Cholecystitis is a suppurative or nonsuppurative inflammatory infiltration of the gallbladder (GB) wall.1 The condition may be associated with other hepatobiliary diseases such as cholangitis, cholangiohepatitis, cholelithiasis, and cholestasis.1–5 In dogs and cats, ultrasonographic features of cholecystitis may include gallbladder wall (GBW) thickening, echoic gallbladder luminal content (GBLC) in various amounts, pericholecystic fluid, and hyperechoic regional fat.6,7 In ferrets, 2 publications1,4 have briefly reported the ultrasonographic features of cholecystitis in a single case of emphysematous cholecystitis that led to the rupture of the GB. Reported sonographic findings included generalized subjective thickening and hyperechogenicity of the biliary tree, gas bubbles in the GB lumen, and mild peritoneal effusion. The ultrasonographic appearance of hepatobiliary diseases other than emphysematous cholecystitis has been poorly documented in ferrets and is usually presumed to be similar to those previously described in dogs and cats.1,3–5,8 Database searches (PubMed, CABI Digital Library, and Scopus) covering the years 1970 to 2024 were negative for detailed ultrasonographic descriptions of the biliary tract in healthy ferrets and ferrets with cholecystitis.
The aims of the study were to describe the clinical signs, biological anomalies, ultrasonographic findings of the hepatobiliary system, and outcome in ferrets with confirmed cholecystitis and to compare the ultrasonographic appearance of the hepatobiliary system between diseased and healthy ferrets.
Methods
This was a single-center (Centre Hospitalier Vétérinaire ADVETIA), retrospective case-control analytical observational study. The protocol included 2 phases and was approved by the Ethics Committee Jacques Bonnod of VetAgro Sup (registration no. 2279). For the retrospective phase (ferrets with cholecystitis, ie, diseased group), the use of data was approved by the hospital director, and all owners gave their consent for the use of images and medical information. For the prospective phase (healthy ferrets, ie, healthy group), client-informed consent was obtained. In both phases of the study, abdominal ultrasound examinations were performed under general anesthesia induced and maintained by inhalation of isoflurane diluted in oxygen and delivered using a face mask. Ultrasound studies were acquired using a high-definition ultrasound system from General Electric Ultrasound. Aplio 300 and Toshiba, equipped with an 8- to 11-MHz curvilinear transducer and a 13- to 18-MHz linear transducer, were used for the retrospective phase of the study. Logiq E10, equipped with a 3- to 10-MHz curvilinear transducer and a 6- to 15-MHz linear transducer, was used for the prospective phase of the study. All ultrasound images and video clips were stored in a picture archiving communication system (PACS) in DICOM format.
Two groups of ferrets were formed: a diseased group and a healthy group. Individual inclusion or exclusion in each group was decided consensually by CVB and a European College of Veterinary Diagnostic Imaging board-certified radiologist (HG) based on the inclusion and exclusion criteria defined below.
Study enrollment
Retrospective phase of the study (diseased group)
The database of Centre Hospitalier Vétérinaire ADVETIA was searched between November 2011 and November 2021 for any ferret with cholecystitis. Inclusion criteria were set as follows: (1) cholecystitis confirmed by bile culture and either bile cytology or GB pathology, (2) an ultrasound examination of the abdomen performed within 48 hours before bile sampling either under ultrasound guidance or during laparotomy, and (3) available ultrasound still images and video clips of the hepatobiliary system. Ultrasound examinations had been performed by either HG or another European College of Veterinary Diagnostic Imaging board-certified radiologist (YR). Selected diseased ferrets formed the diseased group.
Prospective phase of the study (healthy group)
Client-owned healthy ferrets that had to be anesthetized for preventive placement of an SC implant of deslorelin were recruited during the period of November 2021 to December 2022. The goal was to obtain a group size similar to that of the diseased group, being aware that the number of individuals would be limited by the duration of the recruitment process and the need for consent of owners. Inclusion criteria were set as follows: (1) no history of disease, (2) no medication over the previous 3 months including deslorelin implants, (3) normal physical examination, and (4) CBC and serum biochemistry results within reference ranges. An ultrasound examination of the cranial abdomen focused on the hepatobiliary system was performed by CVB. Ferrets were excluded if the examination showed any anomaly of the liver, biliary tract, stomach, duodenum, pancreas, abdominal lymph nodes, or peritoneal cavity. Still images and video clips of the biliary tract were recorded in each ferret.
