• View in gallery

    Representative lateral radiographic view of a male ferret in which digital subtraction angiography was used, revealing the location of a balloon catheter used to temporarily occlude the CVC, collateral blood flow caused by the occlusion, and extravasation of contrast medium.

  • View in gallery

    Representative ventrodorsal radiographic view of the same ferret as in Figure 1, obtained with the same imaging method.

  • View in gallery

    Representative lateral radiographic view of a female ferret in which digital subtraction angiography was used, revealing the location of a balloon catheter used to temporarily occlude the CVC and collateral blood flow caused by the occlusion.

  • View in gallery

    Representative ventrodorsal radiographic view of the same ferret as in Figure 3, obtained with the same imaging method.

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Collateral circulation in ferrets (Mustela putorius) during temporary occlusion of the caudal vena cava

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  • 1 Southern California Veterinary Specialty Hospital, 1371 Reynolds Ave, Irvine, CA 92614.
  • | 2 Department of Clinical Studies, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.
  • | 3 College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.
  • | 4 Department of Clinical Studies, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.
  • | 5 Department of Clinical Studies, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.
  • | 6 Department of Clinical Studies, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.
  • | 7 Department of Clinical Studies, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.
  • | 8 Department of Clinical Studies, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.
  • | 9 Department of Radiology, Division of Interventional Radiology, Medical Center, University of Pennsylvania, Philadelphia, PA 19104.

Abstract

OBJECTIVE To determine whether extent of collateral circulation would change during temporary occlusion of the caudal vena cava (CVC) in ferrets (Mustela putorius), a pressure change would occur caudal to the occlusion, and differences would exist between the sexes with respect to those changes.

ANIMALS 8 adult ferrets (4 castrated males and 4 spayed females).

PROCEDURES Ferrets were anesthetized. A balloon occlusion catheter was introduced through a jugular vein, passed into the CVC by use of fluoroscopy, positioned cranial to the right renal vein, and inflated for 20 minutes. Venography was performed 5 and 15 minutes after occlusion. Pressure in the CVC caudal to the occlusion was measured continuously. A CBC, plasma biochemical analysis, and urinalysis were performed immediately after the procedure and 2 or 3 days later.

RESULTS All 8 ferrets survived the procedure; no differences were apparent between the sexes. Vessels providing collateral circulation were identified in all ferrets, indicating blood flow to the paravertebral venous plexus. Complications observed prior to occlusion included atrial and ventricular premature contractions. Complications after occlusion included bradycardia, seizures, and extravasation of contrast medium. Mean baseline CVC pressure was 5.4 cm H2O. During occlusion, 6 ferrets had a moderate increase in CVC pressure (mean, 24.3 cm H2O) and 2 ferrets had a marked increase in CVC pressure to > 55.0 cm H2O.

CONCLUSIONS AND CLINICAL RELEVANCE Caval occlusion for 20 minutes was performed in healthy ferrets with minimal adverse effects noted within the follow-up period and no apparent differences between sexes. The CVC pressure during occlusion may be prognostic in ferrets undergoing surgical ligation of the CVC, which commonly occurs during adrenal tumor resection.

Abstract

OBJECTIVE To determine whether extent of collateral circulation would change during temporary occlusion of the caudal vena cava (CVC) in ferrets (Mustela putorius), a pressure change would occur caudal to the occlusion, and differences would exist between the sexes with respect to those changes.

ANIMALS 8 adult ferrets (4 castrated males and 4 spayed females).

PROCEDURES Ferrets were anesthetized. A balloon occlusion catheter was introduced through a jugular vein, passed into the CVC by use of fluoroscopy, positioned cranial to the right renal vein, and inflated for 20 minutes. Venography was performed 5 and 15 minutes after occlusion. Pressure in the CVC caudal to the occlusion was measured continuously. A CBC, plasma biochemical analysis, and urinalysis were performed immediately after the procedure and 2 or 3 days later.

