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Mare
Reproductive Loss Syndrome (MRLS)
During
April and May of 2001 the pregnant mare population of central Kentucky,
comprising multiple breeds of horses, experienced a high level of fetal
loss. They included early (40-100 day) fetal losses (EFL) plus late term
abortions and the birth of weak foals, referred to as late fetal losses
(LFL). With no immediate explanation for the cause it was identified as
Mare Reproductive Loss Syndrome (MRLS). Also reported during the month
of May were an unusually high number of cases of unilateral uveitis and
pericarditis among horses of all breeds, ages and sexes. Commencing the
last week of April and early May 2002 cases of MRLS were also reported
on a number of farms in central Kentucky albeit at a reduced level
compared to 2001.
Clinical
and Pathological Description of MRLS Veterinarians
specializing in equine reproductive practice began examining pregnant
mares over 60 days of gestation during the last week of April 2001
utilizing ultrasonography to determine the sex of the fetus. They
reported an unusually high number of fetuses were not viable, lacking a
heart beat, plus the presence of cloudy, flocculent material in the
allantoic and amniotic fluids. Subsequent examination of these cases
confirmed the fetus was no longer present. At the same time the
University of Kentucky Livestock Disease Diagnostic Center (UKLDDC),
Lexington reported a significant increase in the number of late term
abortions submitted for post mortem examination. The mare history
indicated no premonitory signs. Approximately 550 LFL were submitted
from 17 breeds of horses distributed over 32 counties in the state of
Kentucky. Pathological lesions associated with these cases included
inflammation of the umbilical cord (funitis) and amnion (amnionitis),
pneumonia, fetal bacteremia and sometimes placentitis. The findings were
suggestive of in utero fetal
illness and distress but lacked specificity to permit diagnosis of the
inciting cause. Bacterial cultures of the fetus and placenta yielded
non-beta hemolytic Streptococci spp.
and/or Actinobacillus spp. in
over 50% and approximately 20% of the cases respectively. Figures on the
number of EFL were less precise with estimates ranging from 20-30% of
the pregnant mare population of Kentucky.
Registrations to the Jockey Club of foals born in 2002 provide an
accurate figure for the Thoroughbred population in the state. As of
September 2002 the Jockey Club reported 11,697 foal registrations, a
reduction of 15% compared to the same period in 2001. Kentucky in recent
years has produced an annual foal crop that represents 30% of North
America’s yearly Thoroughbred foal population.
In
addition to the reproductive losses an increased number of newborn foals
suffering acute respiratory distress were admitted to the local equine
veterinary hospitals. These cases required intensive veterinary and
nursing care and 50% did not survive. Approximately 30 cases of
unilateral uveitis or endophthalmitis involving hemorrhage and fibrin
deposition were reported during May among horse of all breeds, ages and
sexes. These cases did not respond to treatment leading to loss of sight
in the affected eye. During the same time frame approximately 60 cases
of pericarditis were reported again among horses of all breeds, ages and
sexes. Clinical signs included fever, lethargy, anorexia and muffled
heart sounds. Ultrasound examination of the heart revealed a fibrin
layer on the epicardium and an abundant amount of fluid in the
pericardium. Approximately half of the cases were submitted for post
mortem examination at the UKLDDC where it was confirmed that the
majority of horses with pericarditis had some degree of peritoneal,
pleural and pericardial effusion. Subsequently cases of both eye and
heart conditions were included within the ‘Case Definition’ of MRLS.
Case
Definition of MRLS
During
April and May 2002 an identical clinical and pathological picture
re-emerged with cases of early and late fetal losses as well as cases of
pericarditis and uveitis consistent with what was associated with MRLS
in 2001. Numbers were significantly reduced as compared to 2001. Cases
were less widespread and no cases were reported on farm pastures where
there was a complete absence of the eastern tent caterpillar (Malacosoma
americanum).
Table
1. MRLS Losses 2001/2002
Epidemiological
Studies Undertaken to Investigate MRLS On
May 7, 2001 a questionnaire was faxed to 280 members of the Kentucky
Thoroughbred Farm Managers Club to determine the extent and impact of
MRLS, particularly EFL on farms in five counties around Lexington. From
158 responses received by May 9 it was estimated that 678 (21%) of 3294
pregnant mares had experienced EFL between 42 and approximately 80 days
gestation.
