Epinephrine-enhanced computed tomographic

Research in Veterinary Science 102 (2015) 15–21

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Epinephrine-enhanced computed tomographic arthrography of the canine shoulder Lieve De Rycke a,⁎, Henri van Bree a, Annemie Van Caelenberg a, Ingeborgh Polis b, Luc Duchateau c, Ingrid Gielen a a b c

Department of Veterinary Medical Imaging and Small Animal Orthopaedics, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium Department of Medicine and Clinical Biology of Small Animals, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium Department of Comparative Physiology and Biometrics, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium

a r t i c l e

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Article history: Received 8 January 2014 Received in revised form 6 May 2015 Accepted 21 June 2015 Available online xxxx Keywords: Canine Shoulder Computed tomography Arthrography Epinephrine

a b s t r a c t The aim of this study was to investigate the effect of epinephrine-enhanced computed tomographic arthrography (CTA) on the image sharpness of the lateral and medial glenohumeral ligaments (LGHL and MGHL, respectively), biceps tendon (BT) and joint cartilage (JC) in the canine shoulder. The shoulders of eight normal dogs were examined using a 4-slice helical CT scanner. The right shoulders were injected with Iohexol and the left shoulders with a mixture of Iohexol and epinephrine. CTA images were obtained after 1, 3, 5, 9, 13, 20 and 30 min and the image sharpness of the intra-articular structures in both shoulders was graded for visibility. The attenuation values were measured to examine the persistence of contrast appearance. Admixture of epinephrine and Iohexol significantly improved the image sharpness of the LGHL and the BT, especially on delayed CTA images. The use of epinephrine did not negatively affect post-CTA recovery. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction In human medicine, CTA of the shoulder is widely used to evaluate rotator cuff tears, and labral or capsular abnormalities, and to assess cartilage pathology (Rafii et al., 1986; Yang et al., 1987; De Maeseneer et al., 2000; Charousset et al., 2005; Lecouvet et al., 2007; Lecouvet et al., 2008; Omoumi et al., 2011). In veterinary medicine, CTA of the canine shoulder performed with a 4-slice helical CT-device, is used to evaluate the joint cartilage and intra-articular structures such as the glenohumeral ligaments and the BT (De Rycke et al., 2015). In general, the accuracy and usefulness of arthrography depend on the contrast medium providing a sharp outline of the intra-articular structures. Once the concentration of iodinated contrast material is injected into the joint, it decreases within minutes through diffusion into the cartilage and the highly vascular synovium, resorption, and fluid influx into the joint. Rapid deterioration of the image quality may follow, making the intra-capsular structures indiscernible because of the lack of detail (Spataro et al., 1978; Oberman and Kieft, 1987; Obermann et al., 1989; Van Bree, 1989; Wellings et al., 1994). In animals where inflammatory changes and synovial hyperemia occur, even more rapid resorption of the contrast medium can be expected (Katzberg et al., 1976; Spataro et al., 1978; Wellings et al., 1994). The CTA examination must therefore be performed quickly after intra-articular ⁎ Corresponding author. E-mail address: [email protected] (L. De Rycke).

http://dx.doi.org/10.1016/j.rvsc.2015.06.009 0034-5288/© 2015 Elsevier Ltd. All rights reserved.

injection of the contrast medium to minimize the absorption of contrast solution (Wellings et al., 1994). Also, it is best to use a contrast medium that resorbs slowly (Wellings et al., 1994; Blum et al., 2000). Human studies have shown that non-ionic dimeric contrast agents likely will undergo fewer dilution and resorption processes than non-ionic monomeric contrast agents, and provide a better contrast in delayed CT scans (Ingram and Stoker, 1986; Oberman and Kieft, 1987; Obermann et al., 1989; Wellings et al., 1994; Blum et al., 2000). However, for delayed CTA examinations, adding epinephrine to non-ionic monomeric contrast agents can produce a significant improvement in CT density that surpasses the density provided when the dimeric contrast agent is used alone (Wellings et al., 1994). Epinephrine has a vasoconstrictive effect on the synovial membrane, which temporarily reduces the fluid movement across the membrane (Hall, 1974; Spataro et al., 1978; Ng et al., 1989; Wellings et al., 1994; Jacobsen et al., 2003; Mutschler et al., 2003). This may be important, depending on the interval between the time of injection into the joint and the CT imaging (Jacobsen et al., 2003). The initial sharpness of the image can be improved and image degradation delayed by the greater persistence of the contrast medium in the joint, as well in cases with hyperemic synovia (Wellings et al., 1994). In veterinary medicine, studies have confirmed that image sharpness is improved when epinephrine is added to an ionic contrast medium (diatrizoate meglumine, urografin) with conventional arthrography of the canine shoulder and knee (Hall, 1974; Spataro et al., 1978; Van Bree, 1989). Intra-articular injection of Iohexol is now the method of choice for veterinary arthrography (Hong et al., 2010), including at our

