-miliibitiomi ELISA.

INTRODUCTION named alcelaphine herpesvimus 1 (AHV- 1)

in reference to the principal reservoir hiost,
Malignant catarrhal (‘ever (MCF) has
wildebeest (Con nOc/Ui(’t(’.S spp., subfamily
beemi known for miiany years as a tlramiiatic,
Alcelaphinae) (Roizmnan et al., 1981). A
often lethial, systemiiic viral infectiomi of cat-
relatively large numiil)er of related species-
tle and many species of wild riumninants
adapted variants of the gam maherpesvi-
(Plowrighit, 1968). Its hallmarks are wide-
ruses reside as persistemit infectiomis in
spread lymuiphoproli feration and imiflamn- members of subfamiuihies of Bovidae: Alec-
uiiatory vascular lesions (Rossiter, 1985). laphimiae, Hippotragi nae, Capminae and
Based on the reservoir mumiiinamit species Ovibovinae (Reid, 1992). For example, a
from which the causative virus arises, two distinct but closely-related group of the vi-
muiajor epizootiological entities of’ the dis- ruses, termued Alcelaphimie hierpesvi rus-2
ease have been described: wildebeest-as- (Roizmnan et al., 1981), exists in a numiul)er
sociated (\VA) and sheep-associated (SA) of species of antelope other than the wil-
MCF, between which there are no signif- debeest and have not been reported to
icant differences imi chinico-pathological cause disease in other mumiiinants under
features (Plowright, 1990). The etiologic natural conditions (Mushi et al., 1981). To
agent for \VA-MCF has beemi isolated (Plow- date, the etiologic agent for SA-MCF has
right et al., 1960), characterized as a gam- not been isolated. However, based on cir-
mnalierpesvimus (Plowright et al., 1965), and cii m stan ti al cvi de nec do iii e 5 tic sheep

437

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 438 JOURNAL OF WILDLIFE DISEASES, VOL. 32, NO. 3, JULY 1996

(Ovis ainmon) (subfamily Caprinae) may Diego, San Diego, California, USA. The viral
antigens were prepared by infection of FMSK
serve as a reservoir and transmit the virus
cell monolayers in 900 cm2 roller bottles or 150
to susceptible ruminants such as domestic
cm2 flasks at a multiplicity of infection of 0.1.
cattle (Bos taurus), (leer (Odocoiieus spp.), When 80 to 90% of the cells had cytopathic
and bison (Bison bison) (Plowright, 1990). effects, the supernatant was harvested, clarified
The demonstration of SA-MCF virus by centrifugation at 4300 X G for 30 mum, and
DNA with sequence similarity to Epstein- virus peiheted at 125,000 X C for 90 mm
thromugh a 2-cm 35% (w/w) siucrose column.
Barr virus an(l Herpesvirus sauniri in leu-
The pellets were resuspended in phosphate-
kocytes fromii normal sheep and SA-MCF- buffered saline (PBS), sonicated and the stu-
affected cattle (Baxter et al., 1993) sup- pernatant collected after clarification at 6,000
ports the idea that sheep are indeed car- X G for 5 mm, stored at -20 C. Protein con-
riers of a gamnmnahempesvinus. Based on its centration was determined by BCA proteimi as-
say (Pierce, Rockford, Illinois, USA).
antigenic and base sequence similarity to
We collected 2528 serum samples from 14
AHV-1, the putative SA-MCF agent has species in 11 states of the USA for assay of
1)een tentatively classified as ovine herpes- antibody to MCFV by CI-ELISA (Table 1). Of
virus 2 (OHV-2) (Roizman, 1992). these, 826 were from white-tailed deer (Odo-