RESULTS All 8 ferrets survived the procedure; no differences were apparent between the sexes. Vessels providing collateral circulation were identified in all ferrets, indicating blood flow to the paravertebral venous plexus. Complications observed prior to occlusion included atrial and ventricular premature contractions. Complications after occlusion included bradycardia, seizures, and extravasation of contrast medium. Mean baseline CVC pressure was 5.4 cm H2O. During occlusion, 6 ferrets had a moderate increase in CVC pressure (mean, 24.3 cm H2O) and 2 ferrets had a marked increase in CVC pressure to > 55.0 cm H2O.

CONCLUSIONS AND CLINICAL RELEVANCE Caval occlusion for 20 minutes was performed in healthy ferrets with minimal adverse effects noted within the follow-up period and no apparent differences between sexes. The CVC pressure during occlusion may be prognostic in ferrets undergoing surgical ligation of the CVC, which commonly occurs during adrenal tumor resection.

Hyperadrenocorticism is a common disease affecting domestic ferrets in the United States. Clinical signs and methods of diagnosis have been well described.1–8 Approximately 70% of ferrets with this disease develop clinically important alopecia, and 30% have pruritus. Ninety percent of affected female ferrets have vulvar swelling. Male ferrets may develop stranguria caused by hyperplasia of the periurethral prostatic tissue. An increase in sexual aggression has also been identified in neutered males with hyperadrenocorticism.9 A small number of ferrets with hyperadrenocorticism have developed life-threatening, nonregenerative anemia secondary to bone marrow suppression. Clinical signs are related to increases in circulating concentrations of sex hormones produced by the abnormal adrenal tissue; glucocorticoid production is not typically affected in ferrets.1,7,10–14

Confirmation of hyperadrenocorticism can be achieved by performance of an adrenal gland androgen assay, which is available through the University of Tennessee.7 This assay measures estradiol, androstenendione, and 17-hydroxyprogesterone concentrations in serum samples. Histologically, hyperadrenocorticism may be characterized as adrenocortical hyperplasia, cortical adenoma, or cortical adenocarcinoma.15,16

Several drugs that target sex hormone production have been proposed for the management of adrenocortical disease in ferrets.2,13,17–19 Deslorelin acetate, a gonadotropin-releasing hormone agonist, has recently been introduced to the US market. Use of this drug has gained popularity in Europe over the past decade for treatment of ferrets with hyperadrenocorticism, resulting in resolution of clinical signs and a decrease in circulating concentrations of sex hormones.13,18,19 Medical treatment does not appear to have a clinically important effect on the size of the developing adrenal tumor. Surgical treatment, on the other hand, offers the potential for a complete cure, although it does not prevent the development of a new tumor in the remaining adrenal gland. Surgery also provides the opportunity to identify and possibly correct concurrent disease.6,7,12,19–21

Technically in ferrets, it is easier to remove the left adrenal gland than the right adrenal gland because it is situated farther from the CVC and the associated renal vessels. A diseased left adrenal gland rarely becomes adhered to the CVC. The right adrenal gland is typically situated close to the CVC. As hyperadrenocorticism progresses, the right adrenal gland can become tightly adhered to the CVC, engulfing or invading the vessel.22 Complete resection of the right adrenal gland and its associated mass can be achieved by temporarily crossclamping the CVC to stop the flow of blood while the gland is dissected free of the CVC.23 Any damage to the CVC can be repaired before blood flow is reestablished. Alternatively, permanent ligation of the CVC with complete resection of the adrenal gland as well as the affected segment of the CVC has been described, although this approach raises some concern about decreasing venous return to the heart.24,25 The CVC ligation method is considered faster and easier to perform.