Following
this preliminary survey an in depth field epidemiological study was
organized based on a three tiered approach involving 133 farms, pastures
on those farms and selected mare populations. Twenty-three volunteers
conducted personal interviews of farm owners or managers during June
2001 using a prepared questionnaire previously forwarded to the farm.
Data entry and analyses of this extremely comprehensive survey was
performed by USDA APHIS personnel in Frankfort, Kentucky and the Centers
for Epidemiology and Animal Health, Fort Collins, Colorado. Results
indicated that a high incidence of EFL was associated with pregnant
mares exposed to high or medium levels of eastern tent caterpillars and
cherry trees, farms with a population of more than 50 mares, mares bred
in February 2001.
Later
in the year a number of case control studies were undertaken by Dr Noah
Cohen of Texas A and M University and colleagues to identify risk
factors associated with cases of pericarditis, EFL and LFL. Their
findings indicated that exposure of mares to pasture predisposed to MRLS
and also implicated the role of the eastern tent caterpillar.
A
field study of pregnant mares exposed and not exposed to MRLS in 2001
were monitored through pregnancy to birth of the foal in 2002 by regular
ultrasound examination of the fetus. The findings provided no evidence
the syndrome exerted an abnormal effect on the fetus and on placental
and foal weight at birth.
An
extensive disease surveillance program for MRLS was established in 2002
incorporating weekly weather data, the number of fetal losses submitted
to the UKLDDC, referrals of sick foals to local veterinary clinics and
reports from veterinarians undertaking reproductive examinations of
pregnant mares.
In
June 2002 a further questionnaire was sent to members of the
Thoroughbred Farm Managers Club seeking to identify farms which did and
did not experience EFL in 2002. Of 92 farms, which responded 92.3% of
mares, bred prior to April 1,2002 were still pregnant as of June 1.
Economic Impact The
Department of Equine Business at the University of Louisville was
commissioned in the summer of 2001 by the Commonwealth of Kentucky,
Office of the Governor to quantify the economic loss to the Kentucky
equine breeding industry as a result of MRLS. A
survey of 1024 breeders and breeding farm operations involving
Thoroughbreds, Standardbreds, Quarter Horses, Paint Horse, Saddlebreds
and Tennessee Walking Horses accounting for 96% of all registered foals
in the state was undertaken. A response rate of 28% was achieved. It was
estimated that 9% of the 2001 foal crop and 26% of the 2002 crop was
lost. The total economic loss over a four-year period 2000-2003 was
estimated at $336 million.
Investigations
into the Cause of MRLS in 2001 Preliminary
observations indicated that reproductive losses occurred simultaneously
over a wide area of central Kentucky on many different farms commencing
during the latter part of April. This observation was more indicative of
an environmental toxin as distinct from an infectious agent.
Investigations by several laboratories have so far failed to implicate a
primary disease pathogen. The numerous isolations of opportunistic
bacteria were considered to be secondary invaders. Initial
investigations concentrated on the role of environmental toxins
including mycotoxins, fungal endophytes, phytoestrogens and chemical
compounds including cyanide. During late April and early May 2001 there
was an unusually high emergence in central Kentucky of the eastern tent
caterpillar, crawling on fence posts, pastures and buildings and filling
water troughs and buckets. Field visits had identified the presence of
cherry trees in or around pastures containing mares that had experienced
MRLS. The majority of these trees containing ‘caterpillar tents’ had
been denuded of leaves eaten by the caterpillars. The caterpillars had
then left the trees crawling through pasture in search of a source of
nutrition.
Numerous
analyses of pasture and equine samples failed to implicate the role of
known mycotoxins, fungal endophytes, phytoestrogens and other chemical
compounds.
The
abnormal weather pattern through April 2001 in central Kentucky
comprising low rainfall, high temperatures, punctuated by severe frosts
in mid April stimulated an investigation as to the possible involvement
of weather as a trigger factor for MRLS. Examination of weather patterns
archived by the College of Agriculture’s meteorologist Tom Priddy
identified a similar pattern during April 1981. During 1980 and 1981 EFL
were reported on a number of farms in central Kentucky among mares bred
in February and March of those years.