More than 150 species in the suborder coileus virginianus), black-tailed deer (Odocoi-
leus hemionus columbianus), elk (Cervu.s c/a-
Rumiiinantia are susceptible to MCF virus
phus), pronghorn antelope (Antilocapra amer-
infection (Heuschele, 1988). Clinical dis-
icana) and bighorn sheep (Ovis canaden.sis)
ease has been described in over 30 of and were kindly provided by Drs. David Hun-
these species, including domestic and wild ter, Wildlife Health Laboratory, Idaho Depart-
ruminants, some of which are threatened ment of Fish and Game, Boise, Idaho, USA;
or endangered (Heuschele, 1988). Diag- Philip Schiadweiler, Wildlife Laboratory, Mon-
tana Department of Fish, Wildlife and Parks,
nosis and control of MCF has been hin-
Bozeman, Montana, USA, and Willianu Foreyt,
dered by a lack of reliable screening tools
Department of Veterinary Microbiology and
for epizootiological surveys and by its clin- Pathology, Washington State University, Pull-
ical similarity to several other diseases of man, Washington, USA. Samples fromu moun-
ruminants. Application of newly-devel- tain goats (Oreamnos americanus) and domes-
oped specific assays for MCFV antibody tic llamas (Lame glarna) were provided by Dr.
W Foreyt. We collected 680 sera from donies-
(Li et al., 1994) and DNA (Baxter et al.,
tic sheep (Ovis ammon) in California, Georgia,
1993) prOmilises to ovemcomiie these imped- Idaho, Kentucky, Montana, North Dakota, Ten-
innents and to answer some of the intmigu- nessee, Washington, and Wyoming (USA): 170
ing questions posed by this ill-defined of these were from eight flocks of slueep with
group of viruses that have eluded research known histories of association with cases of
clinical MCF in cattle (Bo.s taurus), white-
efforts for mnany years. Our objective was
tailed deer, or bison. Twenty-one sera were col-
to determine the prevalence of MCFV an-
lected from a group of mouflon sheep (Ovis
tibody in domestic and wild ruminants, us- musimon) associated with a case of clinical
ing the recently developed competitive-in- MCF in sika deer (Cervus nippon) in Washing-
hibition ELISA (CI-ELISA), based on a ton. The bison serum samples were collected
monoclonal antibody to an epitope specific from ranches in Montana and Washington. Do-
mestic goat (Capra hircus) sera were collected
to, and conserved among, all strains of
from a closed Saanen goat herd at Washington
MCF virus examined to date.
State University. Another 238 sera from do-
mestic cattle were selected randomly from the
MATERIALS AND METHODS
archived serum banks of Washingtomu Animal
The Miniiesota isolate of MCFV (MN- Disease Diagnostic Laboratory, Washimigton
MCFV), origimially derived a cow with from State University, having been submitted with
clinical MCF in Minnesota, (Hamdy et USA clinical diagnoses other than MCF. In addition,
al., 1978), and fetal mouuflon sheep kidney 157 serum samples were collected fromuu cattle
(FMSK) cells were kindly provided by Dr. with known history of contact with domuuestic
Werner Heuuschele, Center for Reproduction of sheep in Montana, Washington and Wyoming.
Endangered Species, Zoological Society of San Samples from muskox (Ovibo.s moschatus) were

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 LI ET AL-ANTIBODY TO MCFV IN RUMINANTS 439

TABlE I. Summary of numl)ers amid state of origin of serum samples collected from rumimuants for malignant
catarrhial fever virus seroprevalence studies between 1990 and 1995.

