Synovial effusion is an augmentation of the volume of synovial fluid within a joint as a result of synovitis. Synovial effusion of the DIP joint is commonly seen in horses with osteoarthritis,1 subchondral cysts,2,3 and septic arthritis4,5 but may also arise following trauma and collateral desmopathy.6
Although osteoarthritis is most frequently diagnosed in the distal region of limbs of lame horses,7 osteoarthritis of the DIP joint has received little attention in the veterinary literature.1,8,9 Osteoarthritis of the DIP joint causes few radiographic changes in the early stages of the disease.10 Synovitis, one of the first clinical signs of early osteoarthritis in a joint, may be a cause of pain in DIP joints. However, a DIP joint may have synovitis without signs of pain. There is some evidence that effusion of the DIP joint detected radiographically is linked to systemic markers of osteoarthritis.11 Septic arthritis causes substantial joint effusion and may arise in a DIP joint following trauma or intra-articular injection.5,12 This may be associated with periarticular edema that makes it difficult to assess joint effusion with palpation.
The dorsal recess of the DIP joint attaches to the extensor process of the distal phalanx, remains palmar to the common digital extensor tendon, and extends proximally to the coronary band approximately two-thirds of the dorsal aspect of the middle phalanx. The palmaroproximal recess is Y-shaped with 2 distinct recesses that have a complex relationship and curve proximoabaxially around the branches of the collateral sesamoidean ligaments.13,14 A fluctuant swelling palpated proximal and dorsal to the coronary band is interpreted clinically as effusion within the dorsal recess of the DIP joint. However, sensitivity and reliability of this important clinical finding remain unknown. Radiography is unreliable for detecting and grading DIP joint effusion.15 The ultrasonographic appearance of the dorsal aspect of the DIP joint has been described,16 and little or no fluid is present in the dorsal recess in clinically normal horses. However, measurements of the dorsal recess were not provided.
Ultrasonographic examination has better sensitivity than does palpation for detection of effusion in humans. There is good sensitivity for detection of an increased volume of effusion of 4 to 7 mL in a knee17–19 and 2 mL in an ankle.20
The objectives for the study reported here were to ultrasonographically quantify effusion of a DIP joint, assess the sensitivity of palpation for the detection of DIP joint effusion, and determine the threshold for ultrasonographic detection of effusion in a DIP joint.
Materials and Methods
Sample—Ex vivo preliminary experiments were performed, which were followed by in vivo experiments. For the ex vivo study, 8 fresh forelimbs were obtained from adult horses euthanized for reasons unrelated to the present study. None of the horses had a history of or were suspected of having pathological conditions in the forelimb joints. For the in vivo experiments, 5 Standardbred mares (3 to 8 years old) were enrolled. Horses were not lame, had no soft tissue swelling on the dorsal aspect of the DIP joint, and had no radiographic evidence of osteoarthritis of the DIP joints. The experimental protocol was approved by an institutional animal care and use committee of the Faculté de médecine vétérinaire at the Université de Montréal.
Ex vivo experiments
Two forelimbs were used to determine the maximal volume of fluid that could be injected into a DIP joint without rupturing the articular capsule. Saline (0.9% NaCl) solution mixed with 50% iopamidola (a nonionic iodinated contrast medium) was injected into the dorsal recess of the DIP joint. An 18-gauge, 25-mm needle and 20-mL syringe were used for the injections. The needle was inserted perpendicular to the skin at a point 1.5 cm proximal to the dorsal edge of the coronary band. The solution was injected to distend the joint until strong resistance was felt. Integrity of the joint was assessed with CT.b
The remaining 6 forelimbs were used to identify the synovial recesses that could be easily examined with a linear ultrasonographic transducer and develop a technique for ultrasonographic-guided intra-articular catheter placement. A catheter was used to facilitate repetitive injections of saline solution without the need for repetitive needle insertions and damage to the joint capsule. Each limb was prepared in a standard manner to provide adequate acoustic transmission; the hair was clipped from the region 6 cm proximal to the coronary band, and the skin was washed. Ultrasonographic examination of the DIP joint was performed with a 7.5-MHz linear-array transducer.c
A 22-gauge, 25-mm catheterd was inserted at a point 3 to 4 cm proximal to the coronary band in the dorsosagittal aspect of the DIP joint through the common digital extensor tendon (Figure 1). Correct catheter placement was verified by ultrasonography. Longitudinal sagittal images of the dorsal recess of the DIP joint were obtained immediately lateral and medial to the catheter. Images of the palmar recess were also acquired in longitudinal and transverse planes.