A technique involving use of a 5-mm ameroidring constrictor to gradually occlude the CVC has also been described.26 By that technique, a second surgery is performed 1 to 3 months after ring placement for en bloc removal of the CVC and the associated adrenal gland and caudate process of the liver. The purpose of the ring-occlusion technique is to encourage development of collateral circulation, resulting in fewer adverse effects and a lower risk of death after the CVC is ligated than when collateral circulation is not established. However, the casein in the ring stimulates formation of excessive granulation tissue that complicates the second surgery. Indeed, 2 of 9 ferrets in which the technique was scientifically evaluated26 died as a result of invasion into the liver by the adrenal tumor or inflammatory tissue.a

Results of previous studies27–31 indicate that ligation of the CVC at the level of the right adrenal gland increases the risk of death due to renal failure because the CVC is ligated cranial to the renal veins. In humans and dogs, CVC ligation between the right renal vein and the liver results in death for approximately 25% of patients.32–36 The reason 75% survive and 25% do not remains unknown. The most common adverse effects in humans are marked edema of the legs and formation of a plexus of enlarged and varicose veins over the abdomen, flanks, and lumbar region.27 The edema reportedly resolves as additional collateral vessels develop. Pain is an inconsistent finding that is usually lumbar or abdominal in origin. Anecdotal reports26 suggest a similar mortality rate in ferrets, with about 30% dying within 72 hours after ligation of the CVC cranial to the right renal vein. Some ferrets develop hind limb edema, ascites, azotemia, and swollen kidneys believed to be secondary to venous congestion.7

The purpose of the study reported here was to determine whether healthy ferrets could survive temporary occlusion of the CVC, the nature of any blood flow through collateral vessels, and the pressure in the CVC caudal to the site of the occlusion. We anticipated that healthy ferrets would develop collateral circulation similar to that reported for humans and dogs. We were also interested in whether patterns of collateral circulation that developed as a result of CVC occlusion would appear different between male and female ferrets.

Materials and Methods

Animals

Eight adult purpose-bred fitch ferrets (4 castrated males and 4 spayed females) were used in the study. Each was > 20 weeks of age. Males weighed a mean of 1,235 g (range, 1,120 to 1,370 g), and females weighed a mean of 790.5 g (range, 755 to 820 g). Ferrets were housed individually and fed a commercial ferret diet. They were allowed time to acclimate to the laboratory environment before the study began. Food was withheld for at least 12 hours before the experimental procedure. Prior to induction of anesthesia for the procedure, each ferret was given a complete physical examination, and findings confirmed each was healthy. The study protocol was reviewed and approved by the University of Pennsylvania Institutional Animal Care and Use Committee.

Procedures

Surgical occlusion of the CVC was performed for the 4 male ferrets on day 1 and for the 4 female ferrets on day 2. For the procedure, ferrets were moved to the special procedures room at the Matthew J. Ryan Veterinary Hospital at the University of Pennsylvania. Each ferret was placed in an anesthetic induction chamber, and anesthesia was induced with 5% isoflurane in 4 L of O2/min. Once anesthetized, ferrets were removed from the induction chamber and positioned in dorsal recumbency on a forced warm-air unit.b Anesthesia was maintained with isoflurane in O2 by face mask until ferrets were sufficiently anesthetized to allow endotracheal intubation. An endotracheal tube with an internal diameter of 2.5 mm was used for male ferrets, and one with an internal diameter of 2.0 mm was used for female ferrets. After intubation, the endotracheal tube was connected to a nonrebreathing anesthetic system, and anesthesia was maintained with 1.5% to 2.5% isoflurane in 0.5 L of O2/min.

A 24-gauge catheter was placed in a cephalic vein to allow for administration of lactated Ringer solution to each ferret at a rate of 10 mL/kg/h via an infusion pump. Cefazolin sodium was administered IV once at a dose of 22 mg/kg. Heart rate was monitored by means of an esophageal stethoscope as well as a Doppler ultrasonographic probe placed on the ventral aspect of the tail. A No. 1 blood pressure cuff was positioned on the tail proximal to the Doppler probe to allow for indirect measurement of arterial blood pressure by use of a sphygmomanometer. A pulse oximeter probe was placed on a digital pad of a hind foot to determine the Spo2. Electrical activity of the heart was monitored with a 3-limb lead ECG; the lead II tracing was recorded every 5 minutes. Systolic arterial blood pressure, heart rate, and respiratory rate were recorded every 5 minutes during the procedure.