Number
of serum
utiunuutt tuatiut Scientific uuanue samples State of origin

Bighuorn sheep Otis canadensis 339 California, Idaho, Montana, Washing-

tomi,and Wyoming
Bison Bison bison 103 Montana and Washington
Black-tailed (leer Odocoileus lu’i,nonus colu,nbianu.s 17 California
I)oinestic cattle Box tennis 395 Montamia, Washington, amid \Vyoming
l)omestic goats Capra hzrcu.s 291 \Vashington
l)omestic sheep Otis atnmon 680 California, Georgia, Idaho, Kentucky,
Montana, New York, North Dakota,
Teminessee, Washuington, and Wyo-
ming
Elk Certus clap/ins 323 California, Idaho, Montana, Washing-
ton, and Wyonuing
Llama Llama glalna 41 \Vashingtomu
Mouiflon shueep Otis inusimon 21 Washington
NI ouumitain goats Oreamnos amt’ricanu.s 54 Idaluo and Washington
Mule (leer Odocoileus liemionus 101 California, Idaho, Montana, Washing-
ton, and Wyoming
NI uskox Ovibos inosc/zatu.s 20 Alaska
Pronghorn antelope Antilocapra americana 80 California afl(l Wyonuing
\Vhuite-tailed (leer Odocoileus virginianus 63 Idaho, Montana, Washington, and Wy-
onuing

Total 2,528

kimudly prosnilel by Dr. John Blake, University all tests. Data interpretation was similar to that
of Alaska, Fairbanks, Alaska, USA. described previously (Li et al., 1994): when the
Procedures for competitive-inhibition ELI- mean of the three replicate OD readings of a
SA (CI-ELISA) were described by Li et al. serum was more than 3 SD below the mean of
(1994). Briefly, 96-well polystyremue plates (Im- a panel of six negative control sera (from sheep
niuuhomi 4, Dvuuatechi Lab, Inc., Chantilly, \Tirgmn- or cattle) run in triplicate, the serum was con-
ia, USA) were coated at 4 C for 18 to 20 hr sidered positive for MCFV antibody. This assay
with 0.25 p.g of the Minmuesota isolate of MCFV is highly specific for MCF vmnuses, having been
antigemu/wehl in 50 p.l of 50 nuM carbonate-bi- tested in several animal species against tinnier-
carbomiate buffer (pH 9.6). After blocking with ous numinant pathogens (Li et al., 1994).
20% miomufat milk in PBS at 24 C for 2 hr and Data were analyzed by chum-square goodness-
washing with PBS with 0.1% Tween-20, 250 p.1 of-fit test (Ott, 1993). Statistical significance
of 1:10 dilution of test serum and 50 p.l of was determined as P < 0.05.
mnonoclomual antibody (0.2 p.g) were added and
incubated at 24 C for 1 lur. The wells were RESULTS
washed three timuies with PBSfFsveen-20, and
incubated with alkahimue phosphatase anti- A low percentage (0 to 9%) of seropos-
mouse imnmnuumioglobuuliui C (Sigma Chemical itivity occurred in bison, black-tailed deer,
Co., St. Louis, Missouri, USA) at 24 C for 1 hr.
white-tailed deer, mule deer, and elk (Ta-
After a fimual wash, 50 p.l of substrate buffer
comhtaimiimig 1 muug/muil p-nitrophenyl phosphate
ble 2). There were no apparent differences
(Sigmua Chemical Co.) were added, and incu- in seroprevalence between groups of the
bate(l for 60 mm; the optical density at 414 nm same species, regardless of state of origin
(01)414) was determined. All sera were run in (data not shown). A relatively high per-
triplicate. A pamuel of sera from sheep or cattle
centage, 124 (37%) of 339 bighomn sheep,
defimue(1 as muegative by an absence of MCFV
were seropositive. A significant (P <
antibody omu indirect imuuniuunofluuorescence (Li
et al., 1994) amud immiiuunoprecipitatiomi (Li et al., 0.001) difference was detected between
1995a) was inclu(Ie(I in each run as controls in desert bighomn sheep (Ovis canadensis nd-

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 440 JOURNAL OF WILDLIFE DISEASES, VOL. 32, NO. 3, JULY 1996

TABI,E 2. Prevalence of malignant catarrlual fever vi- TABLE 3. Prevalemuce of malignant catarrhal fever vi-
rius antibody in certain wild rumnimiant sera collected nus antibody in certain domestic nuininant sera col-
imu the USA between 1990 amid 1995. lected in the USA between 1990 and 1995.