Sagittal anatomic section of a specimen injected with red latex in the proximal interphalangeal and DIP joints and blue latex in the navicular bursa (A) and a sagittal reformatted CT image of a specimen following injection of 10 mL of saline (0.9% NaCl) solution into the DIP joint (B). In panel A, notice the path for insertion of a catheter (dashed line) and the angle of the ultrasonographic transducer (white rectangle).
Citation: American Journal of Veterinary Research 75, 1; 10.2460/ajvr.75.1.34
The catheter then was connected to an extension set and 3-way stopcock. A 10-mL syringe was filled with heparinized saline solution, and all ports of the 3-way stopcock were flushed to prevent the introduction of air bubbles into the joint space. The DIP joint was distended with sequential injections up to 10 mL. Capsule integrity was confirmed ultrasonographically by an absence of leakage (leakage was identified as anechoic fluid in the periarticular tissues).
In vivo study
All procedures were performed on weight-bearing forelimbs of standing horses. The dorsal aspect of the proximal phalanx was prepared by use of a standardized method to provide adequate acoustic transmission for ultrasonographic examination; preparation included clipping the hair and washing the skin. Anesthetic creame was topically applied to the skin over the dorsal aspect of the proximal phalanx, and 30 minutes was allowed to elapse before further manipulations. All horses were sedated by IV administration of xylazine hydrochloridef (0.3 mg/kg) and butorphanol tartrateg (0.01 mg/kg) and placed in stocks.
Palmar nerve blocks were performed by injecting bupivacaineh at the base of the proximal sesamoid bones to desensitize the foot and facilitate manipulations. The catheter site then was aseptically prepared with 4% chlorhexidine solution and alcohol. An intra-articular catheterd (22-gauge, 25-mm) was inserted sagittally into the dorsal recess of the DIP joint under ultrasonographic guidance by use of the technique developed in the preliminary experiments. To simulate progressive synovial effusion, the joint was sequentially distended with 1, 4, and 10 mL of 2% lidocainei injected via the intra-articular catheter.
The final experiment included 4 serial injections (0, 1, 4, and 10 mL). Distension was assessed at only these 3 volumes (1, 4, and 10 mL) because of concerns about the duration of the procedure and risks for technical problems. Capsule integrity was confirmed ultrasonographically by an absence of leakage. The procedure was terminated for a particular joint if leakage or catheter displacement was noticed. For each volume injected, 2 ultrasonographers (a veterinarian in an equine internship and a veterinarian in the second year of a radiology residency) performed ultrasonographic examinations with a 7.5-MHz linear-array transducer placed in a sterile glove with coupling gel; a stand-off pad was not used. Alcohol was applied to the skin, and dorsal sagittal images of the dorsal recess were obtained with minimal manual pressure on the transducer. Three measurements of the maximal width of the dorsal recess were obtained with digital calipers by each ultrasonographer. The transducer was raised from the skin and repositioned for each measurement. Measurements were obtained between the dorsal cortex of the middle phalanx and the dorsal aspect of the joint capsule.
Two experienced board-certified equine surgeons evaluated distension of the dorsal recess by palpation of the DIP joint. A semiquantitative scoring system was used (no, moderate, or severe distension). Surgeons were not aware of the injection volume. Surgeons remained in a separate room during injections and ultrasonographic examinations; they were then summoned separately to perform palpation. Surgeons were not allowed to discuss their results. To ensure the surgeons remained as unbiased and blinded as possible to the ongoing procedures, they were not summoned to perform palpation after every injection, and they could be summoned twice to perform palpation after a single injection (order of palpations was not assigned before the experiments; requests for palpation were at the discretion of each ultrasonographer).
At the end of the experimental procedures, 125 mg of amikacinj was injected into each DIP joint to reduce the risk of septic arthritis. The catheter was removed, and a protective bandage was placed over the catheterization site for 24 hours. Each horse received 1 dose of phenylbutazonek (2.2 mg/kg, PO) immediately after the procedures were completed. Physical and lameness examinations were performed once each day for the first week after the procedures and then were performed once each week for the subsequent 2 weeks.
Statistical analysis—Intraobserver and interobserver repeatability of ultrasonographic measurements was assessed with the intraclass correlation coefficient obtained from a mixed linear model. The relationship between ultrasonographic measurements and injected volume was assessed with a repeated-measures ANOVA, with volume as the repeated factor for each subject. The association between ultrasonographic measurements and palpation grades was assessed with a mixed linear model, with horse as a random factor. For all linear models, a post hoc Tukey test was used to evaluate significant differences between measurement means for each injection volume.
