Keywords
dogs - medial shoulder instability - poodle
Introduction
Approximately a third of all canine forelimb joint lameness cases occur due to shoulder
pathology, with 17.7% of those being caused by instability[1] and 64 to 80% of shoulder instabilities occurring medially.[2]
[3]
[4] Medial shoulder instability (MSI) is characterized by medial glenohumeral ligament
(MGHL) pathology, including tears, laxity or avulsion, as seen in the majority of
cases,[5] subscapularis tendinopathy, and labral or capsular tears. Cases of MSI can be classified
as either traumatic or spontaneous in etiology, with 49% reported in one study as
a traumatic tearing of the MGHL.[6] A grading system has been described for the severity of MSI, classifying cases into
grade 1 to 4, which correlate to mild, moderate, severe, and luxated, respectively,[7]
[8] see [Appendix A]. The accepted “normal abduction angle” has been shown to be approximately 30 degrees[9] and, although past studies suggested that abduction angles could be used to diagnose
MSI, it has since been shown that significant variation occurs between observers measuring
abduction angles, that abduction angles do not closely correlate to arthroscopic pathology,
and that abduction angles of up to 75 degrees may be observed in normal joints.[10]
[11]
[12]
[13] Hence a diagnosis of MSI cannot be based upon abduction angle measurement alone.
In cases of instability/subluxation (MSI grade 1–3), arthroscopy is required to confirm
the diagnosis; luxation (MSI grade 4) can be diagnosed from radiographs.
Study populations to date have consisted predominantly of large and medium breed dogs,
often performance dogs, with poodles and their crossbreeds appearing to be consistently
overrepresented in the few small-breed subjects included.[6]
[9]
[14]
[15]
[16] Based on a literature search (PubMed, search criteria: “medial shoulder instability,
medial glenohumeral ligament, abduction angle, subluxation, and poodle”), few data
points were identified that characterized the etiology of MSI in dogs with respect
to breed.
Current described treatment options include both nonsurgical and surgical management
(see [Table 1]).[6]
[7]
[14]
[15]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24] Surgery aims to reconstruct medial stability via tendon augmentation or prosthesis
implantation. There are variations in MGHL reconstruction techniques and implants,
with the consistent aim to reconstruct the medial support for the glenohumeral joint,[14]
[15]
[19]
[20]
[21]
[22]
[25] maintaining joint alignment and normal biomechanics. Biceps and supraspinatus tendon
transpositions have independently been shown to provide improved medial stability.[6]
[26] However, biceps tendon transposition (BTT) has been shown to result in increased
external rotation of the joint and an increased abduction angle in comparison to placing
a MGHL prosthesis, and both tendon transpositions have, in time, been shown to cause
such altered shoulder biomechanics and congruity that degenerative changes will develop.[22]
[23]
Table 1
Nonsurgical and surgical treatment options for medial shoulder instability
Treatment category
|
Options
|
Nonsurgical
|
• Rest
• Nonsteroidal anti-inflammatory drugs
• External coaptation
• Physiotherapy
• Intra-articular treatments:
−Platelet-rich plasma (PRP)
−Hyaluronic acid
−Corticosteroids
|
Surgical stabilization of medial instability
|
• Radiofrequency-induced thermal capsulorrhaphy (RITC)
• Subscapularis imbrication
• Prosthetic reconstruction of medial glenohumeral ligament
−Open/arthroscopically guided techniques
−Implant choice with bone screws/bone anchors/bone tunnels, e.g., Arthrex SutureTak
anchor with FiberWire suture[a], Arthrex Mini Tightrope[b] via bone tunnels
• Biceps tendon transposition (BTT)
• Supraspinatus tendon transposition
|
Surgical salvage
|
• Shoulder arthrodesis
• Excisional arthroplasty of glenoid or humeral head
• Forequarter amputation
|
a FiberWire suture, Arthrex Inc., Naples, FL.
b ACL Tightrope System, Arthrex Inc., Naples, FL.
In our experience, poodles and their crossbreeds appear to be at elevated risk of
MSI, with a high proportion of cases presenting spontaneously (without having sustained
significant trauma) and having an unpredictable outcome in response to treatment.
This led us to undertake this study.