Niuuuubcr positse/ Prevalence Nuumher

Species uutuiher tested (%) positive! Preva-
number leuce
Bison 2/103 2 Species tested (%)

Black-tailed deer 0/17 0

Cattle (no known contact with
Elk 30/:323 9
sheep) 10/238 4
Llama 0/41 0
Cattle (known history of contact
Mountain goats 0/54 0
withu sheep) 21/157 132
Mule deer 2/101 2
Domestic goats 177/29 1 61
White-tailed (leer 2/63 3
Domestic sheep (no known as-
Pronghorn antelope 20/80 25
sociation with cases of clinical
Bighorn sheep 124/339 372
MCF) 282/53 I 53h
Muskox 8/20 40
Domestic sheep (associated with
Mouflon sheep 13/21 62
cases of clinical MCF) 88/149 591)
Including 28 desert higluorn sheep (0% positive) and 26
A difference between cattle with n known history of as-
peuuiuusular bigluortu slueep (65% positive) from California.
sociation with sheep and cattle with a known history of
sheep contact was significant at P < 0(5)1.
h No significant difference detected hetweetu douuuestic sheep
sotii) fromn California amid other popula-
associated with caess of clinical MCF and those without
tions of bighomn sheep, which included known association (P > 0.15).

Rocky Mountain bighiomn sheep (Ovis can-

adensis canadensis) and peninsular big-
not only to domestic cattle or farmuied deer,
horn sheep (Ovis canadensis cremnoba-
but also to propagation of endangered ni-
tes): none (0%) of 28 desert bighomn sheep
minant species in the wild, in captivity, or
had antibodies, compared to 124 (40%) of
on game farms. Prevalence studies have
311 bighomn sheep in other populations
been severely constrained in the past by
(Table 2). Seroprevalence levels did not
deficiemucies in available seroassays for
appear to be related to whether the sheep
MCF viruses (Heuschele and Seal, 1992).
flocks had ever been associated with cases
Although no bona fide SA-MCFV isolate
of clinical MCF (P > 0.15) (Table 3). A
is yet available, we have identified an ep-
highu seroprevalence was present in ani-
itope conserved among all MCFV strains
muals over 1 yr of age, whereas antibody
was rarely detected in animnals less than 1
TABLE 4. Relationship between malignant catarrhal
yr of age (Table 4). The difference be-
fever virus antibody prevalence and age among cer-
tween the two age groups was statistically tain domestic and wild numinants in the USA (sera
significant (P < 0.001). A similar pattern collected between 1990 and 1995).
was observed in the muskox, although
Less than
sample numbers were smuuall. A difference
1 year old Over 1 year old’
(P < 0.001) was observed between cattle
Number Number
with a history of contact with domestic posi- Pre- posi- Pre-
sheep and cattle with no kmiown history of tive! val- tive! sal-
number ence number euuce
association with sheep (Table 3). Species tested (%) tested (%)

DISCUSSION Domestic sheep 2/77 2.5 227/250 91

Domestic goats 0/28 0 102/137 74
It is becoming apparent that MCF Bighorn Sheep 1/21 4.8 63/1 161) 54
agents represent members of a group of Muskox 0/10 0 8/10 80
related gamuimaherpesviruses that exist as Total 3/136 2 400/513 78
enzootic infections in many ruminant spe-
2 Significamut difference observed between the age groups
cies (Metzler, 1991). Viruses of this group (less than 1-yr old amid over 1-yr old) (P < 0.(X)1).
are a potentially imnportant impediment, b Not including any California desert bigluorn sheep.