Data recording: medical records review and follow-up
Data from the medical records were retrieved by CVB and included age, sex, body weight, physical examination findings, CBC, and serum biochemistry results in all ferrets (diseased and healthy groups). Additionally, for diseased ferrets, presenting complaint, ultrasonographic report, bile culture and cytology reports, GB pathology report, diagnosis, and treatment were recorded. The alive or dead status at the time of inclusion and, when relevant, the date and cause of death of diseased ferrets were either retrieved from medical records or sought from owners by phone call.
Abdominal ultrasonography review
In both groups, all ultrasound images and clips were reviewed and analyzed using a dedicated medical image viewer (Vue PACS, version 12.1.6; Philips) based on a consensus between CVB and HG.
Qualitative ultrasonographic variables included (1) for the GB, presence of an echoic GBLC, echogenicity of the GBLC relative to the liver parenchyma, shape and position of the echoic GBLC (amorphous or organized, gravity dependent or not), GBW thickness (normal or increased, regular or irregular), and GBW echogenicity relative to the liver parenchyma; (2) for the common bile duct (CBD), visualization of the CBD either on its proximal or its distal segment, echogenicity of the CBD content, and visualization of the CBD wall; (3) for the duodenal papilla (DP), visualization of the DP; (4) for the liver, size, contour, parenchymal echogenicity, and visualization of intrahepatic bile ducts (IHBDs); (5) for the pancreas, size, contour and parenchymal echogenicity; and (6) for the peritoneal cavity, presence of free fluid and echogenicity of the peritoneal fat.
For quantitative ultrasonographic variables, linear measurements were performed using adjustable calipers. Ultrasonographic measurements included gallbladder volume (GBV) calculated using the formula 0.52 X (length X width X height),9 maximum gallbladder wall thickness (mGBWT), maximum common bile duct diameter (mCBDD), maximum common bile duct wall thickness (mCBDWT), and DP diameter.
Statistical analysis
Data analysis was conducted in R10 (version 4.3.3; R Core Team 2024) by one of the authors (AA). Categorical data are expressed as frequencies and percentages, and continuous data are expressed as medians and ranges. The dependence between the explanatory variables (group, age, body weight, and sex) was assessed by pairwise comparisons: Fisher exact tests were used to compare 2 categorical variables (ie, sex vs group); Wilcoxon rank sum tests were used for a categorical variable against a quantitative one (ie, sex vs age, sex vs body weight, group vs age, group vs body weight); and Spearman's rank correlation tests were used for 2 quantitative variables (ie, age vs body weight). A P value of less than .05 was considered statistically significant.
Results
Study population (diseased group and healthy group)
The search of the hospital database with the words “cholecystitis” and “ferrets” included 13 ferrets. Two of these were excluded due to the absence of bile culture. The diseased group included 11 ferrets with a median age of 5 years (range, 1 to 8 years) and median body weight of 0.92 kg (range, 0.5 to 1.5 kg). Nine ferrets were male and 2 were female.
Ultrasound was performed on 15 clinically healthy ferrets. Five of these were excluded due to the presence of ultrasonographic abnormalities including a liver mass, liver cysts, pancreatic nodules, and cranial abdominal lymphadenomegaly in 2 individuals. Ten ferrets were included in the healthy group, with a median age of 3 years (range, 1 to 5 years), median body weight of 0.88 kg (range, 0.5 to 1.85 kg), and equal number of females and males.
Pairwise comparisons of the explanatory variables (group, age, body weight, and sex) revealed a dependence between sex and body weight, with males significantly heavier than females (Wilcoxon rank sum test, P < .01), and a dependence between group and age, with ferrets in the diseased group significantly older than those in the healthy group (Wilcoxon rank sum test, P < .01).