Farm
Monitoring and Recommendations for the Prevention of MRLS in 2002. A
monitoring program published by the University of Kentucky’s College
of Agriculture for managing the risk of MRLS in 2002 was issued in the
fall of 2001. Thirteen farms were selected as ‘sentinels’ on which
pasture and mare (blood and urine) samples were obtained at intervals of
two weeks from March 1 through June 30. Detailed records of animal and
pasture histories were maintained and samples examined for a variety of
environmental toxins. Where EFL or LFL cases occurred additional samples
from the mare were obtained and the fetus if found submitted to the
UKLDDC for examination. Contingency measures to reduce the risk of MRLS
included minimizing or eliminating the exposure of pregnant mares to the
eastern tent caterpillar, keeping pregnant mares away from cherry trees,
frequent clipping of pastures on which pregnant mares grazed and
offering hay to horses at pasture. Research Projects
Several
projects were undertaken during 2002 within the College of Agriculture
as well as studies in collaboration with two local equine practices in
Lexington, Hagyard-Davidson-McGee Associates and Rood and Riddle Equine
Hospital. Finance for these projects was provided from federal funds,
the local horse industry, the Grayson Jockey Club Foundation and many
private sources.
Four
challenge studies were completed involving the exposure of pregnant
mares to the eastern tent caterpillar. The results of those studies are
summarized in Table 2. For the first time it was possible to reproduce
MRLS under experimental conditions. Information derived from field and
experimental observations provides evidence as to the source of MRLS,
involving the eastern tent caterpillar. It does not at this stage
indicate cause but does narrow the field of investigation considerably.
Additionally it does simplify the recommendations to horse owners and
farm managers to reduce the incidence of the disease by controlling the
incidence of the eastern tent caterpillar.
Table 2. Results of Experimental
Challenge Studies involving the Eastern Tent Caterpillar, April- July
2002.
Communications In addition to investigating MRLS during 2001 a significant amount of time was spent in providing factual up to date information regarding the syndrome to the equine industry and the media, locally, nationally and internationally. The interest the syndrome generated and the voracious appetite for information proved to be a challenging and at times an almost overwhelming task. Early in May 2001 an MRLS web site to address these needs was established by the Department of Veterinary Science in collaboration with the Department of Agricultural Communications at www.uky.edu/Agriculture/VetScience/gluck1.htm. This has proved to be a useful and effective means of communication and by the end of 2001 had been accessed on 33,000 occasions. The Department of Veterinary Science web site continues to be the primary source of information and by the end of March 2003 had been accessed on 48,000 occasions. The MRLS surveillance data referred in the section on epidemiological studies is updated weekly plus regular summaries of results from the monitoring program undertaken on the sentinel farms. Advice on management strategies to control MRLS including reduction of the eastern tent caterpillar population are also provided.
A
‘list server’ was established so that those who requested updates
would receive them as they were posted. Several organizations including
the Kentucky Association of Equine Practitioners, The Jockey Club and
the Kentucky Thoroughbred Owners and Breeders regularly forward the
information on their web site to members. Additionally the Bloodhorse
and the Thoroughbred Times, two weekly equine publications, regularly
post information on their websites and their journals. Overall
coordination of the flow of information is vested in an Equine Industry
Task Force comprising farm managers and owners representing several
horse breeds, practicing equine veterinarians, USDA and state
veterinarians and scientists from the University of Kentucky’s College
of Agriculture. Guidance on the operation of the monitoring program and
recommendations for control of MRLS is provided by a small ‘oversight
group’ derived from members of the Task Force.
In
August 2002, a Workshop to discuss information pertaining to MRLS was
held at the Maxwell H. Gluck Equine Research Center sponsored by the
Grayson Jockey Club Equine Research Foundation, Keeneland Association,
and the University of Kentucky Equine Research Foundation.
The Proceedings to be published in the spring of 2003 provide a
comprehensive review of current knowledge relating to MRLS.
A “Think Tank” sponsored by the Kentucky Association of
Equine Practitioners was held in January 2003 focusing on procedures to
identify the causal agent(s) of MRLS.
Scientific Collaboration This
investigation has since April 2001 involved an enormous number of
individuals at the industry, veterinary and scientific level. Each
individual in their unique way has contributed to piecing together what
has progressively become an increasingly complex puzzle. If and when the
final picture is put together that identifies and controls MRLS it will
be the result of a concerted and dedicated team effort.