Sensitivity and specificity of palpation were calculated by grouping moderate and severe grades as a positive result. The association between injected volume and palpation grade was assessed with a Cochran-Mantel-Haenszel test for repeated measures. Observer agreements were calculated with κ statistics. Strength of agreement indicated by the κ values was as follows: poor, κ < 0.20; fair, κ = 0.21 to 0.40; moderate, κ = 0.41 to 0.60; substantial, κ = 0.61 to 0.80; and excellent, κ = 0.81 to 0.99).21 A value of P < 0.05 was considered significant for all tests. All analyses were performed with commercial statistical software.l
Results
Ex vivo experiments—The maximum volume of saline solution that could be injected into a DIP joint without evident leakage detected with CT was 10 mL (Figure 1). This maximum volume was used to determine a range of volumes between 1 and 10 mL to be injected during the in vivo experiments. Only the dorsal recess of the DIP joint could consistently be visualized during ultrasonography with a linear probe. Portions of the lateral and medial parts of the synovium could be visualized in some horses, but mineralization of the ungular cartilage precluded examination of most of the palmar recess from a lateral or medial approach. The palmar recess was not observed because of the curved shape of the palmar aspect of the proximal phalanx.
The optimal catheter entry point was in the midsagittal plane at a point 3 to 4 cm proximal to the coronary band at 45° oblique to the skin surface. The transducer was positioned in the midsagittal plane distal to the catheter entry point. Therefore, the catheter was introduced through the common digital extensor tendon. A small quantity of air bubbles in the dorsal recess during the first injection ensured the catheter location was correct. In one of the forelimbs, injection of an excessive quantity of air bubbles precluded visual examination of the dorsal recess because of reverberation artifacts. Leakage into the periarticular tissues was observed in 3 joints after repetitive injections. One catheter was incorrectly placed, which led to immediate leakage into the periarticular tissues during the first injection.
In vivo experiments—The intra-articular catheter was safely inserted into the DIP joint in all standing sedated horses. Leakage of saline solution into the periarticular tissues was evident in 2 joints: one catheter displaced from the dorsal recess immediately after insertion, and another catheter displaced after injection of 4 mL of saline solution. Results for these 2 joints were excluded from further analyses; thus, results were available for the remaining 8 joints. No complications were identified during the follow-up observation period.
Intraobserver repeatability was excellent (intraclass correlation coefficient, > 0.89 to < 0.96) for ultrasonographic measurements. Interobserver repeatability was also excellent (intraclass correlation coefficient, 0.90). There was a significant (P < 0.001) overall increase in width of the dorsal recess of the DIP joint with an increase in injected volume (mean ± SD, 5.9 ± 1.3 mm before injection, 6.8 ± 1.2 mm after injection of 1 mL, 7.7 ± 0.9 mm after injection of 4 mL, and 8.6 ± 1.4 mm after injection of 10 mL (Figures 2 and 3). Furthermore, the mean width of the dorsal recess differed significantly among injection volumes.
Representative longitudinal ultrasonographic images of a DIP joint injected with 0 (A), 1 (B), 4 (C), or 10 (C) mL of saline solution. Images were obtained immediately medial or lateral to the catheter at the dorsal aspect of the DIP joint of a horse restrained in a standing weight-bearing position. Ultrasonographic measurements (dotted lines) of the dorsal recess were (A) 7.4, (B) 8.4, (C) 9.7, and (D) 10.2 mm, respectively. For each image, dorsal is toward the top and proximal is toward the left.
Citation: American Journal of Veterinary Research 75, 1; 10.2460/ajvr.75.1.34
Box-and-whiskers plots of ultrasonographic measurements of the dorsal recess of 8 DIP joints of 5 horses after injection of 0, 1, 4, and 10 mL of saline solution. Notice that the ultrasonographic measurement increases rapidly at smaller volumes and apparently plateaus at 10 mL. Each box represents the limits of the upper and lower quartiles, the horizontal line in each box represents the median, and the whiskers represent the upper and lower quartiles ± 1. 5 times the interquartile range.
Citation: American Journal of Veterinary Research 75, 1; 10.2460/ajvr.75.1.34
One surgeon performed 35 palpations, and the other surgeon performed 41 palpations. Interobserver agreement was assessed for 27 palpations. There was moderate (k = 0.47) interobserver agreement for palpation grades of synovial distension. Sensitivity was low (57%) for palpation to detect distension after injection of 1 mL but high for palpation to detect distension after injection of 4 mL (92%) and 10 mL (100%). Specificity for palpation was 75%. There was an overall increase in palpation grade for joint effusion with an increase in injected volume (Figure 4).