We hypothesize that poodles may be overrepresented in the local investigated population
of dogs presenting with MSI. Additionally, we hypothesize that poodles exhibit higher
rates of spontaneous MSI than non-poodle breeds. Finally, we wanted to investigate
whether poodles may end up with a generally poorer treatment outcome, either through
conservative or surgical management, as compared with non-poodle breed dogs.
Materials and Methods
Data Collection
Data were obtained retrospectively from the clinical records spanning 2009 to 2019
from five referral small animal veterinary hospitals in Melbourne, Australia. Records
were searched for all dogs presenting with lameness attributable to MSI, with database
searches performed using the following search terms: canine, medial shoulder instability,
medial glenohumeral ligament, abduction angle, subluxation, and luxation, in RxWorks,
EzyVet, and CiderHouse software programs. For each dog, data were collected regarding
the signalment, affected limb, abduction angle if noted, the level of inciting trauma,
the initial treatment, arthroscopic and surgical findings, postoperative outcome,
and follow-up treatments. The grade of MSI was recorded for each case; cases that
had not been graded were retrospectively assigned according to the previously described
grading system.[7]
[8]
Breeds were classified as poodle (P) and non-poodle (NP). Where the dog was recorded
as a poodle-cross or mixed breed it was allocated to the NP group. For the means of
analysis of injury data, bilaterally affected animals were included only as one case,
with their first diagnosis of MSI as their indexed event, and their subsequent presentation
was excluded. Classification of the etiology of the instability was recorded as either
spontaneous (dogs with no known trauma or whose lameness occurred during normal physiological
activity, such as jumping off one step or a couch, or pawing at the carpet) or traumatic
(dogs known to have sustained a low impact trauma such as having been chasing a ball
or at agility training when the lameness occurred). Cases with medial shoulder luxation
after sustaining high impact trauma such as being hit by a car or falling from a height
were deemed to have traumatic shoulder luxation rather than shoulder instability and
hence excluded. Other exclusion criteria included glenohumeral dysplasia and comorbidities
that may contribute to glenohumeral instability such as immune-mediated polyarthritis.
Cases were included if forelimb lameness was present, a diagnosis of MSI was confirmed
via shoulder arthroscopy visualizing pathology in the MGHL and/or subscapularis tendon,
or via radiographic confirmation of medial luxation of the humeral head without having
sustained high impact trauma, consistent with grade 4 MSI.
Treatment was classified as either conservative, reconstructive surgical (included
MGHL reconstruction or BTT), or treatment with a salvage procedure (excisional arthroplasty,
glenohumeral arthrodesis, or forequarter amputation). Given the multi-center cohort
study, conservative management was considered as a combination of rest, nonsteroidal
anti-inflammatory drugs, intra-articular steroid/stem cell/platelet-rich plasma treatments,
physical therapy, use of hobbles, orthopaedic braces, splints, or slings.
The conclusion for each case was recorded as full (restoration to/maintenance of full
intended level and duration of activities and performance from preinjury or pre-disease
status, without medication), acceptable (restoration to/maintenance of intended activities
and performance from preinjury or pre-disease status that is limited in level or duration
and/or requires medication to achieve), or unacceptable (all other outcomes), as described
by Cook et al,[27] according to examination by the primary clinician and/or assessment by the owner.
Any dog where conservative management resulted in an unacceptable outcome that went
on to have surgical treatment was allocated to the surgical treatment category. For
dogs with incomplete postoperative follow-up documentation, owners were contacted
by telephone/email to obtain postoperative outcome information. All data were retrospectively
collected and no attempt made to assess individual limb function beyond interpreting
clinical records and owner reports.
Statistical Analysis
Breeds were grouped as poodles (P) and non-poodles (NP) for analysis.
The age and sex distribution between the injured P and NP groups were compared using
independent samples t-test with unequal variance and χ2 test, respectively.
Breed Prevalence
To evaluate breed prevalence, a control population was generated by searching the
records of a general practice group of veterinary clinics in the same geographical
area to determine the breeds of dogs registered. A one sample proportion test was
used to test the null hypothesis that the MSI group breed prevalence was consistent
with the control population breed prevalence.
Relationship between grade of MSI and breed was explored via univariate linear regression,
with grade as outcome and breed as the independent variable.
