Received: 12 September 2022 | Revised: 26 October 2022 | Accepted: 8 November 2022 DOI: 10.1111/vcp.13221 CASE REPORT Needle tract seeding and malignant transformation of hepatocellular adenoma into well-­differentiated hepatocellular carcinoma in a dog Oriol Jornet-­Rius1 | Beatriz Agulla1 | María Cristina López2 | Claudia Viñeta2 | Alicia García-­Ferrer2 | Bárbara Serrano3 | Alberto Marco3 | Anna Palomares2 | Rosa Novellas1,2 | Yvonne Espada1,2 | Xavier Roura2 | Laia Solano-­Gallego1 1 Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Abstract Universitat Autònoma de Barcelona, An 11-­year-­old neutered female Golden Retriever was referred for investigation of Barcelona, Spain 2 Hospital Clínic Veterinari, Universitat marked increases in liver enzyme activities. Abdominal ultrasound revealed a large Autònoma de Barcelona, Barcelona, Spain pedunculated liver mass. Diagnosis of hepatocellular adenoma (HCA) was made when 3 Servei de Diagnòstic de Patologia the mass was excised after a first unsuccessful attempt through ultrasound-­guided Veterinària, Facultat de Veterinària, Universitat Autònoma de Barcelona, core-­needle biopsy. One and a half years after presentation, a nodule embedded be- Barcelona, Spain tween muscles of the abdominal wall appeared. The mass was first diagnosed as a Correspondence well-­differentiated hepatocellular carcinoma (HCC) through cytologic examination, Laia Solano-­Gallego, Departament de which was later confirmed with histopathology. Ki 67 immunostaining of the abdomi- Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de nal wall nodule showed an increased immunoreactivity compared with the liver mass. Barcelona, 08193 Bellaterra, Barcelona, Therefore, the present case documents the first needle-­tract seeding of a hepato- Spain. Email: laia.solano@uab.cat cellular epithelial tumor with possible malignant transformation of HCA into a well-­ differentiated HCC in a dog. KEYWORDS canine, implantation, liver, metastasis, neoplasia 1 | C A S E PR E S E NTATI O N pedunculated and continuous with the caudal margin of the left liver lobe. An 11-­year-­old neutered female golden retriever was referred with a An ultrasound-­guided biopsy of the mass was performed using history of a marked increase in liver enzyme activities. At presenta- a semiautomatic 14-­gauge core needle (ARGON Medical Devices, tion, complete blood count (CBC) and biochemistry panel showed a Athens, TX, USA). A small skin incision was performed slightly right mild microcytic normochromic nonregenerative anemia (hematocrit of the midline to facilitate needle passage, and once the needle was 33.7%, reference interval [RI] 37.3%–­61.7%; mean corpuscular vol- positioned in the lesion, the trigger was released, and the needle ume 54.6 fL, RI 61.6–­73.5 fL) and elevation of alanine aminotransfer- was removed. The core specimen was teased from the needle and ase (599 U/L, RI 10–­94 U/L), gamma-­glutamyl transferase (51 U/L, RI placed in formalin for histologic assessment. This procedure was 10–­15 U/L) and alkaline phosphatase (3725 U/L, RI 10–­150 U/L). The performed twice at the same incision site. A small quantity of free abdominal ultrasound revealed a heterogeneous mass in the mid-­ fluid was observed after the core biopsy. The patient was monitored, abdomen. The mass measured approximately 10.5 × 6.7 cm and was and additional free fluid was not detected on repeated ultrasound This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. © 2023 The Authors. Veterinary Clinical Pathology published by Wiley Periodicals LLC on behalf of American Society for Veterinary Clinical Pathology. Vet Clin Pathol. 2023;52:507–513.  wileyonlinelibrary.com/journal/vcp | 507 | 1939165x, 2023, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/vcp.13221 by Readcube (Labtiva Inc.), Wiley Online Library on [09/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 508 JORNET-­RIUS et al. examinations. The histologic examination showed a diffuse mild in- Options were discussed with the owners, and an en-­bloc sur- flammatory process mainly composed of macrophages and scarce gical resection of the muscular nodule was made using an elliptical neutrophils, hepatic trabeculae were regular in thickness, and he- incision with 2 cm macroscopic lateral and deep margins around the patocytes were morphologically normal. The absence of portal lesion. On histopathology, the mass consisted of a partially encap- triads and the small sample size made it impossible to establish a sulated, moderately cellular, lobulated neoplastic growth composed definitive diagnosis. Treatment with a hepatic protector was started of irregular thick trabeculae associated with a moderate amount (Samilyn medium size; two tablets once per day). of fibrous desmoplasia (Figure 1C). Multifocal, randomly distrib- The dog was reevaluated 3 months after the initial presentation. uted areas of coagulative necrosis and hemorrhage were observed The owners described episodes of tachypnea interpreted as pain. (Figure 1D). Neoplastic cells were well differentiated, and mild to The physical examination was normal. CBC, biochemistry, thoracic moderate anisocytosis and anisokaryosis were observed. There was radiographs, and abdominal ultrasound were performed. A