L. De Rycke et al. / Research in Veterinary Science 102 (2015) 15–21

clinic, where arthrographic examinations of the canine shoulder are routinely performed using Iohexol, a non-ionic, monomeric contrast agent. Except for one experimental study on CTA of the canine shoulder (De Rycke et al., 2015), nothing has been published about the use of CTA in veterinary practice. The CTA procedure can be more time-consuming than conventional arthrography, so the need for admixture of epinephrine and Iohexol (Omnipaque) is desirable, but as yet of undetermined efficacy. In this CTA study, the effect of admixture of epinephrine and Omnipaque on the image sharpness of the LGHL, MGHL, BT and JC in the canine shoulder was studied on CTA images taken 1, 3, 5, 9, 13, 20 and 30 min after injection. The persistence of the contrast medium on delayed CTA images was also investigated by measuring the attenuation values Hounsfield Units (HU) in the caudal pouch of the glenohumeral joint. 2. Materials and methods 2.1. Animals CTA was performed on both shoulders of eight clinically normal, 3- to 6-year-old dogs (two foxhounds and six beagles). The dogs were maintained and the procedures performed, in accordance with the Ethical Committee of the Faculty of Veterinary Medicine, Ghent University. None of the dogs had a history of shoulder disease and no abnormalities were detected during physical and radiographic examinations. Two standard radiographs (mediolateral and craniocaudal) were obtained for each shoulder. All shoulder regions were clipped before the scanning procedure. 2.2. CTA The dogs were sedated with medetomidine hydrochloride 1 (30–50 ug/kg of body weight, IM), anesthesia was induced with propofol2 (bolus of 1–2 mg/kg of body weight, IV given to effect) and the dogs were intubated. Anesthesia was maintained with isoflurane3 in oxygen. The dogs were positioned in ventral recumbency with both forelimbs extended cranially on the table of a 4-slice helical CT device.4 Lateral and dorsoventral scout views were taken with an extension angle of 120–150° maintained between the spine of the scapula and the long axis of the humerus. Native, transverse, 1.3-mm thick slices with a 0.7-mm interval of both shoulders also were obtained from the mid-scapula to the mid-humerus regions and perpendicular to the long axis of the spine of the scapula. Settings for the CT imaging, calculated using a bone algorithm, were 120 kV and 140 mA. Image matrix size was 512 × 512 and field of view was 25 cm. All the images were taken in approximately 4 min. During the arthrographic CT scan, each dog was studied using contrast medium5 alone in the right shoulder and a mixture of contrast medium and epinephrine6 in the left shoulder. The dogs were positioned in left lateral recumbency, and 4–6 ml of contrast medium (Omnipaque 240: 4 ml for the beagles, 6 ml for the foxhounds) diluted to 100 mg/ml with sterile saline (0.9% NaCl) was injected into the right shoulder. Immediately after the injection, the dogs were turned to right lateral recumbency and their left shoulders were injected with the same amount of contrast medium mixed with 0.2 mg (0.25 ml) of epinephrine6. This injection time was noted as time zero. Next, the dogs were positioned in ventral recumbency with both forelimbs extended cranially and CT images of both shoulders were obtained 1, 3, 5, 9, 13, 20 and 30 min after the intra-articular injection using the same settings. The reconstructed CT images that were acquired in dorsal and sagittal planes using CT reconstruction imaging software7 were high quality because of their 1.3-mm thickness. 1 2 3 4 5 6 7