In preparation for the procedure, the ventral and lateral aspects of the neck of each ferret were clipped of hair and aseptically prepared. The neck was draped, and a 2- to 4-mm skin incision was made with a No. 11 scalpel blade over the right or left jugular vein to facilitate placement of a catheter. By necessity, the skin incision was longer in female ferrets than in males because the jugular vein was more difficult to identify. Access to the external jugular vein was obtained by use of a 20-gauge shielded peripheral venous catheter.c A 0.46-mm guidewire was advanced through the right atrium into the CVC under fluoroscopic guidance. The 0.46-mm guidewire was changed to a 0.89-mm guidewired by means of a transitional dilator.e A 6F vascular sheathf was placed over the wire and secured. A 5.3F over-the-wire balloon occlusion catheterg was then advanced under fluoroscopic guidance into the CVC. The balloon occlusion catheter was positioned with its tip cranial to both renal veins near the right phrenicoabdominal vein. Baseline CVC pressure was measured by use of a water manometer calibrated to 55 cm H2O.

The balloon was subsequently inflated and a venogram was performed by use of 66% (wt/vol) diatrizoate meglumine and 10% (wt/vol) diatrizoate sodiumh diluted with saline (0.9% NaCl) solution to achieve a 10% solution to assure complete occlusion of the CVC. The catheter was connected to the water manometer for continuous measurement of CVC pressure. Measurements were then recorded 30 seconds and 1, 2, 3, 4, 5, 10, 15, and 20 minutes after balloon inflation. Venography was performed 5 minutes and 15 minutes after balloon inflation. Images were recorded by use of a digital fluoroscopy systemi at a rate of 2 frames/s for 10 seconds. Images were all reviewed by the same radiologist (ALZ), with digital subtraction available to improve evaluation when necessary.

Twenty minutes after the balloon was originally inflated, it was deflated. Blood samples (1 mL) were collected from the jugular catheter, and the catheter was removed along with the vascular sheath. Hemostasis at the puncture site was achieved in male ferrets with a combination of digital pressure and application of a neck bandage. For female ferrets, 3–0 nylon suture material was used to close the stab incision in the skin. Total duration of anesthesia and administered volumes of lactated Ringer solution and contrast medium for each ferret were recorded.

Blood samples collected at the end of the procedure were used to perform a CBC and plasma biochemical analysis by use of an in-house analyzer.j Urine samples were collected via cystocentesis after the procedure if a urinary bladder could be palpated and submitted for urinalysis. The CBC and plasma biochemical analysis were repeated 2 days after the procedure for female ferrets and 3 days after the procedure for male ferrets. Plasma biochemical analyses were performed in triplicate each time. Urine sample collection for urinalysis was also performed on days 2 or 3 when possible.

After ferrets recovered from anesthesia, they were observed by the animal care staff of University Laboratory Animal Resources at the University of Pennsylvania for evidence of abdominal distention or hind limb edema. Appetite and attitude were noted. Daily physical examinations were performed on the ferrets by at least 1 investigator until the time of their adoption. All ferrets appeared healthy and were adopted within 1 week after completion of the study.

Statistical analysis

Data were assessed for normal distribution by means of the Shapiro-Wilk test. Results are summarized as mean ± SD.

Results

Animals

All 8 ferrets survived the procedure. Mean ± SD total duration of anesthesia was 92.8 ± 27.1 minutes. Mean total volume of lactated Ringer solution administered was 10.3 ± 2.7 mL/kg, and mean total volume of contrast medium administered was 8.6 ± 3.5 mL/kg. Perioperative complications were encountered for all except 1 ferret (ferret 7).

Results of CBC and plasma biochemical analysis performed on blood samples collected immediately after and 2 (females) or 3 (males) days after CVC occlusion were generally within reference limits (Table 1). One exception was mildly high plasma ALT activity (671 U/L), which was identified 3 days after the procedure in 1 male ferret (ferret 1). A mild increase above the upper reference limit was identified for plasma BUN concentration in 2 ferrets (ferrets 4 and 5) and for plasma creatinine concentration in 1 ferret (ferret 2) 2 or 3 days after the procedure. In addition, hypoalbuminemia was identified in blood samples collected immediately after CVC occlusion. Blood samples were collected from 4 ferrets (ferrets 1, 2, 5, and 8) after a minimum of 90 minutes of anesthesia, yielding PCV values that were 15.5% to 21.6% lower than values measured 2 or 3 days later.

