Abstract
Objective
To describe the use of laparoscopic ultrasound (LUS) for evaluation of the liver in dogs with clinical liver disease and to compare the findings of LUS to transabdominal ultrasound (TUS).
Methods
8 client-owned dogs presenting for laparoscopic liver biopsies due to clinical liver disease were enrolled. All dogs underwent TUS, and liver lesions were identified, localized, and quantified per presumed liver lobe. Laparoscopic examination and LUS of the liver were performed, and liver lesions were identified, localized, and quantified. Laparoscopic liver biopsies were obtained and submitted for histopathological analysis, copper analysis, and culture and susceptibility.
Results
The median time to perform hepatobiliary TUS was 10 minutes (IQR, 7.5 to 12 minutes), and the median time to perform LUS and laparoscopic examination of the liver was 19.5 minutes (IQR, 17.8 to 23.5 minutes). The number of lesions identified on LUS versus TUS was significantly different, with 5 dogs having an additional 28 lesions identified on LUS that were not found on TUS. The diameter of lesions identified on TUS and LUS ranged from 0.3 to 4.5 cm and 0.1 to 4.1 cm, respectively. In 2 dogs, LUS was used to guide the biopsy of liver lesions that were not grossly appreciable on laparoscopic examination.
Conclusions
LUS identifies more liver lesions compared to TUS and can be used to guide the biopsy of lesions that are not grossly appreciable laparoscopically.
Clinical Relevance
LUS should be considered when staging patients with hepatobiliary neoplasia and may result in the identification of additional liver lesions missed on preoperative imaging.
Transabdominal ultrasound (TUS) and CT are the most common imaging modalities used for the diagnosis and staging of liver disease in dogs. Prior studies1,2 have shown that both CT and TUS have limitations in the localization of hepatic lesions, with the accuracy of localization ranging from 51.8% to 84%. These findings indicate that common preoperative imaging modalities may not always be reliable for diagnosis and surgical planning.
In people, laparoscopic ultrasound (LUS) is used frequently in both the diagnosis of hepatic disease as well as to guide laparoscopic surgery of the liver. Prior studies3–6 have shown that significant disparity exists between preoperative imaging and findings at the time surgery and that LUS is superior for identifying liver lesions compared to TUS, CT, and MRI. In one study,4 LUS detected new malignant hepatic lesions in 22% of patients that had previously undergone TUS and CT, resulting in an altered surgical plan in 80% of these patients.
Hepatocellular carcinoma is the most common type of primary neoplasia of the liver in dogs, with metastatic neoplasia to the liver being the most common overall.7,8 Preoperative staging is critical to evaluate for multifocal or diffuse forms of hepatic neoplasia or metastatic disease as this significantly alters treatment options and prognosis.7,8 Additionally, accurate localization of liver tumors is important in surgical planning and approach as well as determining resectability.
In a prior study,9 LUS of the liver was shown to be feasible and safe in healthy dogs without liver disease. While access to the right division of the liver was challenging in some cases, all liver lobes were able to be accessed in the majority of dogs.9 Another case report10 described the use of LUS to successfully guide microwave ablation of a liver tumor in a dog. Based on these findings, LUS of the liver appears to be a safe, adjunctive diagnostic and treatment-guiding modality for the liver in dogs.
The aim of this study was to describe the use of LUS in dogs with clinical liver disease and to compare the number of liver lesions identified on LUS to preoperative TUS. A secondary objective was to describe the use of LUS to guide laparoscopic liver biopsies in dogs with lesions visualized ultrasonographically that were not observed on laparoscopic examination.
Methods
Ethics
This study was approved by the University of Florida IACUC and the Small Animal Hospital Board at the University of Florida (IACUC #202200000149). Written informed consent was also obtained from all pet owners prior to study participation.