Clinical signs and blood work results in the diseased group
Clinical signs at presentation included lethargy (9/11 [82%]), dysorexia (5/11 [46%]), vomiting (5/11 [46%]), anorexia (3/11 [27%]), icterus (3/11 [27%]), weight loss (3/11 [27%]), abdominal pain (3/11 [27%]), diarrhea (1/11 [9%]), hyperthermia (1/11 [9%]), and distended abdomen (1/11 [9%]; Supplementary Material S1). Ten out of 11 ferrets had a blood biochemistry panel and CBC. Bilirubinemia was measured in 9 ferrets, and 9/9 showed hyperbilirubinemia with total bilirubin ranging from 3.4 to 299.3 μmol/L (0.2 to 17.5 mg/dL). Alkaline phosphatase was measured in 10/11 ferrets and was increased in 5/10 individuals, ranging from 156 to 525 IU/L. Alanine aminotransferase was measured in 8/11 ferrets and was increased in 5/8 individuals, ranging from 639 to 2,000 IU/L. Albumin was measured in 8/11 ferrets and was decreased in 6/8 individuals ranging from 10 to 26 g/L (1 to 2.6 g/dL). Glucose was measured in 10/11 ferrets and was decreased in 1 individual (1.27 or 22.9 mg/dL). Six out of 10 ferrets (60%) had anemia with RBC ranging from 4.9 to 7.3 X 1012/L or X 106/µL. White blood cell count was within normal limits in 10/10 diseased ferrets, ranging from 4 to 12.4 X 109/L or X 103/µL. Platelets were measured in 10/11 ferrets and were decreased in one individual (141 X 109/L or X 103/µL).
Ultrasonographic findings in the diseased and healthy groups
Considering the small size of the study population and the possible interactions between the explanatory variables (see above), no statistical comparisons between the 2 groups were made. The raw data are provided (Supplementary Material S2).
Gallbladder
In the diseased group, GBV and mGBWT could be measured in 8/11 and 11/11 ferrets, respectively. Diseased ferrets showed a greater GBV than healthy ones (median, 1.7 mL; range, 0.3 to 4.3 mL vs median, 0.8 mL; range, 0.1 to 1.8 mL) and a greater mGBWT (median, 2 mm; range, 0.8 to 6.2 mm vs median, 0.75 mm; range, 0.5 to 1.2 mm). An echoic GBLC was more common in the diseased group than in the healthy group (9/11 [82%] vs 1/10 [10%]; Figure 1). In diseased ferrets, the echoic material occupied more than 75% of the GB lumen in 6/9 (67%) ferrets and between 25% and 75% of the lumen in 3/9 (33%) cases. The material was not shadowing in any case and was gravity dependent in 5/9 ferrets. In the only healthy ferret with echoic GBLC, the material occupied less than 25% of the GB lumen; was mildly echogenic, gravity dependent, and not shadowing; and was described as benign biliary sludge.
Ultrasonographic images of the hepatobiliary system in 3 ferrets with confirmed cholecystitis (A through C) and in a healthy ferret (D). In both diseased ferrets, the gallbladder visualized in longitudinal plane (A) and in transverse plane (C) shows an echoic luminal content (asterisk) either organized (A) or unorganized (C) occupying more than 25% of the lumen and a thickened wall (arrows). In a healthy ferret (D), the gallbladder visualized in a longitudinal plane shows an anechoic lumen and a thin, barely visible wall (arrow). A dilated intrahepatic bile duct is visualized in a ferret with cholecystitis (B) with an irregular echoic wall and anechoic lumen (between calipers). IHBD = Intrahepatic bile ducr. mGBWT = Maximum gallbladder wall thickness.
Citation: American Journal of Veterinary Research 86, 1; 10.2460/ajvr.24.07.0191
Common bile duct and duodenal papilla
The CBD was visualized in 9/11 (82%) diseased ferrets and 5/10 (50%) healthy ferrets. The CBD wall was visualized in 6/11 (55%) diseased ferrets and 4/10 (40%) healthy ferrets. In the diseased group, measurement of the mCBDD was obtained in 7/9 ferrets, and measurement of the mCBDWT was obtained in 6/9. The mCBDD was higher in the diseased group than in the healthy group (median, 3.9 mm; range, 2.8 to 7 mm vs median, 1 mm; range, 0.6 to 1.8 mm; Figure 2), as well as the mCBDWT (median, 1 mm; range, 0.7 to 2.1 mm vs median, 0.35 mm; range, 0.2 to 0.4 mm). The DP was visualized in 5/11 (45%) diseased ferrets and 4/10 (40%) healthy ferrets. The DP diameter in the diseased group was very close to that measured in the healthy group (median, 2.1 mm; range, 1.2 to 3 mm vs median, 2.5 mm; range, 2 to 2.9 mm).