Table 1—

Mean ± SD CBC and plasma biochemical values for 8 ferrets immediately after and 2 (4 females) and 3 (4 males) days after temporary (20-minute) occlusion of the CVC with a balloon catheter.

VariableReference limits45,46Immediately after2 to 3 days after
BUN (mg/dL)10–3826.6 ± 3.733.5 ± 7.6
Creatinine (mg/dL)0.2–0.70.51 ± 0.160.53 ± 0.17
Albumin (mg/dL)1.9–3.81.5 ± 0.53.0 ± 0.2
PCV (%)48–5933.0 ± 7.052.9 ± 4.3
Alkaline phosphataste (U/L)8–7232.8 ± 16.741.9 ± 17.4
ALT (U/L)65–346216.6 ± 115.3321.1 ± 181.4
Total bilirubin(mg/dL)0.3–0.60.3 ± 00.3 ± 0
Calcium (mg/dL)8.0–10.47.8 ± 0.610.0 ± 0.4
Phosphorus (mg/dL)3.6–7.37.3 ± 1.35.7 ± 0.8
Potassium (mg/dL)4.1–5.55.7 ± 0.55.2 ± 0.4

Urinalysis was performed for 1 male and 2 female ferrets immediately after CVC occlusion and for 1 female and 1 male ferret 2 and 3 days later, respectively. No renal tubular casts were detected in any urine specimen, and urine specific gravity was within reference limits for all 5 specimens.

CVC pressure

Mean baseline CVC pressure (measured before balloon inflation) was 5.4 cm H2O (range, < 3.0 to 8.5 cm H2O). During occlusion, 6 ferrets had a moderate increase in pressure (mean pressure, 24.3 cm H2O) and 2 ferrets (ferrets 1 and 6) had a marked increase in pressure (mean pressure, > 55.0 cm H2O). The marked increase was first identified in ferret 1 at 10 minutes after CVC occlusion and remained until balloon deflation at 20 minutes; that identified in ferret 6 occurred within 2 minutes after CVC occlusion and did not begin to decrease until the 15-minute measurement point.

Systolic arterial blood pressure

Mean systolic arterial blood pressure at baseline for all 8 ferrets was 80.0 ± 22.2 mm Hg. Thirty seconds after CVC occlusion, systolic arterial blood pressure was greater than at baseline for only 2 ferrets (ferret 1, 70 mm Hg at baseline and 105 mm Hg at 30 seconds; ferret 3, 75 mm Hg at baseline and 90 mm Hg at 30 seconds). For ferret 1, values did not return to baseline until the balloon was deflated 20 minutes later. For ferret 3, values were not recorded between 30 seconds and 15 minutes after CVC occlusion because of equipment malfunction; however, systolic arterial blood pressure was lower than at baseline (ie, to 50 mm Hg) by 15 minutes after CVC occlusion.

Collateral vessels

Vessels identified during venography included the cranial and caudal venae cavae, phrenicoabdominal veins, renal veins, left gonadal vein, circumflex iliac veins, lumbar veins, paravertebral venous plexuses, and azygos vein. All ferrets had blood flow diverted from the occluded CVC through the lumbar veins to the paravertebral venous plexuses to the azygos vein and finally into the cranial vena cava (Figures 1–4).

Figure 1—
Figure 1—

Representative lateral radiographic view of a male ferret in which digital subtraction angiography was used, revealing the location of a balloon catheter used to temporarily occlude the CVC, collateral blood flow caused by the occlusion, and extravasation of contrast medium.

Citation: American Journal of Veterinary Research 77, 5; 10.2460/ajvr.77.5.540

Figure 2—
Figure 2—

Representative ventrodorsal radiographic view of the same ferret as in Figure 1, obtained with the same imaging method.

