Journal of Equine
Veterinary Science • May 2005 • Volume 25 • Number 5
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Diagnostic
criteria for degenerative suspensory ligament desmitis in peruvian paso horses
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Degenerative
suspensory ligament desmitis (DSLD) has arisen in recent years as a health issue
of concern to breeders and owners of Peruvian Paso horses. Lack of understanding
of this disease and a “gold-standard” antemortem test
has led to widespread confusion and uncertainty in the diagnosis of the disease
in these horses. Using observations and measurements from a group of horses with
histologically confirmed DSLD and from an age-matched
group of horses without evidence of DSLD, estimates of the sensitivity and
specificity of various measurements were calculated. The results of these
analyses suggested four steps for the diagnosis of DSLD when screening large
numbers of horses and as part of pre-purchase examinations. These four steps
included: palpation of the suspensory ligaments, observance of baseline
lameness, fetlock flexion tests, and sonographic
examinations of the suspensory ligament at mid-cannon and both branches. These
four steps accurately provide the information needed to make a diagnosis of
degenerative suspensory ligament desmitis in Peruvian
Pasos.
Degenerative
suspensory ligament desmitis (DSLD) as a syndrome has been largely unknown and
misunderstood. As opposed to a single suspensory desmitis injury, DSLD is
characterized by a widespread, progressive degeneration of the collagen of the
suspensory ligament and subsequent enlargement of the suspensory tissue, which
occurs throughout the entire ligament system and affects multiple limbs.1 DSLD occurs sporadically
in many breeds of horse, usually in older animals, career broodmares, in animals
that have been intensively exercised, or in those individuals that have
sustained prior suspensory injuries.2–4 In recent years, DSLD in the Peruvian Paso horse has become a
major topic of discussion among owners, breeders, veterinarians, and farriers
involved with the breed. However, there are no prevalence studies of DSLD in
Peruvians and most references to their predisposition for the disease are
anecdotal.2,3,5,6 Historically, DSLD in all
horses has been diagnosed based on the presence of enlarged, hyperextended rear fetlocks. Recently, an author published
the first paper characterizing DSLD in the Peruvian Paso horse and emphasized
the different clinical courses of DSLD in the Peruvian as compared with horses
of other breeds.1 Peruvian Pasos more
commonly develop four-limb DSLD, with no age or sex predilection, and often
develop disease without any meaningful physical activity.1 They do not consistently
exhibit fetlock enlargement and hyperextension, can exhibit a range of obscure,
nebulous signs, and DSLD in Peruvians usually results in a poor outcome.1
The difference in
clinical presentation of DSLD in the Peruvian Paso compared with all other
breeds necessitated specific and accurate diagnostic steps and criteria. Further
research is underway into the genetic and biochemical causes of DSLD in the
Peruvian, aimed at a genetic marker and/or biochemical test for this disease in
Peruvians. But an immediate need exists for a diagnostic/screening protocol that
will aid in the identification of Peruvian horses affected with DSLD, especially
in the earliest stages of disease. The purpose of this study was to identify a
minimal set of clinical signs and ultrasound measurements for DSLD in the
Peruvian Paso horse that would accurately and practically distinguish horses
with DSLD from those without it.
The horses with DSLD
in this study were identified from a larger group of Peruvian Paso horses
presented to the first author for lameness issues over a 3-year period. The
criteria used to diagnose DSLD tentatively in these horses were composed of a
combination of information: a history of chronic lameness and palpable pain
and/or enlargement of the suspensory tissues in more than one limb. Nineteen of
45 horses meeting these criteria have now been necropsied and histopathologically
confirmed with DSLD. Histopathologic confirmation
served as the gold standard to estimate the sensitivity of various
measurements.
A group of 45 purebred
Peruvian Pasos horses examined by J. L. M. without palpable pain and/or
enlargement of the suspensory tissues in more than one limb were
frequency-matched to be of roughly the same age as the affected horses and
served as the comparison group. These horses were used to estimate the
specificity of various measurements.