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 LI ET AL-ANTIBODY TO MCFV IN RUMINANTS 441

examuuined (Li et al., 1994). This has en- from a non-lethal disease, or the infection
al)led production of an efficient CI-E LISA was entirely subclinical is unknown. Al-
for identification of animals infected with though a clear association between age
any of the known MC F viruses. and seroprevalence has been observed in
Based on thus CI-ELISA, we found ev- domestic sheep (Li et al., 1994), the dif-
idence for a wider host range for MCF ference in seroprevalence I)etween desert
vimuses than formerly suspected, including bighomn sheep (0%) and other populations
several species of wild ruminants such as of bighorns (40%) (Table 2) seems not to
muskox and some popuilttions of bighiorn be associated with the age of the animals,

sheep. There also was a large difference in since most of the desert bighiomn shueep ex-
antibody prevalence between clinically- amined were adults. The explanation for
susceptible species such as cattle and (leer this observation is not known, l)ut factors
(6%), and carrier species such as domestic such as location and management efforts
sheep and domestic goats (56%). Cattle specific to these populations need further
amid (leer with clinical MCF camu recover exploration. The difference in seropreval-
fronu the disease (Milne and Reid, 1990). ence between mnountain goats (0%) and
Our data support these othier studies that mnuskox (40%) (Table 2), both muuemnbems of
there is a significant level of non-lethal in- subfamily Caprinae, is intriguing. The rea-
fectiomi in these clinically susceptible spe- son for the difference is not apparent, but
cies (O’Toole et al., 1994). could relate to the differences in popula-
There is a degree of uncertaimity about tion density or social interactions betveen
whuethier MCF occurs naturally in free- mnembers of these two species.
ranging deer (Blake et al., 1990). The Sheep-associated MCF in cattle often

prevtlence of antibody in this study was occurs during or shortly after lambing sea-
low, in the range of 0 to 3%. The data from son (Buxton and Reid, 1980), which is sim-
this study are evidence that MCFV infec- ilar to the pattern of WA-MCF. Lambs
tiomu indeed exists among free-ranging deem might play the same role in transmission
albeit the pre’a1ence of antibody was low. as wildebeest calves (Mushui amid Rurangir-
Jessup (1985) reported a case of suspected va, 1981). The notion that sheep are in-
MCF imi a free-ranging black-tailed deer fected at early age and serve as a source
from California. Anti- MC FV antibodies of transmission, similar to wildebeest, has
were recently demuuonstrated in this animal recently been challenged because Li et al.
by CI-ELISA (H. Li, unpuibl.). Malignant (1995b) have shown that lambs are infect-
catamrhal fever is the most important in- ed not at an early age, but sometime in
fectious disease affecting game farmuu-raised later life. The present study supports the
red (leer (Cervus elaplius) in New Zealand concept that the MCFV infection in sheep
(Mackintosh, 1992). Several incidences of is age-related: similar seroprevalence pat-
MCF have occurred in cervids in North terns were observed among domestic
Amuierica in recent years resulting in sig- goats, muskox, mouflon sheep, and some
nificant miiortality (Brown and Bloss, 1992). populations of bighuomn sheep. If lambs can
These observatiomis amid the present study be ruled out as a source of transmission,
enuphuasize the mueed for caution in man- the peaks of SA-MCF occurrence during
agemnent and the advisability of avoiding lambing season muiay he due to enhanced
co-habitation betveen cervid and ovine virus shedding by ewes undergoing stress

sPecies imi zoos, on gamuue farms, and in the during the periparturient period. Whether
wild. domestic goats, muuuskox, and some popu-
Small miumuubers of free-ranging deer, elk, lations of bighomn sheep are capable of
and bison were seropositive; these animals serving as sources of virus transmission to
were once infected by MCF viruses. clinically susceptible species in nature has
\Vhether these animuuals had recovered not been determined. The amplification of