Mare
Reproductive Loss Syndrome Suggested Reading List Following
is a suggested reading list of articles, papers and other publications
relevant to mare reproductive loss syndrome. The list is arranged in
chronological order, with each year’s publications additionally
arranged alphabetically by author. The
Morris Library at the Gluck Equine Research Center maintains and updates
this list, as well as retaining copies of the various publications. For
further information, to request an article be added to the list, or
receive updates of the list please contact: Gracie Hale, Morris Library,
Gluck Equine Research Center, University of Kentucky, Lexington, KY
40546. Phone: 859-257-1192 Fax: 859-257-8542, Email: ghale@uky.edu 1.
Fitzgerald, T. D. The Tent caterpillars. Ithaca: Comstock Publishing
Associates; 1995. (Cornell series in arthropod biology). 2.
Mare reproductive loss syndrome. Journal of Equine Veterinary Science.
2001; 21(5):217-218. 3.
Mare reproductive loss syndrome. Journal of Equine Veterinary Science.
2001; 21(12):587-588. 4.
Bush, L. Mare reproductive loss syndrome (MRLS). In: Southern Extension
and Research Activity Information Exchange Group-8. Tall Fescue
Toxicosis Workshop; Chapel Hill, Tenn. s.l.: s.n.; 2001:
21-23. 5.
Cohen, N.; Carey, V.; Donahue, J.; Seahorn, J.; Slovis, N., and Reimer,
J. Report of pericarditis
case-control study: prepared for the Governor's Task Force on the Mare
Reproductive Loss Syndrome. 2001. 6.
Dwyer, R. M. MRLS epidemiological study. Equine Disease Quarterly. 2001;
10(1):5-6. 7.
Gray, S. L.; Cross, D. L.; Gimenez, T.; Bridges, W. C.; McMillan, P. D.,
and Evans, P. Factors associated with mare reproductive loss syndrome in
Central Kentucky and surrounding areas. In: Southern Extension and
Research Activity Information Exchange Group-8. Tall Fescue Toxicosis
Workshop; Chapel Hill, Tenn. s.l.: s.n.; 2001: 48-49. 8.
Harrison, L. R. Kentucky equine abortion storm and related conditions.
Proceedings of the United States Animal Health Association. 2001;
(105):227-229. 9.
Kane, E. and Kilby, E. Death in the Bluegrass: an epidemic of lost
pregnancies, dead foals and sick horses strikes Central Kentucky and
beyond, challenging researchers and veterinarians to identify the cause
and staunch the unprecedented loss of equine lives. Equus. 2001;
(287):60-68. 10.
Powell, D. G. Commentary (MRLS). Equine Disease Quarterly. 2001;
10(1):1. 11.
Powell, D. G. Mare reproductive loss syndrome (MRLS). Equine Disease
Quarterly. 2001; 9(4):4-6. 12.
Thalheimer, R. and Lawrence, R. G. The Economic loss to the Kentucky
breeding industry from Mare Reproductive Loss Syndrome (MRLS) of 2001:
prepared for the Office of the Governor, Commonwealth of Kentucky. 2001. 13.
Mare reproductive loss syndrome. Journal of Equine Veterinary Science.
2002; 22(8):349-350. 14.
Mare reproductive loss syndrome returns, but losses are fewer - Evidence
further suggests that eastern tent caterpillar is culprit. Journal of
the American Veterinary Medical Association. 2002; 221(2):179-180. 15.
Asbury, A. C. MRLS Workshop. The Horse. 2002; 19(10):22. 16.
Bain, F. T. and Williams, N. M. The Mare reproductive loss syndrome (MRSL):
fetal and neonatal problems. In. Proceedings of the 2002 American
College of Veterinary Internal Medicine Veterinary Medical Forum.;
Dallas, Tex. 2002.
Available at: http://www.vin.com/Members/Proceedings 17.
Dwyer, R. M.; Garber, L.; Traub-Dargatz, J.; Meade, B., and Pavlick, M.
Dissecting an outbreak of mysterious etiology: mare reproductive loss
syndrome. In: Proceedings of the 2002 American College of Veterinary
Internal Medicine Veterinary Medical Forum.; Dallas, Tex.
2002. Available
at: http://www.vin.com/Members/Proceedings 18.
Dwyer, R. M.; Garber, L.; Traub-Dargatz, J.; Meade, B.; Pavlick, M., and
Walker, J. An epidemiological investigation of mare reproductive loss
syndrome: breaking ground on a new disease. Society for Veterinary
Epidemiology and Preventive Medicine. 2002; 44-47. 19.
Fitzgerald, T. D.; Jeffers, P. M., and Mantella, D. Depletion of host
derived cyanide in the gut of the eastern tent caterpillar, Malacosoma
americanum. Journal of Chemical Ecology. 2002; 28(2):257-268. 20.
