Vascular ultrasonographic findings in canine patients with clinically diagnosed phlebitis

Abstract Peripheral vein phlebitis (inflammation) is a relatively frequent complication in dogs, however, published information on the ultrasonographic characteristics is currently lacking. This prospective, observational study describes the ultrasound (US) characteristics of normal canine cephalic veins, and veins with clinical phlebitis. Correlations among US findings and between US findings versus time that the intravenous catheter was in place were investigated. Safety of the US procedure was evaluated. Fifty patients were prospectively recruited for the study and 18 met the final inclusion criteria. Each patient underwent daily US examinations and was assessed for multiple criteria (vascular wall appearance, compressibility, spontaneity of flow, color fill, and presence/absence of filling defects, flow contour, direction, non‐pulsatility). Characteristics of normal canine cephalic veins were as follows: smooth and thin wall, complete compressibility, no flow disturbances, no filling defects, smooth flow contours, and unidirectional, non‐pulsatile flow with no turbulence. Characteristics of cephalic veins with clinical phlebitis were as follows: wall thickening (83%), decreased compressibility (55%), filling defects consistent with intraluminal thrombus (55%), vessel wall hyperechogenicity (44%), and abnormal color Doppler flow (39%). Significant correlations were found between Doppler filling defects and compressibility, Doppler filling defects and presumed thrombosis, and compressibility and presumed thrombosis (P = .001, P = .001, P = .000, respectively). No correlation was found between the US findings and time the intravenous catheter was in place. Findings indicated that duplex and compressibility US are feasible and safe methods for characterizing and monitoring cephalic veins in dogs with clinical phlebitis.

thrombophlebitis classified as the end stage of phlebitis. 4 In veterinary practice, phlebitis is most commonly diagnosed based on subjective clinical characteristics such as warmth, pain on injection, swelling, and erythema. 16,17 The incidence of phlebitis ranges from 3% 16 to 22%. 17 Duplex US uses a combination of traditional real-time grey scale US (B-mode) and color Doppler sonography, and has become the gold standard in assessing the morphology and hemodynamics of the vascular system in human medicine. 9 This imaging modality has largely replaced venography in the diagnosis and management of leg vein thrombosis in humans. The procedure can be done at the patient's bed-side and is widely available. 7 Several studies have been published documenting its diagnostic accuracy in humans. 8,[18][19][20][21][22] Compressibility US is often combined with duplex US for vascular imaging in humans and involves application of manual compression with enough pressure on the skin to completely obliterate the normal vein lumen. 23 The appearance of a thrombus has been described as variable, depending on its chronicity. In acute stages, a thrombus may be poorly echogenic and might be more difficult to visualize using B-mode and Doppler ultrasonography. This is why the standard B-mode and Doppler US examinations are routinely combined with the compressibility US technique. Multiple reports have been published on vascular US in the abdomen of small animals, however published studies on superficial vascular US are currently lacking. 24,25 Our hypotheses were that duplex US and compressibility US methods would be feasible and safe for investigation of cephalic veins in canine patients, that US abnormalities would be present in patients with clinically diagnosed phlebitis, and that there would be positive correlations between US findings and time the intravenous catheter was in place. Therefore, the objectives of this study were fourfold: (1) describe the US features of normal canine cephalic veins; (2) describe the US features of cephalic veins in dogs with clinically diagnosed phlebitis; (3) test correlations among US findings and between US findings and time the intravenous catheter was in place; and (4) describe approximate times for performing examinations and any adverse reactions to the scanning procedure. The primary inclusion criteria included the following: (1) heart rate, respiratory rate, and pulse quality that were within normal limits and

Patient population
(2) no suggestion of vascular disease on the day of admission. The final inclusion criterion was a clinical diagnosis of cephalic phlebitis by the anesthetist that was based on at least one of the following criteria: erythema, edema, and/or response to injection. Initial exclusion criteria included the following: (1) preexisting known cephalic vein pathology; (2) known peripheral venous catheterization of the cephalic vein less than 7 days prior to the scan, and (3) extremity tumor where the radiotherapy would be delivered in that location. Dogs that did not develop clinical phlebitis were excluded from the analysis. All decisions for study inclusion or exclusion were independently made by a veterinary radiologist in training (J.L.) and were based on medical record entries.