Each horse received a
physical exam, lameness exam, and ultrasonographic
exam of their suspensory tissues. In each case, the sex and age were noted.
Physical data were recorded for each limb as follows: presence of fetlock
enlargement and/or effusions of the fetlock joints or tendon sheath; angle of
the fetlock during weight-bearing as being either upright, level, or hyperextended; palpable pain and enlargement or thickening
of the suspensory ligament as being either none, mild, moderate, or severe;
baseline lameness using the AAEP Lameness Grading System of 0-57;and fetlock flexion tests
using the same grading system.
Ultrasonographically, the suspensory
ligament of each limb was examined just proximal to the bifurcation or in zones
2A or 3A, and both branches roughly midway along their
length or in zones 3A or 4A. Measurements were recorded as follows: the
suspensory body in cm in the palmar/plantar to dorsal
plane and both branches in area in cm2and in cm in the lateral to
medial plane, or medial to lateral plane—totaling 5 measurements per leg. Sonographic lesions were recorded as either hypoechoic or hyperechogenic areas in the suspensory ligament, and it was noted whether
there were other soft tissue lesions usually involving the flexor tendons.
Finally, whether the animal had a histopathologic
confirmation of DSLD was recorded.
Statistical
methods
Since most of the
continuous measurements were not normally distributed, the median measurements
among horses with and without DSLD were compared using the Wilcoxon rank sum test.8 For those parameters where
there was a statistically significant difference between groups, cut-offs were
selected and estimates of the sensitivity and specificity of each parameter were
determined using standard formulas.8 The cut-offs were selected
to maximize specificity (ie, minimize the probability
of false positives) since horses diagnosed with DSLD have a poor prognosis.
Sensitivity measures how well a test performs among horses with the disease of
interest (as determined by a gold standard). Specificity measures how well a
test performs among horses that do not have disease.8
Categorical
characteristics (eg, gender) were compared between the
groups using the Chi square test of independence unless the numbers in any cell
were less than 5. In these instances, the Fisher exact test was used. P
values
.05 were considered
significant.
There was a higher percentage of mares, fewer stallions, and a
somewhat higher percentage of animals over 10 years of age among the horses with
confirmed DSLD compared to control horses. However, the differences were not
statistically significantly different (Table 1). Overall, 57.9% (11/19) of
affected animals were 10 years old or less, and 94.7% (18/19) were 15 years old
or less. Among the affected horses, 5.3% (1/19) were affected in the front limbs
only, 36.8% (7/19) had only rear limbs affected, and 57.9% (11/19) had front and
rear limbs involved.
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Table 1. Characteristics of Peruvian Paso
horses with and without degenerative suspensory ligament desmitis
(DSLD)
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Horses with
DSLD |
Controls | |||
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Characteristics |
No.
(N =
19) |
% |
No.
(N =
45) |
% |
P
value |
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Gender |
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Mares |
11 |
57.9 |
21 |
46.7 |
NS |
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Stallions |
2 |
10.5 |
9 |
20.0 |
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Geldings |
6 |
31.6 |
15 |
33.3 |
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Age
(yrs) |
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3 |
15.8 |
9 |
20.0 |
NS |
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6-10 |
8 |
42.1 |
21 |
46.7 |
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11-15 |
7 |
36.8 |
10 |
22.2 |
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15 |
1 |
5.3 |
5 |
11.1 |
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Physical
examination findings
The presence or
absence of lameness in at least one limb, in 2 or more limbs, and abnormal
fetlock flexion tests were more common in horses with DSLD than unaffected
horses (Table 2). In the affected group, each
limb was painful on palpation to some degree of pain in the following
percentages: 63.2% (12/19) left front, 47.4% (9/19) right front, 89.5% (17/19)
left rear, and 89.5% (17/19) right rear limb.