Case selection
Eight dogs presenting to the University of Florida Soft Tissue Surgery Service for laparoscopic liver biopsy due to previously diagnosed clinical liver disease were prospectively enrolled from March 1, 2023, through June 1, 2024. Liver enzyme elevations (ALT, ALP, and GGT) and/or the prior discovery of liver lesions on TUS were considered criteria for clinical liver disease. Dogs were excluded if they were considered poor candidates for laparoscopic surgery (active liver failure, clinical evidence of portal hypertension, ascites, severe thrombocytopenia, etc). All dogs underwent a complete general physical examination, CBC, biochemistry panel, and coagulation panel (prothrombin time and activated prothrombin time) prior to TUS, anesthesia, and surgery.
Transabdominal ultrasound
All dogs were sedated with 0.2 mg/kg butorphanol, IV, as well as 5 μg/kg dexmedetomidine, IV, if indicated and safe as determined by the overseeing veterinary clinician. The dogs underwent a focused hepatobiliary TUS by a single board-certified veterinary radiologist (FVG). Ultrasound examination was performed using an ultrasound device (RS85 Prestige; Samsung Healthcare) and a 4-to-9-MHz microconvex transducer (CA4-10M Transducer; Samsung Healthcare).
During focused hepatobiliary TUS, representative still images and cine loops in longitudinal and transverse planes were obtained of the caudate process of the caudate lobe, right hepatic division, central hepatic division, left hepatic division, and gallbladder. If nodules or masses were identified within the liver, representative still images and cine loops were obtained in longitudinal and transverse planes. The total time to perform hepatobiliary TUS was recorded.
Lesions identified were then presumably localized to a liver lobe. Lesions were localized to the left lateral lobe if they were located to the left of midline, in broad contact with the cranioventral aspect of the stomach; to the left medial lobe if they were on the left close to ventral midline, in contact with the diaphragm and separated from the quadrate lobe by the falciform ligament; to the quadrate lobe if they were to the right of midline, in contact with the diaphragm and the medial aspect of the gallbladder; to the right medial lobe if they were in contact with the diaphragm and lateral aspect of the gallbladder and ventral to the duodenum; to the right lateral lobe if they were dorsal to the right medial lobe and lateral to the portal vein, in contact with the diaphragm on the lateral aspect; to the caudate process of the caudate lobe if they were in close contact to the right kidney; and to the papillary process of the caudate lobe if they were on midline, between the portal vein and caudal vena cava, and medial to the stomach. In addition, hepatic veins and portal branches were also used to determine the location of the lesions. The number of lesions per liver lobe was determined. If there were more than 5 lesions in 1 lobe, it was considered diffuse change within that lobe and recorded as > 5.
Lesions were then measured and their appearance described. In lobes where there were > 5 lesions, the smallest and largest lesions were measured and expressed as a range in size.
Laparoscopic examination and ultrasound of the liver
All dogs were anesthetized according to standard clinical protocol determined by a board-certified veterinary anesthesiologist. Following induction of general anesthesia, dogs were placed in dorsal recumbency, and their ventral abdomen was clipped and aseptically prepared. All dogs received perioperative cefazolin (22 mg/kg, IV) up to 30 minutes prior to the first incision and every 90 minutes thereafter.
Laparoscopic examination and LUS of the liver were then performed as previously described.9 All laparoscopic procedures were performed by the same board-certified veterinary surgeon (JBC). Briefly, dogs were positioned in dorsal recumbency, and a 30-mm single-incision laparoscopic surgery port (SILS Flexible Port; Medtronic) was placed on midline centered over the umbilicus in dogs ≥ 20 kg or caudal to the umbilicus in dogs < 20 kg. An additional 5-mm port was placed cranial to the single incision laparoscopic surgery port when necessary to aid in retraction and manipulation of liver lobes. The abdominal cavity was insufflated to a pressure of 8 to 10 mm Hg. A 5-mm, 30° laparoscope with a high-definition camera (Karl Storz Endoscopy-America) was placed in the port.