Citation: American Journal of Veterinary Research 77, 5; 10.2460/ajvr.77.5.540

Figure 3—
Figure 3—

Representative lateral radiographic view of a female ferret in which digital subtraction angiography was used, revealing the location of a balloon catheter used to temporarily occlude the CVC and collateral blood flow caused by the occlusion.

Citation: American Journal of Veterinary Research 77, 5; 10.2460/ajvr.77.5.540

Figure 4—
Figure 4—

Representative ventrodorsal radiographic view of the same ferret as in Figure 3, obtained with the same imaging method.

Citation: American Journal of Veterinary Research 77, 5; 10.2460/ajvr.77.5.540

Individual ferret responses

Atrial and ventricular premature contractions were detected in 5 ferrets (ferrets 1, 2, 3, 4, and 8) during passage of the guidewire from the jugular vein through the right atrium into the CVC. Two ferrets (ferrets 6 and 8) developed bradycardia following initial injection of the contrast medium that was used to confirm complete occlusion of the CVC with the balloon catheter. In ferret 6, heart rate decreased from 220 to 70 beats/min and Spo2 decreased from 100% to 72%. Atropine (0.02 mg/kg, IV) was administered to that ferret twice before its heart rate and Spo2 returned to within reference limits. In ferret 8, heart rate decreased from 250 to 75 beats/min and the Spo2 decreased from 98% to 70%. Atropine (0.02 mg/kg, IV) was administered twice to that ferret with little effect. Its heart appeared to be contracting weakly when visualized via fluoroscopy. Epinephrine (0.05 mg/kg, IV) was then administered, after which heart rate increased to 300 beats/min. The Spo2 increased to 100% and heart rate returned to within reference limits within 15 minutes after epinephrine administration. No additional cardiac abnormalities were detected in either ferret for the remainder of the study.

Two ferrets (ferrets 1 and 5) had damage to their vasculature that resulted in extravasation of contrast medium into the retroperitoneal space during performance of venography (Figures 1 and 2). No changes in measured variables occurred in response to contrast medium leakage.

One ferret (ferret 8) had a seizure during recovery from anesthesia. Its blood glucose concentration at the time was 172 mg/dL, and diazepam (0.05 mg/kg, IV) administration was effective in controlling the seizure. This ferret had additional seizures 30, 90, and 120 minutes after the first one. To manage those seizures, diazepam was administered IV at doses of 0.05 mg/kg, 0.05 mg/kg, and 0.03 mg/kg, respectively. Seizures stopped, and by 9 hours after study completion, ferret 8 was alert and eating and drinking.

Discussion

Collateral vessels were identified via angiography in all ferrets of the present study, in which the CVC was temporarily occluded with a balloon catheter. A marked increase in CVC pressure was identified after occlusion of the vessel in 1 male (ferret 1) and 1 female (ferret 6). Systolic arterial blood pressure also increased in the male ferret only. A mild increase in plasma ALT activity was identified for that male ferret 3 days after the procedure. All other CBC and plasma biochemical values measured 2 or 3 days after CVC occlusion were within reference limits.

In a previous study37 involving dogs, extent of collateral circulation was evaluated after gradual occlusion (over a 2-week period) of the CVC cranial to the renal veins. Venograms were performed every 3 weeks, and dogs were euthanized 6 weeks after placement of the CVC occlusion device. Investigators found no evidence of hind limb weakness, edema, or pain in any dog throughout the study. Overall glomerular filtration rate did not change. Results of plasma biochemical analyses remained within reference limits. Gross necroscopic findings were consistent with those obtained via venography. Extensive formation of collateral vessels was identified, extending from the CVC, renal capsules, and iliac veins to the lumbar veins, vertebral veins, and azygos vein. Investigators in that study37 concluded that gradual occlusion of the CVC in dogs may allow safe removal of adrenal gland tumors with vascular invasion.