Ultrasonographic images of the common bile duct in 2 ferrets with confirmed cholecystitis (A and C) and 2 healthy ferrets (B and D). The common bile duct (CBD) visualized in longitudinal plane in a diseased ferret (A; asterisk and between calipers) is dilated compared to the CBD in a healthy ferret (B; asterisk and between calipers). The CBD visualized in transverse plane in a diseased ferret (C) shows a thickened wall (arrow) compared with the CBD visualized in longitudinal plane in a healthy ferret (D), which shows a thin wall (between arrows). mCBDD = Maximum common bile duct diameter. mCBDWT = Maximum common bile duct wall thickness.
Citation: American Journal of Veterinary Research 86, 1; 10.2460/ajvr.24.07.0191
Intrahepatic bile ducts
The IHBDs were visualized in 5/11 (46%) diseased ferrets (Figure 1) and in none of the healthy ferrets (0/10).
Additional ultrasonographic findings in the diseased group
Liver size was assessed in all diseased ferrets and considered enlarged in 4/11 (36%) and normal in the remaining 7 individuals. The liver parenchyma was hypoechoic and homogenous in 3/11 (27%) ferrets and normoechoic in the remaining individuals.
Hepatic lymph nodes were the most frequently identified regional lymph nodes (9/11 [82%]) and were subjectively described as enlarged in 6/9 (67%) ferrets with a thickness ranging from 4.6 to 8 mm. Hepatic lymph nodes were reported as mildly hypoechoic to peritoneal fat in 8/9 ferrets and normoechoic in the remaining individual.
Peritoneal anomalies were noticed in 5/11 (46%) ferrets. In 4/11 (36%), a mild amount of free anechoic peritoneal fluid was observed that was located adjacent to the GB in 2/4 (50%) ferrets. In 3/11 (27%) individuals, the retrohepatic fat was hyperechoic.
Bacteriological, cytological, and histopathological results in the diseased group
Bile culture was performed in all ferrets with cholecystitis. The most commonly isolated bacteria was E coli (8/11 [73%]). Chryseobacterium indologenes was isolated in 1 ferret, and Flavobacterium meningosepticum was isolated in another ferret. Bile culture was negative in the remaining individual ferret. Bile cytology was performed in 7/11 ferrets, with a diagnosis of septic purulent cholecystitis in all 7 individuals. In the 2 ferrets that underwent cholecystectomy, the histopathological report indicated a fibronecrotizing suppurative and chronic hyperplastic cholecystitis, including the only ferret in which bile culture was negative.
Treatment response and outcome
All diseased ferrets were treated with antibiotics according to sensitivity test results when available. The 8 ferrets with E coli isolated from their bile were prescribed antibiotics, which included β-lactams in 2 ferrets (amoxicillin-clavulanic acid), fluoroquinolones in 5 (marbofloxacin and enrofloxacin), and imidazoles in 1 (metronidazole). Chryseobacterium indologenes was treated with fluoroquinolones, and F meningosepticum was treated with macrolides and rifamycins (clarithromycin and rifabutin). The ferret with a negative bile culture but evidence of fibronecrotizing suppurative cholecystitis on GB pathology was treated with fluoroquinolones; this is the only individual still alive at the time of writing.
Follow-up information was obtained in 10/11 ferrets. Three out of 10 (30%) ferrets did not show any clinical improvement and died at 7, 10, and 54 weeks after initial presentation. Seven out of 10 (70%) ferrets showed remission of clinical signs and normalization of hematobiochemical results within 3 weeks of treatment. Among these, 1 was still alive and doing well at the time of writing (95 weeks from initial presentation); 5 relapsed and died at 6,15, 36, 40, and 104 weeks after initial presentation; and 1 was lost for follow-up after initial remission. Owners declined necropsy in all deceased ferrets. In summary, among the 9 diseased ferrets with an available long-term follow-up, survival time ranged from 6 to 104 weeks, with a median of 36 weeks (1 ferret was still alive at the time of writing with a minimal survival time of 95 weeks). The 2 ferrets undergoing cholecystectomy had the longest survival time (≥ 95 and 104 weeks).