The use of epinephrine did not negatively affect post-CTA recovery. After completion of the study, the CTA images of each dog, both with and without epinephrine injection, were evaluated, compared and scored by blinded radiologists. Three experienced radiologists, who had no knowledge about the time when the CT was performed or which side received the epinephrine injection, interpreted the arthrograms. The radiologists agreed by consensus about the image sharpness of the intra-articular structures with medium-coated contrast and the persistence of the contrast medium when they evaluated the images. The persistence of contrast medium was determined by measuring the attenuation value (HU) at the caudal pouch of the glenohumeral joint. For each specific set of arthrograms (performed at a certain time) an average HU score was calculated for the eight dogs, with separate calculations made for the shoulders injected with epinephrine and those without. The MGHL, LGHL, and BT at the height of the intertubercular sulcus and the joint JC on the CTA images with and without epinephrine were graded for visibility on a scale from 3 to 0 (3 = excellent visibility, 2 = moderate, 1 = poor, 0 = not visible). The CTA images performed at 1, 3, 5, 9, 13, 20 and 30 min after the intra-articular injection were graded separately. For each structure, an average score was calculated for each time period for the eight dogs. A mixed model was fitted to HU, the score of the three different structures separately and the average score as response variables, including dog as random effect, and time (continuous), epinephrine (categorical) and their interaction as fixed effects. To assess the effect of epinephrine, we test the hypothesis whether the slopes with and without epinephrine, corresponding to the reduction of score or HU over time, differ significantly from each other using a F-test at the 5% significance level.

3. Results The decrease of HU was not significantly faster (P = 0.50) in shoulders without epinephrine (slope = −13.2 (se = 2.24)) compared with the shoulders with epinephrine (slope = −9.7 (se = 2.24)) (Fig. 1). For the BT, the visibility score decreased significantly faster in the shoulders without epinephrine (slope = −0.048 (se = 0.007)) compared with those with epinephrine (slope = − 0.024 (se = 0.007)) (P = 0.0037) (Fig. 2). CTA images of both shoulders of one dog, 1 and 30 min after injection showed that the visibility score for the BT decreased from 2 to 0 in the shoulder without epinephrine and from 3 to 1 with epinephrine (Fig. 3).

2500

Houndsfield Units

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0 Domitor, Orion Corp, Espoo, Finland. Rapinovet, Schering-Plough, Comazzo, Italy. IsoFlo, Abbott Laboratories, Abbott Park, IL. CT-scanner, LightSpeed, GE Medical Systems, Milwaukee, WI. Omnipaque 240, GE Healthcare Ireland, Cork, Ireland. Epinephrine HLC (adrenaline 0.8 mg/mL) Sterop, Brussels, Belgium. OsiriX 32-bit, advanced open source PACS workstation, DICOM viewer.

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Time minutes after injection Fig. 1. Mean Hounsfield Units (HU) in the caudal pouch of the shoulder joint versus time comparing shoulders with Iohexol alone and with Iohexol and epinephrine.

L. De Rycke et al. / Research in Veterinary Science 102 (2015) 15–21 3

Mean visibility score BT

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Time minutes after injection Fig. 2. Mean visibility score for the biceps tendon versus time comparing shoulders with Iohexol alone and with Iohexol and epinephrine.

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For the MGHL, the visibility score decreased at similar rates in the shoulders without epinephrine (slope = − 0.037 (se = 0.007)) compared with those with epinephrine (slope = −0.034 (se = 0.007)) (P = 0.742) (Fig. 4). Fig. 5 shows the comparison of the CTA images of both shoulders of one dog, 1 and 30 min after the injection. No difference can be observed for the MGHL, because the visibility scores decreased from 3 to 1 in both shoulders. For the LGHL, the visibility score decreased at a significantly faster rate in the shoulders without epinephrine (slope = − 0.050 (se = 0.008)) compared with those with epinephrine (slope = − 0.031 (se = 0.008)) (P = 0.041) (Fig. 6). Fig. 7 shows the CTA images of both shoulders from one dog, 1 and 30 min after the injection. The visibility score for the LGHL decreased from 3 to 0 in the shoulder without epinephrine and from 3 to 1 in the shoulder with epinephrine. For the JC, the visibility decreased at similar rates in the shoulders without epinephrine (slope = −0.032 (se = 0.007)) and those with epinephrine (slope = −0.023 (se = 0.007)) (P = 0.220) (Fig. 8). Fig. 9 shows the CTA images of the left shoulder (with epinephrine) of one

Fig. 3. Comparison of the CTA images of the right shoulder with Iohexol alone (A, C) and the left shoulder with Iohexol and epinephrine (B, D), 1 (A, B) and 30 (C, D) minutes after injection. The visibility score for the BT decreases from 3 to 0 in the shoulder without epinephrine and from 3 to 1 in the shoulder with epinephrine.