Cause
A logistic regression was used to estimate the relative odds of a spontaneous cause
of the MSI according to breed type.
Outcome
Case numbers were too few to allow analysis of outcome according to breed or treatment.
Descriptive statistics are provided.
A 95% confidence interval (CI) is reported for each estimate of the relative odds,
along with a p-value for a test of the null hypothesis that the relative odds are one.
All analysis was undertaken in Stata V16 (StataCorp. 2019. Stata Statistical Software:
Release 16. College Station, TX: StataCorp LLC).
Results
Seventy-four dogs were identified with MSI, including 12 bilaterally affected (3P,
9NP). Of these, 13 were excluded: 6 due to evidence of high impact trauma (1P, 5NP),
4 due to glenohumeral dysplasia (1P, 3NP), and 3 due to potentially contributing comorbidities
(3NP), leaving 61 dogs with presumed MSI, diagnosed in clinical records by a combination
of abduction angle assessment, radiographs, and arthroscopic assessment. Given the
limitation of diagnosis of grade 1–3 MSI based on palpation and radiographic assessment
alone,[10]
[11]
[12]
[13] inclusion criteria required confirmation via arthroscopic examination for all grade
1–3 cases (n = 11; 2P, 9NP) and/or radiographic evidence of medial luxation of the humeral head
for grade 4 MSI (n = 37; arthroscopic diagnosis in 18 = 7P, 11NP; radiographic diagnosis in 19 = 8P,
11NP). Lack of confirmation of diagnosis by these methods excluded a further 13 dogs.
The 48 dogs that met the criteria for study inclusion were divided according to breed,
P (n = 17) and NP (n = 31, see [Table 2]). An independent samples t-test and χ2 test revealed no statistically significant difference in mean age or sex respectively
between the two resulting groups (estimated mean age difference (P – NP) = 0.70 years,
95% CI = -1.96–3.35, p = 0.60; Pearson, χi2 = 1.95, p = 0.58).
Table 2
Breed distribution of MSI cases
Group
|
Total number of dogs
|
Breeds included
|
Poodle
“P”
|
17
|
Poodle (miniature/toy; n = 17)
|
Non-poodle
“NP”
|
31
|
Australian Shepherd (1)
Border Collie (3)
Boxer (1)
Cavalier King Charles Spaniel (1)
Chihuahua (1)
Fox Terrier (1)
Greyhound (1)
Jack-Russell Terrier-cross (1)
Japanese Spitz (2)
Kelpie (1)
Maltese-cross (1)
Pomeranian (1)
Poodle-cross (Cavalier King Charles Spaniel, Cocker Spaniel, Labrador, Maltese Terrier,
unknown; n = 11)
Rottweiler (1)
Shih-tzu-cross (1)
Staffordshire Bull Terrier (1)
West Highland White Terrier (1)
Whippet (1)
|
Abbreviation: MSI, medial shoulder instability.
Breed Prevalence
In the control population, 82,956 dogs were identified, within which there were 2,267P,
representing a control population prevalence of 2.73% P (95% CI: 2.62–2.85%). Poodles
represented 35.4% (95% CI: 21.9–48.9%) of the MSI population (see [Fig. 1]). Utilizing a one sample test that the true proportion was that of the control population,
we found that P were 12.9 times overrepresented in the MSI population, p-value less than 0.0001.
Fig. 1 Graph showing percentage of poodles and non-poodles in the control group and MSI
cohort. MSI, medial shoulder instability.
There were 4 dogs with grade 2 MSI (1P, 3NP), 7 with grade 3 (1P, 6NP), and 37 with
grade 4 (15P, 22NP), see [Fig. 2]. Linear regression showed that although P were more likely to present with higher
grade MSI than NP, the difference was not significant (p = 0.26).
Fig. 2 Graph showing MSI grade distribution within each breed population. MSI, medial shoulder
instability.
Cause
For 30 of the 48 dogs (62.5%), the MSI was spontaneous. This included 14 of 17P, and
16 of 31NP (see [Fig. 3]).
Fig. 3 Graph showing percentage of each breed group presenting with traumatic and spontaneous
MSI. MSI, medial shoulder instability.