Discussion
Ferrets with hepatobiliary disease usually show unspecific clinical signs that rarely include icterus.4 Blood analyses are therefore useful screening tools for suspecting the condition.4 Increased bilirubinemia has been reported to occur very rarely in ferrets with hepatobiliary disease, possibly due to rapid renal excretion of bilirubin that would compensate for a decreased hepatic clearance.4,7 This information is not consonant with the results of the current study as 9/9 (100%) ferrets with cholecystitis and available bilirubinemia measurement showed hyperbilirubinemia and 3/11 (27%) diseased ferrets were icteric. Hyperbilirubinemia in diseased ferrets suggests the presence of a concurrent hepatobiliary disorder, as the inflammation of the GB wall is not expected to induce hyperbilirubinemia by itself. The occurrence of another biliary disease concurrently to cholecystitis has been suggested in ferrets, such as cholangitis, cholangiohepatitis, cholestasis, or cholelithiasis.3 In dogs and cats, causes of hepatic or posthepatic hyperbilirubinemia include hepatic inflammation (hepatitic and cholangiohepatitis), hepatic neoplastic infiltration, and any disorder resulting in an extrahepatic biliary obstruction (EHBO).11 In the present study, no diseased ferret had a lesion with the potential of EHBO found on ultrasound (0/11) or during surgery (0/2). In addition, 3/11 diseased individuals showed a hypoechoic liver, and IHBDs were visualized in 5/11 ferrets with cholecystitis while none of the healthy ones showed visible IHBDs. These results suggest that, in ferrets with cholecystitis, a hypoechoic liver and visible IHBDs in the absence of a lesion potentially obstructing the CBD may represent ultrasonographic signs of cholangitis, similarly to what has been reported in cats.9,12,13 Unfortunately, none of the diseased ferrets had their liver sampled for cytological or pathological evaluation, preventing confirmation of this hypothesis.
In the current study, the CBD lumen was larger in diseased ferrets (mCBDD ≥ 2.8 mm), compared with healthy individuals (mCBDD ≤ 1.8 mm), with no mCBDD values overlap between the 2 groups. A dilated CBD has been reported as one of the most frequent ultrasonographic findings (9/26 [35%]) in dogs with bacterial cholecystitis and/or cholangitis.14 In the current study, a dilated CBD was observed in ferrets with cholecystitis at a higher rate (7/11 [64%]) than in dogs.14 However, the specificity of this finding remains to be established in ferrets.
The GB wall was thicker in diseased than in healthy ferrets with a narrow overlap of mGBWT values between the 2 groups. In the only ferret previously reported with cholecystitis and abdominal ultrasonography, a thickening of the GB wall was described with no measurement reported.1 In the 3 ferrets reported with EHBO and abdominal ultrasonography,5,8 a GB wall thickening with a wall thickness of 3 mm was described in 2/3 ferrets despite a sterile bile. The comparison of this information from the literature with the results of the current study suggests that a GB wall thickening may not be a specific sign of cholecystitis, as previously reported in dogs and cats.1,3,15
A nonshadowing echoic material within the GB lumen was much more common in diseased than in healthy ferrets suggesting that this finding could be a key ultrasonographic feature of cholecystitis in ferrets. In the only healthy ferret with echoic content, the material occupied less than 25% of the GB lumen, was gravity dependent, and was described as benign biliary sludge. Our results suggest that GB sludge might be uncommon in healthy ferrets compared with healthy dogs (10% in the current study vs 55% to 58% in dogs).16,17 Gallbladder sludge has been reported to be common in dogs and cats undergoing abdominal ultrasound for various reasons.18–21 In ferrets, the prevalence of an echoic material within the GB in hepatobiliary diseases other than cholecystitis and in gastrointestinal diseases remains to be determined.