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Table 2. Sensitivity (Se) and specificity
(Sp) of various physical examination findings among Peru-vian Paso horses with and without DSLD
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Se (%)
N =
19 |
Sp (%)
N =
45 |
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Lame in at
least 1 limb |
89.5 (68, 99)* |
84.4 (69,
93) |
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Lame in 2 or
more limbs |
73.7 (50,
91) |
97.8 (88,
100) |
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Abnormal
flexion test ( |
100 (83,
100) |
66.7 (52,
80) |
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*95% Confidence
limits. | ||
Fifty-three percent
(10/19) of horses in the affected group displayed palpable changes to some
degree in their left front limbs, 73.7% (14/19) in their left rear limbs, 36.8%
(7/19) in the right front limbs, and 73.7% (14/19) in their right rear limbs.
All of these percentages were statistically significantly larger than those
observed in the corresponding limbs of unaffected horses (all P <
.0001).
Lameness, while not a
specific indicator of suspensory disease, was common among affected horses. Of
the affected horses, 89.5% (17/19) were lame in at least one limb when examined.
In contrast, only 16% (7/45) were lame in the unaffected group. Each limb in
affected horses was significantly more likely to be lame than its counterpart
among unaffected horses (all P < .05). At the time of examination, each limb
of the affected horses was lame in the following percentages: 26.3% (5/19) left
front, 21.1% (4/19) right front, 68.4% (13/19) left rear, and 57.9% (11/19)
right rear limb. Similarly, the affected group displayed significantly more
multi-limb (2 or more limbs) lameness (73.7%) than the unaffected group (2%)
(P < .0001).
Fetlock flexion tests
in the affected group, while again not specific for diseased suspensory tissue, were consistently positive and had higher grading
scores compared to the unaffected group. Every affected horse (19/19) had at
least one limb with a flexion grade of 2.5 or higher, while only 33% (15/45) of
the unaffected group had at least one limb with a flexion grade of 2.5 or higher
(P < .0001). Additionally, the affected group was more likely than the
unaffected group to flex lame in multiple limbs. Eighty-nine percent (17/19) of
affected horses flexed lame (had a score of at least 1) in 3 or more limbs,
while only 20% (9/45) flexed lame in 3 or more limbs among unaffected animals (P
< .001). Overall, the probability of flexing lame (with a score of at least 1
or for a score of at least 2.5) for each limb was statistically significantly
higher among affected compared with unaffected horses (all P values.05).
Ultrasound
measurements
The median
measurements of the suspensory ligaments of each limb regardless of the location
of the measurement, and regardless of whether the measurement was only in a
linear plane or in 2 planes, were all statistically significantly larger among
affected compared with unaffected horses. All P values were <
.01.
After empirically
comparing the distribution of the ultrasonographic
measurements of the suspensory tissue in the 2 groups of horses, we selected
cut-off points that would maximize specificity. That is, we selected
conservative cut-off points or measurement limits for normal suspensory ligament
tissue in the Peruvian Paso, minimizing the likelihood of false positive results
(since the ramifications for a diagnosis of DSLD are so serious). By doing so,
we increased the likelihood of false negative results. The following cut-offs
were selected, above which horses were considered to have evidence of DSLD: (1)
for all limbs the suspensory body in zone 3A, 1.3 cm in the plantar to dorsal
plane; (2) for both suspensory branches in any limb, 0.7 cm2on area;
(3) for both suspensory branches in any limb in the linear plane of lateral to
medial or medial to lateral, 1.1 cm in length. The sensitivities and
specificities associated with these cutoffs for both rear limbs were estimated
(Table 3). Using the same cutoffs, the
estimates of sensitivity and specificity were somewhat lower for the front limbs
than for the rear limbs (data not shown). Affected horses had fewer and less
severely affected front limbs compared with hind limbs.