Laparoscopic examination of the liver and LUS were performed concurrently. Lateral rotation to the left and right was performed for improved exposure and access to the right and left divisions as previously described.9,11 Any gross abnormalities observed were recorded and described, and images and/or video clips were acquired and saved with the laparoscope. Laparoscopic ultrasound was performed using an ultrasound device (ProSound Alpha-7 Surgical Ultrasound System; Hitachi Aloka Medical) and a 13-to-5-MHz curved array laparoscopic 4-way transducer (UST-9150 4-Way Laparoscopic; Hitachi Aloka Medical). The transducer was inserted into a 15-mm cannula placed in the single incision laparoscopic surgery port, and each liver lobe was scanned by placing the transducer directly on the ventral parenchymal surface. The transducer was moved in a side-to-side manner from the hilus to the apex of each lobe. Scanning started at the left lateral lobe and ended with the caudate lobe. Representative images and cine loops of the hilus, midbody, and apex of each liver lobe were obtained in the longitudinal plane.
Lesions were identified via LUS and numbered. If lesions visualized grossly on laparoscopic examination were not identified on LUS, or if lesions on LUS were not visualized grossly on laparoscopic examination, this was noted. Representative images and cine loops of liver lesions were obtained in the longitudinal plane. The number of lesions per liver lobe was determined. If there were more than 5 lesions in 1 lobe, it was considered diffuse change within that lobe and recorded as > 5. The time to perform laparoscopic examination and LUS of the liver was recorded, starting from the moment that the transducer was introduced into the port and ending with the completion of scanning the last liver lobe.
All saved LUS images and cine loops were reviewed by the same board-certified veterinary radiologist (FVG). Lesions were measured and their appearance described. In lobes where there were > 5 lesions, the smallest and largest lesions were measured and expressed as a range in size.
Laparoscopic liver biopsy
All dogs then underwent laparoscopic liver biopsy. The method of biopsy and the individual lobes biopsied, as well as the number of lobes biopsied, were at the discretion of the board-certified veterinary surgeon (JBC). This information was recorded in the standardized operative report. Following the completion of surgery, port incisions were closed routinely. Biopsy samples were submitted for histopathology, anaerobic/aerobic culture and susceptibility, and mineral analysis. The results of these tests were recorded.
Postoperative care and follow-up
Any perioperative surgical complications from the start of surgery to discharge from the hospital that occurred were recorded and graded according to the Clavien-Dindo scheme.12,13 As mild, self-limiting hemorrhage is expected following laparoscopic liver biopsy, this was not considered a complication if no further intervention (eg, the use of hemostatic agents, conversion, blood transfusion, etc) was deemed necessary. The time to discharge from the hospital was recorded. Postoperatively, dogs were managed with methadone (0.1 mg/kg, IV, q 6 h) while in hospital, gabapentin (10 to 20 mg/kg, PO, q 8 h) for 14 days, and trazodone (3 to 5 mg/kg, PO, q 8 h) as needed for anxiolysis for 14 days. Dogs returned in 10 to 14 days for incision assessment and removal of skin sutures. Any postoperative complications from the date of discharge to the time of recheck that occurred were recorded.
Statistical analysis
Descriptive statistics were performed using commercially available statistic software (SAS, version 9.4; JMP, version 9.0.2; SAS Institute Inc). Categorical and discrete numeric variables were summarized by frequencies. Continuous numeric variables were summarized with median and IQR. The Wilcoxon matched pairs signed-rank test was used to determine if there was a difference between the number of liver lesions identified with TUS and LUS. For statistical analysis, lobes with > 5 lesions were considered to have 5 lesions.
Results
Signalment and clinical data
Eight dogs were prospectively enrolled that met the inclusion criteria. The median body weight was 16.15 kg (IQR, 10.15 to 22.2 kg). The breeds represented included mixed-breed dog (3), Miniature Schnauzer (1), Nova Scotia Duck Tolling Retriever (1), Australian Shepherd (1), Shetland Sheepdog (1), and Plott Hound (1). The median age was 8.38 years (IQR, 6.8 to 10.34 years). The sexes were spayed female (5), castrated male (2), and intact female (1). All relevant hepatic bloodwork parameters and coagulation results are summarized in Table 1.