With the exception of the atrial and ventricular premature contractions observed in 5 ferrets during passage of the guidewire into the CVC in the present study, all complications appeared to coincide with injection of contrast medium. Intravenous injection of ionic contrast medium, such as that used in the present study, can cause bradyarrhythmia.38 Nephrotoxic effects have also been identified with the use of these agents.39,40 Use of contrast medium containing diatrizoate can cause significant decreases in potassium, ATP, and total adenine nucleotide content in cells of the renal proximal tubules. Significant decreases in both basal and uncoupled tubule respiratory rates and significant increases in the tubule content of calcium have been reported. The amount of erythrocyte deformation is reportedly reduced when high-osmolality contrast medium is used. Such medium can augment blood viscosity, potentially resulting in hypoperfusion of the kidneys. Renal medullary hypoxemia may increase the susceptibility of the kidneys to the toxic effects of contrast medium. Studies39,40 have shown that diatrizoate adds to the degree of renal tubule cell injury induced by hypoxemia.

Nephrotoxicity induced by IV injection of high-osmolality contrast medium can be identified by a subclinical increase in serum creatinine concentration within 24 to 72 hours after contrast angiography.39 In the present study, CBC and plasma biochemical findings in ferrets immediately following CVC occlusion were compared with those measured 2 or 3 days later, revealing mild increases in plasma BUN concentration in 2 ferrets (ferrets 4 and 5) and in plasma creatinine concentration in 1 ferret (ferret 2). Although not as sensitive nor as specific as a change in blood values, the presence of tubular casts in urine samples can be used to identify nephrotoxic effects. In the present study, urine samples collected from 3 ferrets 2 or 3 days after CVC occlusion contained no casts.

Another concern when performing angiographic evaluations involving ionic contrast medium is the potential for inducing seizures. In a study41 involving 10 adult mixed-breed dogs that received injection of 60% (wt/vol) meglumine diatrizoate into the lumbar arteries, 2 dogs had spontaneous seizures and 6 had induced seizures. Induced seizures were precipitated by clamping the skin of a hind limb with hemostats. Investigators in that study41 concluded that the seizure threshold had been lowered to a point at which even minor stimuli could result in massive neuronal discharge. In the present study, a solution containing 10% contrast medium was used to minimize the risk of adverse effects. The seizures identified in 1 ferret (ferret 8) might have been caused by the large volume of contrast medium given in relation to its body weight. In this ferret, several small-volume boluses of contrast agent were required to confirm correct placement of the balloon catheter. This resulted in a dose of contrast medium (15.9 mg/kg) that was twice the mean dose for the other 7 ferrets (7.6 mg/kg). In future studies involving angiography in ferrets, nonionic contrast medium may provide a safer alternative to ionic medium.38

We chose to administer antimicrobials preoperatively in the present study despite aseptic preparation of the catheter insertion site. The CVC occlusion procedure was not performed in a sterile surgical suite but rather in the special procedures room, and the risk of contamination was increased by the passage of various guidewires and repeated manipulations of the balloon catheter. At the time of adoption, all ferrets were healthy with no evidence of catheter site infection.

Blood samples collected immediately after the procedure and those collected 2 or 3 days later were used to compare PCV between anesthetized and conscious ferrets. In a previous study42 involving ferrets, a 30% decrease in PCV was identified after just 15 minutes of inhalation anesthesia. Packed cell volumes in that study returned to near baseline after 90 minutes of anesthesia. The lower viscosity of circulating blood is an important consideration in that it may increase flow through existing collateral vessels. In the present study, PCV would have been at its lowest point at the time of CVC occlusion. Blood samples were collected from 4 ferrets after a minimum of 90 minutes of anesthesia, at which point values were 15.5% to 21.6% lower than the values measured 2 or 3 days later, when ferrets were conscious. Total duration of anesthesia was ≤ 80 minutes for the other 4 ferrets.

Splenic sequestration may have contributed to the finding that PCV had not returned to within reference limits as previously reported. A study43 involving technetium 99m–labeled RBCs in ferrets revealed that isoflurane anesthesia caused splenic sequestration of RBCs that was partially reversed by the termination of anesthesia. Hemodilution may also explain the low PCV values in the present study. Hypoalbuminemia was likewise identified in blood samples collected immediately after CVC occlusion. Plasma albumin concentration returned to within reference limits in all ferrets 2 or 3 days following the procedure.