Green, E. M. MRLS outbreak response in Florida: the ripple effects. In:
Proceedings of the 2002 American College of Veterinary Internal Medicine
Veterinary Medical Forum.; Dallas, Tex.
2002. Available at: http://www.vin.com/Members/Proceedings 21.
Kane, E. and Kilby, E. The plan pays off: 20/20 hindsight and targeted
science guide Kentucky horse breeders through a foaling season free of
ugly surprises. Equus. 2002; (299):54-61. 22.
Morehead, J. P.; Blanchard, T. L.; Thompson, J. A., and Brinsko, S. P.
Evaluation of early fetal losses on four equine farms in central
Kentucky: 73 cases (2001). Journal of the American Veterinary Medical
Association. 2002; 220(12):1828-1830. 23.
Powell, D. G. Commentary (MRLS). Equine Disease Quarterly. 2002;
10(4):1. 24.
Powell, D. G. Mare reproductive loss syndrome. Journal of Equine
Veterinary Science. 2002; 22(3):108-110. 25.
Powell, D. G. Mare reproductive loss syndrome (MRLS). In. Bluegrass
Equine Reproduction Symposium; Lexington, Ky. Lexington: Hagyard-Davidson-McGee
Associates, PLLC; 2002. 26.
Powell, D. G. An Update on mare reproductive loss syndrome (MRLS) in
Kentucky. In. Conference Proceedings Society for Theriogenology,
American College of Theriogenologists;
Colorado Springs, Colo. Nashville: Society for Theriogenology;
2002: 147-152. 27.
Priddy, T. MRLS degree days - what it means. Equine Disease Quarterly.
2002; 10(4):5-6. 28.
Reimer, J. Pericarditis outbreak: management and prognosis. In.
Proceedings of the 2002 American College of Veterinary Internal Medicine
Veterinary Medical Forum.; Dallas, Tex.
2002. Available
at: http://www.vin.com/Members/Proceedings 29.
Swerczek, T. W. Saprotrophic fungi and bacteria and commensal bacteria
that infect frost-damaged pastures may be contributing to microbial
overgrowth and lesions associated with the Mare Reproductive Loss
Syndrome. Journal of Equine Veterinary Science. 2002; 22(6):234-236. 30.
Taylor, J. R. Theory of ammonia toxicity as the mechanism of abortion in
the Mare Reproductive Loss Syndrome. Journal of Equine Veterinary
Science. 2002; 22(6):237-239. 31.
Vince, K. J.; Riddle, W. T.; LeBlanc, M. M.; Estes, R., and Stromberg,
A. J. Ultrasonographic appearance of fetal fluids between 55 and 176
days of gestation in the mare: effect of mare reproductive loss
syndrome. Proceedings of the Annual Convention of the American
Association of Equine Practitioners. 2002; (48):350-352. 32.
Williams, N. M. Mare reproductive loss syndrome: pathologic findings.
Equine Disease Quarterly. 2002; 10(4):4-5. 33.
Brown, S. E. The MRLS mystery. The Horse. 2003; 20(2):66. 34.
Cohen, N. D.; Carey, V. J.; Donahue, J. G.; Seahorn, J. L.; Donahoe, J.
K.; Williams, D. M., and Harrison, L. R. Case-control study of late-term
abortions associated with mare reproductive loss syndrome in central
Kentucky. Journal of the American Veterinary Medical Association. 2003;
222(2):199-209. 35.
Cohen, N. D.; Donahue, J. G.; Carey, V. J.; Seahorn, J. L.; Piercy, D.;
Donahoe, J. K.; Williams, D. M.; Brown, S. E., and Riddle, T. W.
Case-control study of early-term abortions (early fetal losses)
associated with mare reproductive loss syndrome in central Kentucky.
Journal of the American Veterinary Medical Association. 2003;
222(2):210-217. 36.
Dwyer, R. M.; Garber, L. P.; Traub-Dargatz, J. L.; Meade, B. J.; Powell,
D. G.; Pavlick, M. P., and Kane, A. J. A case-control study of factors
associated with excessive proportions of early fetal losses associated
with mare reproductive loss syndrome in central Kentucky during 2001.
Journal of the American Veterinary Medical Association. 2003;
222(5):613-619. 37.
Herbert, K. S. Pasture monitoring in Kentucky. The Horse. 2003;
20(2):16-17. |