Pertinent preoperative clinicopathologic data for 8 dogs undergoing transabdominal ultrasound (TUS) followed by laparoscopic liver biopsies and laparoscopic ultrasound (LUS) of the liver.
| Variable | Median (IQR) | Reference interval |
|---|---|---|
| ALT (μ/L) | 397.5 (190.5–714.25) | 23–93 |
| ALP (μ/L) | 246.5 (114–763.25) | 7–116 |
| GGT (μ/L) | 6.5 (4.75–14.25) | 6–10 |
| Albumin (g/dL) | 3.06 (2.95–3.23) | 2.62–3.91 |
| Glucose (mg/dL) | 102 (96.25–108.5) | 78–124 |
| Bilirubin (mg/dL) | 0.35 (0.2–0.4) | 0.1–0.4 |
| Cholesterol (mg/dL) | 292 (233.25–415.5) | 102–340 |
| BUN (mg/dL) | 15 (11.5–18) | 7–27 |
| Prothrombin time (s) | 9.2 (8.05–9.8) | 7.06–9.00 |
| Partial thromboplastin time (s) | 12.8 (12.35–13.5) | 10.12–14.21 |
Transabdominal versus LUS
The median time to perform hepatobiliary TUS was 10 minutes (IQR, 7.5 to 12.0 minutes). The median time to perform concurrent laparoscopic examination and LUS was 19.5 minutes (IQR, 17.75 to 23.5 minutes). Only 1 dog had no liver lesions identified on TUS, laparoscopic examination, and LUS. Of the 7 dogs with liver lesions identified, 5 of 7 had additional lesions identified on LUS that were not identified on TUS. In 3 dogs, there were lesions that were not noted on laparoscopic liver examination but were discovered during LUS (Figure 1). In 1 dog, lesions were noted on laparoscopic examination that were not noted on TUS or LUS (Figure 2). These lesions were all capsular and flat, ranging in color from white to tan.
A 10-year-old male castrated Plott Hound underwent transabdominal ultrasound followed by laparoscopic liver biopsies and laparoscopic ultrasound (LUS) of the liver due to chronic liver enzyme elevations and liver nodules. A—Laparoscopic examination of the liver revealed no grossly identifiable lesions within the right medial liver lobe. The LUS transducer is applied to the midbody of the right medial liver lobe. B—Corresponding LUS image of the right medial liver lobe, revealing a well-defined, oval, hypoechoic mass measuring 1.6 cm X 0.9 cm (arrows). C—Laparoscopic examination revealed no grossly identifiable lesions within the left medial liver lobe. The LUS transducer is applied near the hilus of the left medial liver lobe. D—Corresponding LUS image of the left medial liver lobe, revealing a well-defined, hypoechoic nodule measuring 0.3 cm X 0.3 cm (arrow).
Citation: American Journal of Veterinary Research 86, 6; 10.2460/ajvr.25.01.0031
A 14-year-old female spayed Miniature Schnauzer underwent transabdominal ultrasound followed by laparoscopic liver biopsies and LUS of the liver due to chronic liver enzyme elevations. A—Laparoscopic examination revealed a small, tan, flat capsular lesion (arrow) in the midbody of the left medial liver lobe. B—Laparoscopic ultrasound of the same area does not reveal any appreciable corresponding lesion.
Citation: American Journal of Veterinary Research 86, 6; 10.2460/ajvr.25.01.0031
The number of lesions noted on TUS and LUS are summarized in Table 2. In 5 dogs, a minimum of 28 additional lesions were identified on LUS that were not seen on TUS. The number of liver lesions identified was significantly different between TUS and LUS (P = .016), with more lesions identified with LUS (76) than TUS (48). The diameter of the lesions identified on TUS ranged from 0.3 cm to 4.5 cm. The diameter of the lesions identified on LUS ranged from 0.1 cm to 4.1 cm.
Total number of lesions identified in each liver lobe with TUS versus LUS for the 8 dogs mentioned in Table 1.
| Number of lesions (TUS) | Number of lesions (LUS) | |
|---|---|---|
| Left lateral lobe | 13 | 13 |
| Left medial lobe | 8 | 14 |
| Quadrate lobe | 7 | 8 |
| Right medial lobe | 4 | 10 |
| Right lateral lobe | 8 | 14 |
| Caudate lobe | 6 | 14 |
| Papillary lobe | 2 | 3 |
| Total | 48 | 76 |
Surgery
A median of 5 biopsies were performed (IQR, 4 to 6). Laparoscopic punch biopsy forceps were used for the biopsy of all samples except 2, in which laparoscopic Kelley forceps and Metzenbaum scissors were used to perform an excisional biopsy of a cystic lesion. In 2 of 3 dogs that had lesions discovered on LUS that could not be grossly appreciated, LUS was used to localize the lesion and determine the region of the liver lobe to be biopsied.