Poodles were more likely to suffer spontaneous than traumatic MSI, with 82.4% of P
(95% CI: 56.6–96.2%) suffering spontaneous MSI.
A logistic regression was used to estimate the relative odds of spontaneous MSI.
For P, the odds of MSI occurring spontaneously were four times greater than NP (p = 0.04, odds ratio: 4.38, 95% CI: 1.04–18.32).
Outcome
Cases that did not represent for assessment and for whom no response was obtained
through telephone/email communication were deemed lost to follow-up (n = 11; 5P, 6NP).
Overall, outcome information was available for 37 dogs (see [Table 3]): 17 dogs had return to full function (4P, 13NP; 45.9%), 13 acceptable (6P, 7NP;
35.1%), and 6 unacceptable (2P, 4NP; 16.2%). One animal was euthanised due to unrelated
comorbidities (1NP; 2.7%).
Table 3
Outcome by treatment type and breed for all cases of MSI
Treatment type
|
Breed population
|
Cases with follow-up,
n
|
Full function,
n
(%)
|
Acceptable function,
n
(%)
|
Unacceptable function,
n
(%)
|
Overall
|
Poodles
|
12
|
4 (33.3)
|
6 (50.0)
|
2 (16.7)
|
Non-poodle
|
24
|
13 (54.2)
|
7 (29.2)
|
4 (16.7)
|
Conservative
|
Overall
|
17
|
8 (47.0)
|
9 (52.9)
|
0 (0)
|
Poodles
|
5
|
1 (20.0)
|
4 (80.0)
|
0 (0)
|
Non-poodle
|
12
|
7 (58.3)
|
5 (41.7)
|
0 (0)
|
Surgical
|
Overall
|
17
|
9 (52.9)
|
4 (23.5)
|
4 (23.5)
|
Poodles
|
7
|
3 (42.8)
|
2 (28.5)
|
2 (28.5)
|
Non-poodle
|
10
|
6 (60.0)
|
2 (20.0)
|
2 (20.0)
|
MGHL reconstruction overall
|
11
|
4 (36.4)
|
3 (27.3)
|
4 (36.4)
|
Poodles
|
4
|
0 (0)
|
2 (50.0)
|
2 (50.0)
|
Non-poodle
|
7
|
4 (57.1)
|
1 (14.3)
|
2 (28.6)
|
BTT overall
|
6
|
5 (83.3)
|
1 (16.7)
|
0 (0)
|
Poodles
|
3
|
3 (100.0)
|
0 (0)
|
0 (0)
|
Non-poodle
|
3
|
2 (66.6)
|
1 (33.3)
|
0 (0)
|
Abbreviations: BTT, biceps tendon transposition; MGHL, medial glenohumeral ligament.
Return to full, acceptable, and unacceptable function for P was seen in 4 (33.3%),
6 (50.0%), and 2 (16.7%) respectively, and for NP was seen in 13 (54.2%), 7 (29.2%),
and 4 (16.7%), respectively (see [Fig. 4]).
Fig. 4 Graph showing overall outcome percentages for poodles and non-poodles.
Conservative management was selected for 25 dogs (9P, 16NP), while MGHL reconstruction
was performed in 14 dogs (5P, 9NP), BTT in 7 dogs (3P, 4NP), and salvage procedures
as first choice surgery in 2 dogs (2NP).
Conservative management resulted in full function in 8 cases (47.0%; 1P, 7NP) and
acceptable function in 9 (52.9%; 4P, 5NP).
Surgical management had the following outcomes:
MGHL reconstruction achieved full function in 4 cases (36.4%; 4NP), acceptable in
3 (27.3%; 2P, 1NP), and unacceptable in 4 (36.4%, 2P, 2NP).
BTT achieved full function in 5 cases (83.3%, 3P, 2NP) and acceptable in 1 (16.7%,
1NP).
Overall, surgical stabilization (MGHL or BTT) resulted in full function in 9 cases
(52.9%; 3P, 6NP), acceptable in 4 (23.5%; 2P, 2NP), and unacceptable in 4 (23.5%;
2P, 2NP).
Within the 31 NP dogs there were 11 poodle crossbreeds, of which 9 presented with
spontaneous MSI, showing a similar trend of overrepresentation and high incidence
of spontaneous MSI to that seen with poodles (see [Table 4]).