The GB volume in diseased ferrets was larger than in healthy ones but with a wide overlap of GB volume values between the 2 groups, suggesting that this parameter would be poorly discriminatory between the 2 groups. This result is consistent with ultrasonographic observations in cats with spontaneous EHBO, suggesting that the volume of the GB might be affected by factors other than an obstructive process such as compliance of the GB wall and elasticity of the surrounding liver parenchyma.12
In the current study, the most commonly isolated bacteria in the bile of ferrets with cholecystitis was E coli (8/11 [73%’). This result is comparable to those previously reported in dogs and cats.22,23 Ascending GB infection from the gastrointestinal tract via the biliary tree is considered to be the most common route in dogs and cats and, by extension, in ferrets.1,24 Although in the current study the diseased group was small, the high rate of isolated enteric bacteria did not contradict this hypothesis.
Cholecystectomy has been reported to be successfully performed in ferrets.2,25 In the current study, the 2 ferrets having undergone cholecystectomy showed the longest survival times (≥ 95 and 104 weeks). In cats and dogs, reported perioperative mortality rates of nonelective cholecystectomy are relatively high (22% and 20%, respectively),26,27 and a much lower mortality rate has been reported in dogs undergoing elective cholecystectomy (2%).27 The perioperative mortality rate of cholecystectomy in ferrets with cholecystitis is currently unknown, and the benefit of an elective cholecystectomy at an early stage of cholecystitis remains to be determined in this species.
The ultrasound examinations in this study were performed under general anesthesia using isoflurane as the inhalation agent. Historically, direct face mask induction with isoflurane has been widely employed by exotic mammal practitioners due to its broader margin of flexibility and clear practical advantages.28 However, it is now widely recognized that this technique can lead to some undesirable and uncontrolled side effects such as apnea and hypotension, particularly when used at high concentrations.28 On the other hand, a multimodal anesthetic approach including appropriate premedication and a smooth, gentle induction can significantly reduce these risks, improving patient safety and survival.28 Therefore, adopting this approach is essential for modern ferret anesthesia and is the method recommended for anesthetizing ferrets in future studies.
This study has several limitations. An important one was the small size of each group, which prevented performing a legitimate and relevant statistical comparison between the 2 groups, particularly for ultrasonographic data. Other variables besides health status (eg, age, body weight, and sex) may have influenced the results in this small-scale cross-sectional study. Consequently, the conclusions of the current study should be taken with caution and required to be confirmed by further studies conducted on larger cohorts.
The retrospective design of the study was also an important limitation as all ultrasonographic variables could not be evaluated in all diseased ferrets, further reducing the number of data available for analysis. Further studies should ideally have a prospective design and include thorough ultrasonographic examinations including the search of the CBD with measurements of the lumen diameter and wall thickness as often as possible.
A final limitation of the current study is the absence of a surgical approach to rule out an EHBO in most ferrets with cholecystitis. Extrahepatic biliary obstruction was ruled out in the 2/11 individuals who were managed surgically. In the remaining 9, a surgical approach was not performed as the condition was managed with medical treatment, and CBD catheterization would have been ethically unacceptable.
In conclusion, this is the first study describing the clinical signs, biological anomalies, ultrasonographic findings, and outcomes after treatment in a series of domestic ferrets diagnosed with cholecystitis. Diseased ferrets presented with nonspecific clinical signs and most showed hyperbilirubinemia. Compared with healthy individuals, diseased ferrets showed on ultrasound a larger CBD, a thicker CBD wall, a thicker GBW, a more frequent and more abundant GB sludge, visible IHBD, and a larger GB. The presence of one or more of these features in a domestic ferret should prompt further investigation including ultrasound-guided cholecystocentesis for bile cytological and bacteriological analyses. The accuracy of these ultrasonographic variables as indicators of cholecystitis in ferrets remains to be determined in further studies on larger cohorts. The most commonly isolated bacteria in bile was E coli. Survival time ranged from 6 to 104 weeks with a median of 36 weeks.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
The authors thank technicians and clinical staff of the Department of Exotics, Centre Hospitalier Vétérinaire ADVETIA, for their assistance with image acquisition and also the referring veterinarians and owners of the ferrets included in this study.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose.
ORCID
C. V. Basse https://orcid.org/0000-0003-3724-9777
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