Anaerobic and aerobic culture results were negative for all samples. The median copper level of hepatic tissue was 455.08 μg/g dry weight (IQR, 203.30 to 952.29 μg/g dry weight; reference interval, 137 to 400 μg/g dry weight). The results of histopathology and copper analysis are summarized in Supplementary Table S1. No malignant neoplastic lesions were diagnosed.
No perioperative complications occurred. All dogs were discharged within 1 day of their procedure. Four dogs returned for a follow-up examination and incision check in 10 to 14 days. The 4 dogs that did not return were seen by their primary veterinarian, and records of that visit were received. No postoperative complications occurred.
Discussion
Laparoscopic ultrasound and biopsy of the liver was safe and effective in this cohort of dogs with underlying liver disease. Most of the dogs (71%) had additional liver lesions identified with LUS that were not noted on preoperative TUS, indicating that LUS is more sensitive for the detection of liver lesions compared to TUS. The use of LUS facilitated correct localization of all liver lesions as the respective lobe could be directly identified while viewing the ultrasound image. Additionally, in 2 dogs where LUS identified liver lesions that could not be appreciated grossly on laparoscopic examination or on preoperative TUS, LUS was successfully used to guide the sampling of these lesions.
Laparoscopic ultrasound for the evaluation of the liver has previously been shown to be feasible in healthy dogs. In that study,9 all liver lobes were scanned with the exception of the caudate lobe, which could not be accessed due to obscurement by the gastrointestinal tract in 2 cases. In the current study, the caudate lobe could not be accessed in 1 dog due to adhesions from a prior right nephroureterectomy. In the remaining 7 dogs, all liver lobes could be accessed and scanned completely.
The time to perform LUS of the liver in the current study was considerably longer than what has been previously reported.9 This is likely due to the presence of liver lesions in most cases, requiring additional time to evaluate these lesions. This is further supported by the fact that the dog with no liver lesions had the shortest LUS time (12 minutes), and the dogs with the most lesions had the longest LUS times (25 and 28 minutes). Further, in the prior study, the time to perform visual laparoscopic examination was separated from the time to perform LUS, whereas in the current study these were performed simultaneously. In the previously mentioned study,9 the time to perform LUS improved with experience. In the current study, all LUS procedures were performed by a surgeon who already had considerable experience with LUS of the liver. Therefore, LUS of the liver in dogs with liver disease may take longer for a novice surgeon but would be expected to improve over time with more experience.
Laparoscopic ultrasound of the liver is frequently performed in people with liver cancer for complete staging prior to curative intent surgery. Prior studies3–5,14 have shown that LUS is more sensitive for small liver lesions compared to preoperative ultrasound, CT, and MRI. In one study4 comparing LUS to preoperative TUS and CT scan, LUS detected new lesions histologically confirmed to be malignant in 22% of people. In 12 patients, this resulted in modification of the original planned surgical treatment.4 The disparity between preoperative imaging and LUS is likely multifactorial. Laparoscopic ultrasound allows for the placement of an ultrasound transducer directly on the liver parenchyma, avoiding ultrasonographic artifacts associated with the gastrointestinal contents or with the lungs that may obscure assessment of the liver, concealment of the liver beneath the ribcage, and difficulty accessing dorsal regions of the liver, which are challenges faced with TUS.
In the current study, most dogs had lesions identified with LUS that were not noted on TUS, indicating that LUS is more sensitive for detecting liver lesions compared to TUS. While all lesions were benign in our study, this could result in a change in prognosis or surgical plan in patients with malignant or metastatic disease. Therefore, LUS combined with laparoscopic liver biopsy may be a useful staging tool prior to definitive surgical treatment for dogs with hepatic neoplasia. Additionally, if more lesions or metastatic disease is identified, other strategies for multifocal disease, like microwave ablation, may be considered in addition to or instead of surgical resection, which could result in better patient outcome.