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Table 3. Sensitivity*
and specificity**
of rear limb ultrasound measurements for determining DSLD using noted
cutoff measurement points
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Left Rear
Limb |
Right Rear
Limb | ||
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Se
(%) |
Sp
(%) |
Se
(%) |
Sp
(%) |
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SL3A—1.3cm*** |
70.5 |
40 |
81.3 |
84.4 |
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Lat B Area—0.7
cm2 |
77.8 |
100 |
94.1 |
100 |
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Med B Area—0.7
cm2 |
77.8 |
100 |
94.1 |
100 |
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Lat B Lat to
Med—1.1 cm |
83.3 |
100 |
94.1 |
100 |
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Med B Med to
Lat—1.1 cm |
77.8 |
100 |
100 |
97.8 |
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*Sensitivity
based on measurements of 19 histopathologically
confirmed horses. | ||||
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**Specificity
based on horses with absence of pain and palpable enlargement of
suspensory ligaments in 2 or more limbs. | ||||
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***Horses with
values exceeding cutoff values were considered to have evidence of DSLD.
SL3A, Suspensory ligament body measurement zone 3A; Lat B, lateral branch
area measurement; Med B, medial branch area measurement; Lat B Lat to Med,
lateral branch linear measurement in lateral to medial plane; Med B Med to
Lat, medial branch linear measurement in medial to lateral
plane. | ||||
Finally, when data
from the total 45 affected horses (including suspected and histologically confirmed) were evaluated, the sensitivity
estimates for the ultrasound measurements did not change significantly compared
with those estimated from the histologically confirmed
horses only (data not shown).
DSLD in the Peruvian
Paso breed represents a disease that is a chronic, progressive multi-limb
syndrome that affects either sex, does not have an age predilection, and is
usually nontreatable. Consistent exam findings are
pain on isolated palpation of the suspensory ligament and palpable enlargements
and thickenings of the ligament in at least 2 limbs; lameness in at least one
limb and often multiple limbs; positive fetlock flexion tests usually in 3 or
more limbs, with at least one limb having a flexion grade of 2.5 or higher; and
enlarged suspensory ligament body and branch measurements on ultrasound exams,
again in more than one limb.
Many feel that the
incidence of DSLD has been increasing within this breed over the last 10 years.
The main stumbling blocks to a better understanding of this disease in this
breed have been the rareness of the Peruvian breed overall (many have never
heard of the breed), the lack of information about DSLD in the scientific
literature in general, and the unique way in which the Peruvian horse develops
DSLD compared with all other breeds. These issues have combined to cause many
Peruvians to go years before being diagnosed with DSLD or to be simply
undiagnosed altogether. DSLD in Peruvians, especially in the early stages, does
not present with consistent owner complaints and clinical signs. Peruvians often
are presented with complaints of upper limb and/or back pain, surly and
miserable temperaments, reluctance and/or a refusal to work, unwillingness to
stand for the farrier, and subtle gait changes that are not at first overt
lameness. Overall the Peruvian Paso breed is a healthy one and is not plagued
with a variety of the common equine lameness issues such as navicular syndrome,
osteoarthritis, OCD, and chronic laminitis. However, DSLD in the Peruvian horse
is a disease that the clinician must truly look for and have an index of
suspicion for to diagnose, especially in early onset
disease.
The results of this
paper indicate that 4 steps are useful and reasonably accurate in either the
diagnosis of, or screening for, DSLD in Peruvian Paso horses. We did not report
the results of all clinical parameters that were tested, rather only the ones
with relatively high sensitivity and specificity. The three physical exam
procedures for each limb of palpation for pain and/or enlargement and thickening
of the suspensory ligament, observance of a baseline lameness, and abnormal
fetlock flexion tests all taken together provide useful information in the
screening for DSLD, particularly when large numbers of animals are examined.
Given that (1) no unaffected horses exhibit either specific pain or palpable
changes to the suspensory ligament, (2) few nonaffected horses are lame, and (3) only 33% of nonaffected horses have a fetlock flex worse than 2.5, a
horse that (1) does not reveal any pain or palpation changes to the suspensory,
(2) does not exhibit any lameness, and (3) does not flex lame in the fetlocks or
has grades of flexion lameness of 2.5 or less would be highly unlikely to be
affected with DSLD.