Stacked bar chart of the frequency of palpation grades (no distension [light gray bars], moderate distension [dark gray bars], and severe distention [black bars]) for the DIP joint after injection of various volumes of saline solution into the DIP joints of standing horses. Number of palpations was 8 for 0 mL, 7 for 1 mL, 13 for 4 mL, and 7 for 10 mL. There was a significant (P < 0.001) positive correlation between the volume injected and palpation grade.
Citation: American Journal of Veterinary Research 75, 1; 10.2460/ajvr.75.1.34
Palpation grade and ultrasonographic measurements had a significant (P < 0.001) positive association. Mean ± SD ultrasonographic measurements of the dorsal recess were 5.7 ± 1.3 mm, 7.6 ± 0.8 mm, and 8.9 ± 1.3 mm for DIP joints with palpation grades of no, moderate, or severe distension, respectively (Figure 5). Mean ultrasonographic measurements differed significantly among injection volumes.
Box-and-whiskers plots of ultrasonographic measurements of the dorsal recess of 8 DIP joints of 5 standing horses in relation to palpation grade. Data represent results for 1 ultrasonographer and 1 surgeon. See Figure 3 for remainder of key.
Citation: American Journal of Veterinary Research 75, 1; 10.2460/ajvr.75.1.34
Discussion
Ultrasonographic examination was superior to palpation for the assessment of experimentally induced effusion of the dorsal recess of the DIP joint. Ultrasonography was able to detect as little as 1 mL of fluid and had better repeatability than palpation. However, digital palpation permitted satisfactory detection of 4 mL of fluid (2 and 3 mL of fluid were not assessed).
A number of possible explanations existed for the lower threshold for detection of synovial effusion by ultrasonographic assessment of the equine DIP joint (1 mL), compared with detection of effusion in the human knee (4 to 7 mL)17,19 or ankle (2 mL).20 First, there may have been a smaller baseline volume of the DIP joint than for the human knee. Second, the location of the DIP joint within the hoof capsule may prevent expansion except in a proximal direction, and recesses would expand at lower volumes. Finally, the study was performed in horses in a standing weight-bearing position, in contrast to the position of the subjects in the human studies, and this would contribute to bulging of the dorsal recess. It is known that intra-articular pressure increases in horses in a standing weight-bearing position.22 Palpation of the recesses of the DIP joint had lower interobserver repeatability and low sensitivity after intra-articular injection of 1 mL of fluid, compared with results for ultrasonography. This observation agrees with previous findings in respect to palpation of human knees because clinical examination in 1 study18 detected effusion in only 36% of joints with effusion detected ultrasonographically.
The ultrasonographers were trained prior to the in vivo experiments in the present study because they measured the dorsal recess of the DIP joint during the ex vivo experiments, and this might have enhanced their agreement during the in vivo experiments. The surgeons had no preliminary training period. A training period for the surgeons with a consensus on the semiquantitative grades of distension following injections of various volumes may have enhanced subsequent agreement of palpation results.
There was an overall increase of the distension grade with increasing injection volume, and sensitivity for the detection of larger volumes (4 or 10 mL) was high (92% and 100%, respectively). However, sensitivity was lower (57%) for the detection of mild distension (1 mL). Moreover, there were only 4 injection volumes (0, 1, 4, and 10 mL) and 3 semiquantitative grades for palpation, so this may have further contributed to insensitivity for the palpation technique. Following an injection of 1 mL, it is possible that the palpators had to choose between grades of no distension and moderate distension.
The capacity of a joint to distend (10 mL for the DIP joint in the ex vivo experiments reported here) has physical limits beyond which joint pressure will increase. Palpation of synovial effusion incorporates assessment of both a subjective volume and pressure. Ultrasonography exclusively measures physical distortion. Therefore, the 2 assessment techniques used do not assess the same characteristics, which also may explain some of the discrepancy in results. It seems extremely unlikely that the presence of the catheter could have influenced scoring for palpations or ultrasonographic measurements because of its small diameter. In future studies, it may be of value to also compare palpation grades to joint pressure measurements.22–24
We attempted to ensure the surgeons (palpators) were not aware of the amount of fluid injected; however, it is likely that they anticipated progressive distension because no fluid was removed at any point. In an effort to remove bias, surgeons were randomly summoned twice or were not summoned at all after injection of a specific volume. Consequently, we believed the palpators did not know the actual volume that had been infused prior to each palpation.