Table 4
Summary of MSI case numbers by breed (showing poodle crossbreeds separated out from
non-poodles), cause, grade, treatment, and outcome
Breed group
|
Number of cases
|
Cause
|
MSI grade
|
Treatment
|
Outcome
|
Control group
|
Cases included
|
Cases confirmed
|
Traumatic
|
Spontaneous
|
1
|
2
|
3
|
4
|
Conservative
|
MGHL
|
BTT
|
Salvage
|
Full
|
Acceptable
|
Unacceptable
|
Lost
|
Other
|
Poodles
|
2,267
|
20
|
17
|
3
|
14
|
0
|
1
|
1
|
15
|
9
|
5
|
3
|
0
|
4
|
6
|
2
|
5
|
0
|
% of total
|
2.73
|
|
35.42
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
Poodle crossbreeds
|
5,827
|
14
|
11
|
2
|
9
|
0
|
0
|
3
|
8
|
4
|
4
|
1
|
2
|
3
|
3
|
3
|
2
|
0
|
% of total
|
7.02
|
|
22.91
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
Non-poodles
|
74,862
|
27
|
20
|
13
|
7
|
0
|
3
|
3
|
14
|
12
|
5
|
3
|
0
|
10
|
4
|
1
|
4
|
1
|
% of total
|
90.25
|
|
41.67
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
|
Totals
|
82,956
|
61
|
48
|
18
|
30
|
0
|
4
|
7
|
37
|
25
|
14
|
7
|
2
|
17
|
13
|
6
|
11
|
1
|
Abbreviations: BTT, biceps tendon transposition; MGHL, medial glenohumeral ligament;
MSI, medial shoulder instability.
Discussion
Our data show that poodles presenting with MSI are overrepresented in the local population
of dogs, and that they are over four times as likely to present with spontaneous MSI
than other breeds. Why poodle breeds are overrepresented is unknown. When considering
joint instability, two variables need to be considered: soft tissue laxity and joint
anatomy. These factors have the potential to cause instability independently, though
the possibility of an interplay between the two exists, as seen with other polygenic,
multifactorial traits in dogs such as hip dysplasia[28] and patellar luxation.[29] The absence of glenoid dysplasia shows that this is not the cause of MSI in our
population, and hence, without note of other orthopaedic anatomical variations, suggests
that an increase in soft tissue laxity is the likely explanation for the joint instability
affecting these dogs. Whether or not this is due to an underlying hypermobility syndrome
warrants further investigation.
While a higher percentage of P presented with grade 4 MSI than NP, there was not a
statistically significant difference in the grades by breed. This may be a statistical
power problem, with too few P cases to be compared with the NP or may reflect a true
lack of difference. More testing would need to be performed to investigate this.
Our results showed that 82.4% of P affected by MSI within our local dog population
occurred spontaneously, while 51.6% of NP MSI occurred spontaneously (48.4% traumatic).
The latter rate of incidence is consistent with previous findings of 49% of MSI cases
being reported as a traumatic tearing for the MGHL,[6] likely reflecting the breed populations within previous studies and reinforcing
the notion that poodles are different to other breeds.
The high number of poodle crossbreeds within the NP group, of which the vast majority
presented with spontaneous MSI, suggests that poodle crossbreeds, often bred to be
at least 50% poodle genome,[30] are similarly at risk as poodles. Further studies into this are warranted.
Our data suggests that P are associated with a higher risk of a poorer outcome following
management of MSI. Outcome following management of MSI would benefit from further
investigation with prospective studies evaluating standardized approaches.
There are shortcomings of this study, such as the retrospective nature inheriting
a selection bias and the high number of cases lost to follow-up. The study was also
limited by the relatively small dataset, enhanced by the fact that many clinicians
were willing to diagnose MSI based on palpation and radiographs alone which led to
exclusion of 13 potential grade 1–3 MSI cases. Larger studies are warranted.
Conclusion
Our data show that poodles were overrepresented in the local population of dogs presenting
with MSI in general as well as with spontaneously occurring MSI. This has significant
clinical relevance, placing MSI higher up on the differential list for poodles presenting
with forelimb lameness, irrespective of whether they have sustained trauma or not.