However, given that
these physical exam procedures are subjective and not particularly specific for
the suspensory ligament, the fourth step of measuring
the suspensory ligament at 3 sites per leg improves a clinician's confidence in
the diagnosis. In the earlier years of sonogramming
horses for DSLD, the first author made routine exams and measurements of the
suspensory ligaments in all zones of the leg. This clearly is too time-consuming
and too expensive to be made standard practice for widespread use in the
veterinary community—hence the selection of sites of the suspensory body at
midcannon and both branches
only.
The cut-off points for
the suspensory ligament measurements were conservatively chosen to minimize the
possibility of false positives. The first author (J. L. M.) elected to err on
the side of false negatives and potentially re-examine a particular horse at a
later date rather than to falsely diagnose a horse with a disease that is known
to be incurable and often life-threatening. However, combining the information
from all 4 steps should decrease the likelihood of making false negative
determinations. In other words, an animal that palpates with pain, is lame, and
flexes lame with high grades, especially in several fetlocks (combined with
ultrasound measurements near to or at the cutoff points) suggests the presence
of disease. At the very least, if the ultrasound measurements are within normal
limits, but the horse physically has positive signs, a repeat exam in several
months' time would be a prudent suggestion. In contrast, a horse with no
positive physical exam signs for DSLD but ultrasound measurements that are at or
close to the cut-offs should not be diagnosed with DSLD based on the ultrasound
measurements alone.
The major limitation
of this study is the lack of a feasible, widely accepted, valid, “gold standard”
to definitively establish the presence or absence of DSLD in horses ante
mortem. Horses were initially separated into those with and without DSLD on
the basis of pain and enlargement of the suspensory ligaments in more than 1
limb. Then, as affected horses were euthanized or died, limbs of presumably
affected horses were examined histopathologically. All
horses with presumed DSLD were confirmed. The sensitivity estimates reported in
this paper were based on the confirmed cases. We had no confirmation of
unaffected horses because confirmation currently requires euthanasia and none of
these animals have died. Using a constellation of clinical signs to define
affected horses when no better standard is available is certainly acceptable.
The disadvantage, however, is that we were forced to compare the validity
(sensitivity and specificity) of individual signs or measurements against a
standard that was partially based on those signs. This may have led to
artificially inflated estimates of their clinical usefulness. Also, the
sensitivity and specificity estimates are based on 19 and 45 horses,
respectively. The 95% confidence limits on these estimates (particularly for
sensitivity) are relatively broad and clinicians should use them as guidelines
only. We hope this study aids in the further research that is underway to
provide a more predictive and accurate diagnostic test for DSLD such as a gene
marker test, or a biochemical test, but we believe that these recommendations
are likely to greatly improve veterinarians' ability to diagnose DSLD in
Peruvian Pasos at this time.
The work in this paper
has been born out of several years of the first author examining a large number
of DSLD cases in Peruvians (from across North America), as well as in other
breeds, in an effort to systematically refine better diagnostic criteria for
DSLD. Late- to end-stage cases, regardless of the breed, are usually not
difficult to diagnose. The need and challenge is in the detection of early- to
mid-course onset cases of DSLD in the Peruvian. Earlier detection and screening
for DSLD allows owners and breeders to make informed decisions prior to sales
and purchases, potential breeding, and future plans for young stock. While a
physical and ultrasound exam is not a guarantee for future soundness, until a
reliable gene marker test becomes available, it is the best defense available at
this time in combating DSLD within the Peruvian Paso
breed.
Acknowledgments: The
first author wishes to thank Drs Roy Pool, E. Gus Cothran, Steve Derwelis, and Alice Wolf for their long time support and
continued assistance in this project.
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8.
2.5 in at least 1 limb)