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Time minutes after injection Fig. 4. Mean visibility score for the MGHL in the shoulders versus time comparing the shoulders with Iohexol alone and with Iohexol and epinephrine.

dog compared 1 and 30 min after the injection. The visibility score decreased from 3 to 1, which was the same as the shoulder without epinephrine.

Time minutes after injection Fig. 6. Mean visibility score for the LGHL versus time comparing shoulders with Iohexol alone and with Iohexol and epinephrine.

The overall visibility score for all the structures decreased significantly faster in the shoulders without epinephrine (slope = − 0.041 (se = 0.006)) compared with those with epinephrine (slope = −0.028 (se = 0.006)) (P = 0.047).

Fig. 5. Comparison of the CTA images of the right shoulder with Iohexol alone (A, C) and the left shoulder with Iohexol and epinephrine (B, D), 1 (A, B) and 30 (C, D) minutes after injection. The visibility score for the MGHL decreases from 3 to 1 in both shoulders.


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Fig. 7. Comparison of the CTA images of the right shoulder with Iohexol alone (A, C) and the left shoulder with Iohexol and epinephrine (B, D), 1 (A, B) and 30 (C, D) minutes after the injection. The visibility score for the LGHL decreases from 3 to 0 in the right shoulder and from 3 to 1 in the left shoulder.

4. Discussion and conclusions The study results suggest that admixture of epinephrine and the non-ionic, monomeric contrast medium Iohexol increases the visibility of the intra-articular structures in delayed CT arthrograms. The effect of epinephrine on the visibility of the BT and LGHL is highly significant. In veterinary medicine, Iohexol is the drug of choice for intraarticular injection in arthrography (Hong et al., 2010) but no reports have been published on the admixture of epinephrine for CTA. In human medicine studies, epinephrine was not added when non-ionic

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Mean Visibility score JC

A contrast-enhanced infraspinatus bursa, between the tendon of the infraspinatus and the greater tubercle of the humerus, was seen in one dog (Fig. 10). In another dog, a synovial blind pouch of the glenohumeral joint was visible between the deep pectoral muscle and the triceps brachii muscle (Fig. 11). Because a large amount of contrast agent filled the pouch in this dog, less contrast remained in the joint space, which resulted in low visibility scores for the intra-articular structures.

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Time minutes after injection Fig. 8. Mean visibility score for the JC versus time comparing shoulders with Iohexol alone and with Iohexol and epinephrine.

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Fig. 9. CTA of the canine left shoulder with Iohexol and epinephrine, 1 and 30 min after injection. The visibility score for the JC decreases from 3 to 1.

monomeric (Blum et al., 2000; Binkert et al., 2003; Charousset et al., 2005; Moser et al., 2008; Wyler et al., 2009) or dimeric contrast agents (Blum et al., 2000) were used for CTA of the shoulder, but it was added in a combined study of magnetic resonance imaging (MRA) and CTA (Jacobsen et al., 2003). These contrast agents remain in the joint longer than ionic contrast agents (Hong et al., 2010) and epinephrine is therefore unnecessary because a CTA procedure rarely takes more than 30 min (Oberman and Kieft, 1987; Obermann et al., 1989; Wellings et al., 1994; Omoumi et al., 2011). Qualitative studies have shown that dimeric agents are better than monomeric agents for arthrography (Schmidt and Papassotiriou, 1989). However, if a 45-minute or more delay is anticipated, adding epinephrine to non-ionic monomeric contrast agents can significantly improve CT density, even more than produced by the dimeric contrast agent alone (Wellings et al., 1994).

In human literature, admixture of epinephrine and ionic contrast media is routine for CTA procedures of the joints when using diatrizoate meglumine (renografin, hypaque) (Rafii et al., 1986; McNiesh and Callaghan, 1987; Yang et al., 1987), iothalamate meglumine (Pennes et al., 1989) or ioxaglate meglumine (Hexabrix) (Vande Berg et al., 2000; Vande Berg et al., 2002; Mutschler et al., 2003; Lecouvet et al., 2007). Other investigators who use Ioxaglate meglumine (Hexabrix) for CTA do not add epinephrine. One author (Ng et al., 1989) reported that adding adrenaline to the ionic Ioxaglate meglumine (Hexabrix) produces no significant improvement in arthrographic quality in either immediate or delayed films. According to the ‘Instructions for Use’ with Hexabrix, the concomitant use of epinephrine is not necessary because Hexabrix's low osmolality reduces the rate of contrast medium absorption, as well as the production of synovial fluid and consequent dilution of the medium. Furthermore, epinephrine increases the articular

Fig. 10. CTA of the left shoulder with contrast filling of the bursa infraspinatus.