One of the reported drawbacks of laparoscopic surgery is the loss of tactile feedback due to the inability to palpate structures. This is overcome by the concurrent use of LUS in people, which allows real-time evaluation of deep parenchymal lesions, vasculature, and oncologic margins.15,16 In the current study, 3 dogs had lesions that could not be visualized on laparoscopic examination of the liver and were only identified with LUS examination. Laparoscopic ultrasound was then used to guide the acquisition of biopsies of these lesions in 2 of the dogs, which otherwise may have been missed without the aid of LUS.
Laparoscopic liver resections are considered the standard of care in people due to multiple reported benefits, including decreased pain, complications, blood loss, and hospitalization time, without compromising oncologic outcomes.17–19 In people, LUS is used to guide liver resections and microwave ablation of liver tumors.15,16,20 The concurrent use of LUS allows the mapping of vasculature within the hepatic parenchyma and determination of tumor margins to ensure safe and effective hepatectomies.15,16 While laparoscopic liver resections are not widely performed in veterinary medicine currently, a prior report21 described the feasibility of a laparoscopic approach to partial and complete liver lobectomies in select cases. This report21 did not describe the use of LUS to guide laparoscopic liver resections. Further investigation into laparoscopic liver resections in dogs is needed, with the evaluation of LUS to guide surgical planning.
One of the challenges faced during the current study was concurrent evaluation of the laparoscopic image and the LUS image by the surgeon. As the screens are separate, this required the surgeon to often look back and forth between the screens and likely prolonged the procedure. Furthermore, this could have resulted in lesions that were missed on LUS when the surgeon looked away. In human medicine, this challenge has been described, especially when LUS is used to guide laparoscopic procedures of the liver, like microwave ablation. A prior report22 described overcoming this issue by overlaying the ultrasound image on the laparoscopic video, creating an augmented reality experience. This was tested in tissue phantoms made of gelatin and in several pigs and was used to guide the placement of a microwave ablation probe within fabricated lesions. The use of the augmented reality navigation system improved both needle placement time and targeting accuracy in experienced surgeons and fellows.22 While this may improve the challenges experienced with LUS in the current report, this technology is not currently available in veterinary medicine and therefore was not evaluated in the current report.
Multiple limitations of our study exist. Our sample size was small, making more in-depth statistical analysis unrealistic. Therefore, largely descriptive statistics were reported. Additional analyses to understand factors that may have contributed to a difference in lesion identification, like division of the liver, size of the lesion, or ultrasonographic appearance of the liver, could not be reasonably evaluated with this small sample size. Another limitation was the lack of a gold standard diagnostic to serve as a control, such as contrast-enhanced CT. Requiring all dogs to have a CT scan performed is costly and was not performed for all dogs in this study. The surgeon performing LUS was not necessarily blinded to the results of TUS, which may have influenced the identification of lesions on LUS. However, this was intentionally designed to mimic a typical clinical scenario where TUS would likely be performed prior to LUS. Lastly, all procedures were performed by the same board-certified surgeon with extensive laparoscopic surgery experience and prior LUS experience. Therefore, LUS may be more challenging and require more time when performed by novice surgeons or those without prior LUS experience.
In conclusion, LUS of the liver was safely performed in all dogs and allowed thorough evaluation of the liver at the time of laparoscopic liver biopsy. Significantly more lesions were identified with LUS than conventional TUS. Additionally, LUS helped guide the biopsy of lesions that could not be identified laparoscopically. Therefore, LUS should be considered as a useful adjunctive tool in the diagnosis and staging of dogs with hepatic neoplasia and can be used to guide laparoscopic interventions of the liver in dogs.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
None reported.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the composition of this manuscript.
Funding
This study was funded by the generous contribution of the DeBartolo Minimally Invasive Surgery fund at the University of Florida.
ORCID
F. P. Solari https://orcid.org/0000-0002-4202-8701
E. A. Maxwell https://orcid.org/0000-0002-8201-040X
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