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 442 JOURNAL OF WILDLIFE DISEASES, VOL. 32, NO. 3, JULY 1996

a DNA fragment from peripheral blood catarrhal fever in captive cervidae: A case report
and a brief review of the present data on the
lymphocytes of domestic goats using OHV-
aetiopathogenesis. Medecin-Veterinarire-du-
2-specific polyrnerase chain reaction prim-
Quebec 22: 180-183.
ers (Wiyono et al., 1994) provided evi- BLAKE, J. E., N. 0. NIELSEN, AND W P. HEUSCHELE.
dence that domestic goats and sheep are 1990. Lymphoprohiferation in captive wild ru-
infected with the same or very closely-re- minants affected with malignant catarrhal fever:
lated viruses. Moreover, several recent 25 cases (1977-1985). Journal of the American
Veterinary Medical Association 196: 1141-1143.
MCF cases of captive deer have been only
BROWN, C. C., AND L. L. BLoss. 1992. An epizootic
associated with mouflon sheep (Bienvenu of malignant catarrhal fever in a large captive
and Helie, 1992). herd of white-tailed deer (Odocoileus virgini-
Based on this study as well as others anus). Journal of Wildlife Diseases 28: 301-305.

(Rossiter, 1981), a high prevalence of an- BUXTON, D., AND H. W. REID. 1980. Transmission
of malignant catarrhal fever to rabbits. The Vet-
tibody to MCFV exists in domestic sheep,
erinary Record 106: 243-245.
mouflon sheep, domestic goats, and cer-
HAMDY, F. M., A. H. DARDmRI, C. MEBUS, H. E.
tain subpopulations of bighorn sheep. Al- PIERSON, AND D. JOHNSON. 1978. Aetiology of
though domestic sheep, for example, are malignant catarrhal fever outbreak in Miuunesota.
virtually all infected, transmission of the Proceedings of the Annual Meeting of the Unit-
ed States Animal Health Association 82: 248-
virus is not a predictable event. On some
267.
ranches, cattle are pastured with sheep for
HEUSCHELE, W. P. 1988. Malignant catarrhial fever:
many years without occurrence of MCF, A review of a serious disease hazard for exotic
whereas on other farms the disease prob- and domestic ruminants. Zoologische Gartemu 58:
lems are relatively frequent when cattle 123-133.

and sheep are housed in contact. This is AND B. S. SEAL. 1992. Malignant catarrhal
fever. In Veterinary diagnostic virology: A prac-
evidence for multifactorial influences on
titioner’s guide, A. E. Castro and W. P. Ileuschiele
disease expression.
(eds.), Mosby-Year Book, Inc. St. Louis, Missouu-
Based on our data, MCFV is more prev- ri, pp. 108-112.
alent among captive and wild ruminants in JESSUP, D. A. 1985. Malignant catarrhal fever in a

North America than previously thought. free-ranging black-tailed deer (Odocoileus hem-

The results support the need for more re- ionus colunubzanus) in California. Journal of
Wildlife Diseases 21: 167-169.
search in this area, and the necessity of
Lm, H., D. T SHEN, D. P. KNOWLES, J. H. GORHAM,
care in management to avoid mixing spe-
AND T. B. CRAWFORD. 1994. Competitive-inhi-
cies susceptible to clinical MCF with spe- bition enzyme-linked immumuosorbent assay for
cies that may be MCFV carriers. antibody in sheep and other ruminants to a con-
served epitope of malignant catarrhal fever virus.
ACKNOWLEDGEMENTS Journal of Clinical Microbiology 32: 1674-1679.
W. C. DA\’ms, D. P. KNOWLES, J. H.
We thank Dongyue Zhuang, Soohnee Kwon,
CORHAM, AND T B. CRAWFORD. 1995a. Iden-
and Lori Fuller for technical assistance, Dr. Su-
tification and characterization of the major pro-
san Tornquist for assistance in statistical anal-
teins of malignant catarrhal fever virus. Journal
ysis, Karen Jones and the staff of the Wildlife
of Ceneral Virology 76: 123-129.
Investigations Lab for sample collection. The
D. O’TooLE, D. P. KNO\VLES, J. H.
authors also acknowledge Dr. William Foreyt
CORHAM, AND T. B. CRAWFORD. 19951). Inves-
for discussions and suggestions and Dr. Walter
tigation of sheep-associated malmgnamut catarrhual
Boyce, Department of Pathology, Microbiology
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