Ultrasound technique
All US studies were performed and interpreted by the same veteri-  Clinical assessments were performed and recorded by multiple anesthesiologists on radiotherapy duty (residents with at least 2 years of clinical experience and board-certified anesthesiologists).
Observers were instructed by an anesthesiologist in training (H.L.) and all data were recorded on a standardized form specifically prepared for the purpose of this study. All decisions were made independently and the anesthesiologists were blinded to the ultrasonographic findings.

Statistical analysis
Statistical analysis was selected and performed by a veterinary radiologist in training (J.L.), as advised by the University's statistician.

Patient population
A total of 50 dogs undergoing daily radiotherapy met initial inclusion criteria for the study. Of those, 18 met the final inclusion criteria.
There were 12 females (two entire and 10 neutered) and six males  The US findings from patients with clinical phlebitis are summarized in Table 1.  Table 2.

DISCUSSION
Based on our review of the literature, the use of duplex US (B-mode and Doppler) and compressibility US for characterizing normal and pathologic superficial veins of the canine thoracic limb has not been previously published. The ultrasonographic characteristics of normal superficial veins in our sample population of dogs were similar to those reported in humans and are included in Table 1 and Figure 1. 23 Authors did not identify US abnormalities in the patient cohort examined on day 1. All patients that showed clinical signs consistent with phlebitis also showed US changes.
Wall thickening was the most common US finding in this sample of dogs. In normal conditions the vascular wall is smooth and thin and often difficult to visualize as it blends with the surrounding tissues. 23 Any increase in wall thickness should then raise a suspicion of early inflammatory changes. These findings replicate what has been published in human medicine with regards to superficial thrombosis, phlebitis, and thrombophlebitis. 14,23,26 In veterinary medicine, ultrasonography is also used routinely in horses to diagnose jugular vein thrombophlebitis. 26,27 The US appearance of abnormal vessels in our patient group, was consistent with that reported in the jugular vein of equine patients. 26 Presumed intraluminal thrombosis was diagnosed in 10 of our patients, but only seven dogs in our study showed color Doppler filling defects. All 10 patients with presumed intraluminal thrombus had decreased compressibility ( Figure 2). One would expect flow disturbances to be present in all the cases of thrombosis, however, our findings were supported by a previous review article in which the disappearance of the color signal was not considered to be a strict requirement for exclusion of thrombosis in humans. 28 The essential, exclusion criterion for thrombosis was described as complete compressibility of the vein. Lack of compressibility was therefore considered to be diagnostic for thrombosis in humans, as direct visualization of a thrombus could not always be achieved. Critically ill dogs may therefore benefit from this scanning protocol, which requires only minimal manual restraint, and short scanning time.
F I G U R E 1 A, Transverse (left image) and sagittal (right image) B mode images of a normal canine cephalic vein (between calipers). B, Normal color Doppler flow. C, The same vessel in transverse plane before (left image) and after (right image) manual pressure has been applied and the vascular lumen has been compressed (arrows). In sagittal images, the proximal vein is to the left of the screen and distal vein to the right of the screen. In transverse plane, the lateral aspect is shown to the left of the screen. Images were acquired with a high frequency linear array transducer (10-18 MHz) F I G U R E 2 A, Transverse (left image) and sagittal (right image) B mode images of a vein with a presumed intraluminal thrombus (between callipers). B, A thrombotic vessel with color Doppler filling defect. Note the echogenic structure in the far field that represents the thrombus in sagittal plane (between calipers). C, The same vessel in transverse plane before (left image) and after (right image) manual pressure has been applied and the vascular lumen has not been compressed because of the intraluminal structure (between calipers). In sagittal images, the proximal vein is to the left of the screen and distal vein to the right of the screen. In transverse plane, the lateral aspect is shown to the left of the screen. Images were acquired with a high frequency linear array transducer (10-18 MHz) The main limitation of this study was a relatively small sample size.
A larger number of dogs would have allowed more accurate description of the findings and determination whether a correlation existed between clinical signs and time the intravenous catheter was in place.
The clinically suspected phlebitis was not confirmed histologically; however, this was not possible in our client-owned patient cohort. In our clinical cases, visualization of the venous structures was possible in all patients but varied depending on the size of the dog. Ultrasound visualization of the cephalic vein in smaller dogs was more challenging compared to larger breeds due to complete collapse of the vessel lumen with probe pressure. Thus, the use of this technique in small breeds of dogs requires more skill and training. This is in accordance with human studies where decreased vessel size prevents US examination. 29 In this study, the procedure has been performed always by the same operator and this represents a limitation as generalizability of findings for operators with lower or no ultrasound experience was not assessed. In