Fig. 11. CTA of the left shoulder showing a synovial blind pouch of the glenohumeral joint coursing distally between the deep pectoral muscle and the triceps brachii muscle.


reaction and the pain associated with ionic contrast agents (Corbetti et al., 1986), either because epinephrine is a direct irritant to the synovium or because it increases the time the synovium is exposed to the hyperosmolar contrast agent (Hall et al., 1985; Ng et al., 1989). This post-arthrographic morbidity is not seen when combining adrenaline with non-ionic contrast media (Corbetti et al., 1986). No complications or injection-associated discomfort occurred in this study. To avoid beam-hardening artifacts, the contrast material is routinely diluted with saline (Lecouvet et al., 2008; Omoumi et al., 2011). However, no consensus has been established on the need for dilution, which mainly depends on the radiologists' preferences (Lecouvet et al., 2007). In this study, the contrast medium (Omnipaque 240) was diluted to 100 mg/ml with sterile saline (0.9% NaCl). To avoid further dilution, the synovial joint fluid was aspirated and 4–6 ml of diluted contrast agent was injected into the shoulder. This amount of contrast material is routinely used for this procedure at our institution, and whether there would be any advantage with a larger amount was not assessed. According to Jacobsen et al., 2003 the amount of injected contrast medium can vary in cases of pathologic shoulder disease. In humans, a patient with chronic shoulder subluxation may require more volume and a patient with adhesive capsulitis may require less. Increased resistance to injection or the retrograde flow of contrast material from the connecting tubing after the syringe is disconnected indicates adequate joint distention (Jacobsen et al., 2003). In humans, lidocaine or xylocaine may be added to the contrast medium to provide pain relief that will help the patient remain motionless during the examination (Blum et al., 2000; Brown et al., 2000; Charousset et al., 2005), although the injection of local anesthesia for arthrography is painful (Moser et al., 2008). Canine patients are placed under general anesthesia, so no local anesthetic is necessary. In this study, 0.2 mg (4.2–6.2%) epinephrine was added to the contrast medium. No veterinary studies show that a smaller dosage of epinephrine would be equally effective. Generally, acceptable images would be expected with an attenuation value in excess of 1500 HU (Wellings et al., 1994). In our study, the mean HU at 30 min was 1447 in the shoulders without epinephrine and 1653 in the shoulders with epinephrine. In conclusion, admixture of epinephrine and non-ionic monomeric contrast agents to perform CTA of the canine shoulder can help visualize the intra-articular structures, especially when examinations are delayed. This positive effect of epinephrine may be more pronounced when CTA is performed on pathologic shoulders with inflammatory changes, where even more rapid resorption of the contrast medium can be expected. Further studies are needed to confirm these predictions about epinephrine's usefulness for diseased joints. References Binkert, C.A., Verdun, F.R., Zanetti, M., Pfirrmann, C., Hodler, J., 2003. CT arthrography of the glenohumeral joint: CT fluoroscopy versus conventional CT and fluoroscopy — comparison of image-guidance techniques. Radiology 229, 153–158. Blum, A.G., Simon, J.M., Cotton, A., Quirin-Cosmidis, I., Boyer, B., Boutry, N., Antonini, J.P., 2000. Comparison of double-contrast CT arthrography image quality with nonionic contrast agents: isotonic dimeric Iodixanol 270 mg I/mL and monomeric Iohexol 300 mg I/mL. Investig. Radiol. 35, 304–310. Brown, R.R., Clarke, D.W., Daffner, R.H., 2000. Is a mixture of gadolinium and iodated contrast material safe during arthrography? Am. J. Roentgenol. 175, 1087–1090. Charousset, C., Bellaïche, L., Duanthon, L.D., Grimberg, J., 2005. Accuracy of CT arthrography in the assessment of tears of the rotator cuff. J. Bone Joint Surg. 87-B, 824–828. Corbetti, F., Malatesta, V., Camposampiero, A., Mazzi, A., Punzi, L., Angelini, F., Vigo, M., Todesco, S., 1986. Knee arthrography: effects of various contrast media and epinephrine on synovial fluid. Radiology 161, 195–198.

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