Results of the present study suggested that healthy ferrets possessed adequate collateral circulation to survive 20 minutes of CVC occlusion with no resultant organ dysfunction. Those healthy ferrets had lumbar vessels that diverted blood from the CVC to the paravertebral venous plexus to the azygos vein and then to the cranial vena cava. Ferrets can be used as a model for evaluating the effects of caval ligation in humans and dogs, which possess similar collateral pathways.44 No differences were apparent in collateral circulation or in response to caval occlusion between male and female ferrets. The marked increase in CVC pressure in 2 of the 8 ferrets (1 male and 1 female) following balloon occlusion suggested that an unfavorable outcome might occur in these ferrets with permanent ligation of the vessel. This suggestion would be consistent with anecdotal reports26 of a 30% mortality rate following CVC ligation in ferrets. Additional research is needed to determine whether CVC pressures caudal to the site of temporary balloon occlusion or permanent ligation of the CVC could be used to predict survival in ferrets requiring adrenalectomy.

Acknowledgments

Supported by Dr. Bennett's foundation account at the Matthew J. Ryan Veterinary Hospital, University of Pennsylvania, and client donations.

Presented in abstract form at the 14th Annual Scientific Meeting of the Society of Veterinary Soft Tissue Surgeons, Santa Barbara, Calif, May 2015; 29th Annual Conference of the Association of Avian Veterinarians and the Association of Exotic Mammal Veterinarians, Savannah, Ga, August 2008; 13th Annual Surgical Summit of the American College of Veterinary Surgeons, Washington, DC, October 2003; and 28th Annual Conference of the Society for Interventional Radiology, Salt Lake City, March 2003.

ABBREVIATIONS

CVC

Caudal vena cava

ALT

Alanine transaminase

Spo2

Oxygen saturation as measured by pulse oximetry

Footnotes

a.

Todd Driggers, Avian and Exotic Animal Clinic of Arizona, Gilbert, Ariz: Personal communication, 2015.

b.

Bair Hugger warming unit model 505, Augustine Medical Inc, Eden Prairie, Minn.

c.

BD Insyte Autoguard shielded IV catheter, Becton Dickinson, Franklin Lakes, NJ.

d.

Amplatz Super Stiff guidewire, Boston Scientific Corp, Natick, Mass.

e.

Vaxcel Mini-Stick vascular entry system, Boston Scientific Corp, Natick, Mass.

f.

Brite Tip interventional sheath, Cordis Corpo, Miami, Fla.

g.

Cook Group, Bloomington, Ind.

h.

Hypaque 76, Nycomed Inc, Princeton, NJ.

i.

GE medical system DRS3.2 with Advantx console, GE Healthcare, Waukesha, Wisc.

j.

VetScan, Abaxis Inc, Union City, Calif.

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Contributor Notes

Dr. Calicchio and Dr. Bennett's present address is Lauderdale Veterinary Specialists, 3217 NW 10th Terr, Ste 303, Fort Lauderdale, FL 33317.

Dr. Laraio's present address is Banfìeld Pet Hospital, 11183 S Parker Rd, Unit H, Parker, CO 80134.

Dr. Weisse's present address is Interventional Radiology Service, The Animal Medical Center, 510 E 62nd St, New York, NY 10065.

Dr. Zwingenberger's present address is School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

Dr. Rosenthal's present address is School of Veterinary Medicine, St. Matthew's University, Grand Cayman, British West Indies.

Dr. Johnston's present address is College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523.

Dr. Campbell's present address is Peak Veterinary Specialists and Emergency, 4650 Royal Vista Cir, Ste 100, Windsor, CO 80528.

Dr. Solomon's present address is Infiniti Medical LLC, 525 Middlefield Rd, Ste 150, Menlo Park, CA 94025.

Address correspondence to Dr. Calicchio (kcalicchio@lauderdalevets.com).