Mean ± SD ultrasonographic measurements of the width of the dorsal recess of the DIP joint (5.9 ± 1.3 mm prior to injection) can serve as benchmark data for a typical adult horse without DIP joint distension. This measurement is expected to differ for larger or smaller breeds.
The question arises as to the clinical importance of synovial effusion in the DIP joint and whether the inability of a clinician to accurately detect an increase of 1 mL during palpation is of clinical relevance. The relationship of synovitis to underlying joint disease in horses remains largely unexplored; consequently, it is difficult to answer this question. It is clear from several studies25–27 with MRI that effusion in the DIP joint is an extremely common and apparently nonspecific finding, irrespective of additional findings. However, even high-field MRI underestimates the severity of DIP joint lesions.28 Although the technique lacks specificity,29,30 the potential importance of effusion should be verified by intra-articular analgesia.8,31 The correlation between DIP joint effusion and early osteoarthritis remains to be elucidated. Although synovitis is expected with advanced osteoarthritis,32 it is also probably a sentinel of early osteoarthritis in a joint. Some horses have DIP joint synovitis without signs of pain, but it remains unknown whether the synovitis in these horses reflects early structural or molecular changes in the articular cartilage with subsequent osteoarthritis. Similarly, the exact contribution of this frequent finding to lameness originating from the foot area has yet to be examined. It is noteworthy that the severity of joint effusion and synovitis has been linked to pain originating in the osteoarthritic knees of humans more consistently than has detection of other imaging features, such as osteophytosis, meniscal tears, and cartilage erosions.33–36 Therefore, it is possible that DIP joint effusion may contribute to lameness originating from the foot, but this warrants further investigation.
The present study was performed on healthy horses without radiographic signs of osteoarthritis or extra-articular soft tissue thickening (eg, periarticular edema or fibrosis). Periarticular edema would arise following trauma or joint sepsis. Capsular fibrosis is also evident in advanced osteoarthritis. It is likely that palpation would be even less reliable under these conditions. The compliance of the synovial membrane and fibrous capsule is unknown in pathological conditions. Fibrosis of the joint capsule could limit accurate palpation of the dorsal recess or potentially limit the capacity of the joint structures to distend. It is also possible that the maximal measurements obtained ultrasonographically in healthy DIP joints may be greater than the maximal measurements in chronically distended joints because of compensatory expansion of the joint tissues.
Although the thickness of the synovial membrane, which indicates hypertrophy in response to joint disease, was not assessed in the present study of healthy horses, the capacity to assess synovial membrane structures and synovial fluid is an additional advantage of ultrasonographic examination. Future prospective clinical studies are required to elucidate the association of DIP joint synovitis with lameness and pathological changes.
Ultrasonographic-guided intra-articular placement of the catheter into the dorsal recess of the DIP joint was tolerated well by most of the horses. The frequent leakage during the ex vivo experiments was likely attributable to the reduced elasticity of the postmortem specimens. This technique for intra-articular catheter placement could also potentially be used for joint lavage in horses with DIP joint sepsis.
Ultrasonography is recommended over digital palpation to accurately assess distension of the dorsal recess of the DIP joint in horses; ultrasonography provides high sensitivity and better repeatability than does palpation. However, the clinical relationship of synovial effusion with DIP joint pain and osteoarthritis in horses warrants additional prospective studies.
ABBREVIATION
| DIP | Distal interphalangeal |
Isovue 300 mg/mL, Bracco Diagnostics Inc, Vaughan, ON, Canada.
GE Lightspeed 16 slice helicoidal, General Electric, Mississauga, ON, Canada.
Prosound SSD 4000 Plus with 7.5-MHz linear transducer, Aloka Co Ltd, Vaudreuil-Dorion, QC, Canada.
BD Angiocath No. 381123, Becton Dickinson Infusion Therapy Systems Inc, Sandy, Utah.
EMLA, Astrazeneca Canada Inc, Mississauga, ON, Canada.
Rompun 10%, 100 mg/mL, Bayer Healthcare Inc, Toronto, ON, Canada.
Torbugesic 1%, 10 mg/mL, Pfizer Animal Health Inc, Kirkland, QC, Canada.
Marcaine 0.5%, 5 mg/mL, Hospira, Healthcare Corp, Montreal, QC, Canada.
Lurocaine, 20 mg/mL, Vetoquinol Inc, Lavaltrie, QC, Canada.
Amiglyde-V, 250 mg/mL, Wyeth Animal Health, Guelph, ON, Canada.
Phenylbutazone tablets, Dominion Veterinary Laboratories Ltd, Winnipeg, MB, Canada.
SAS, version 9.1, SAS Institute Inc, Cary, NC.
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