per- a low mitotic index (2–­3 mitotic figures/HPF) with occasionally aber- sistent marked increase in liver enzyme activities was detected in rant mitotic figures. Ki 67 immunostaining showed a highly increased the biochemistry profile, and the ultrasound showed a mild increase cellular activity (Figure 1F). A diagnosis of well-­differentiated tra- in the size of the liver mass (12 × 8.6 cm), with a similar appearance. becular hepatocellular carcinoma (HCC) was made. Given these changes, an exploratory laparotomy with a partial The dog recovered without any complications, and 8 months hepatectomy was performed. Before the mass excision, a surgical after surgery, the dog showed no clinical signs, and the physical ex- stapling of the liver parenchyma and vessels was performed. No ad- amination was unremarkable. Unfortunately, a complete staging, in- hesions were observed between the liver mass and other abdominal cluding imaging diagnostics, was not performed. structures. Eventually, the liver mass was sent for histopathologic evaluation. The histopathologic examination of the mass showed a nonen- 2 | DISCUSSION capsulated, moderately cellular, neoplastic epithelial proliferation that was clearly demarcated and well differentiated from the adja- Hepatic neoplasia is an infrequent condition in dogs accounting cent normal liver (Figure 1A). Neoplastic cells formed regular trabec- for between 0.6% and 1.3% of all canine neoplasms.1,2 HCC is the ulae of 2–­3 cells thick and were separated by sinusoids (Figure 1B). most frequent primary hepatic neoplasm in dogs; however, HCA is Neoplastic cells were well differentiated and had focal areas of finely an unusual condition. Both neoplasms usually appear in dogs older vacuolated cytoplasm and round nuclei with single nucleoli. Mild than 10 years, and sex or breed predispositions do not seem to be anisocytosis and anisokaryosis were seen, with 0–­1 mitotic figures/ present.1,2 Dogs with hepatic neoplasia can show nonspecific clini- HPF and mild positivity for Ki 67, a marker of cellular proliferation cal signs.1,2 However, like in the present case, up to 50% of dogs (Figure 1E). A diagnosis of hepatocellular adenoma (HCA) was made. with these neoplasms show no clinical signs and are diagnosed dur- Seventeen months after the core-­needle biopsy, the presence of ing the investigation of increased liver enzyme activities.3 Although an adhered 3 cm subcutaneous nodule was noted at the previous the physical examination is often unremarkable, a cranial abdomi- core-­needle biopsy site. An abdominal ultrasound was performed nal mass can be detected in up to 75% of dogs with a liver tumor. 2 and found to be unremarkable. Ultrasound of the nodule showed Clinicopathologic findings are also nonspecific; therefore, they can- that it was embedded into the muscular layers of the ventral abdom- not distinguish between neoplastic and nonneoplastic liver disease. inal wall and measured 1.96 × 2.16 cm (Figure 2A). An ultrasound-­ Nonregenerative anemia, leukocytosis, and increased liver enzyme guided fine-­needle aspiration (FNA) of the nodule using a 23-­gauge activities are the most common laboratory findings.1,2 needle was performed and sent for cytopathologic examination. Differential diagnoses of hepatic masses in dogs include nod- On cytology, many sheets of polygonal to round hepatocytes with ular hyperplasia, regenerative nodules, HCA, HCC, bile duct car- mild to moderate atypia were seen, including moderate anisokary- cinoma, hepatic carcinoids, abscesses, and metastatic neoplasia. osis, frequent binucleated and multinucleated cells, macrokaryosis, Therefore, in veterinary medicine, morphologic evaluations of multiple nucleoli, and atypical mitotic figures. These findings were the liver remain necessary to establish a definitive diagnosis.4 suggestive of a proliferation of hepatocytes with mild to moderate In this case, a first diagnostic attempt was carried out through atypia and a cytologic diagnosis of well-­differentiated hepatocellular an ultrasound-­g uided core-­n eedle biopsy. The regularity of the carcinoma (WD-­HCC; Figure 3A–­F ). trabeculae and the morphologic features of the hepatocytes re- CBC and biochemistry results were within normal limits, with sembled normal liver parenchyma, but the absence of portal no abnormalities found on thoracic radiographs. On full-­body com- spaces made it impossible to establish whether it was a well-­ puted tomography, a soft tissue-­attenuating nodule of 2 cm in diam- differentiated benign neoplastic growth (adenoma) or hyperplas- eter was identified in the rectus abdominis muscle, affecting both tic nodule. However, in human medicine, a diagnosis is primarily internal and external layers without extending into the peritoneal based on computed tomography and magnetic resonance imag- cavity (Figure 2B,C). The lesion showed a moderate heterogeneous ing findings, and biopsy is only used when the imaging pattern is contrast enhancement and was located at the level of the third lum- not fully concordant with the diagnostic criteria. 5 A study in dogs bar vertebra. comparing different methods of liver core-­n eedle biopsies using | 1939165x, 2023, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/vcp.13221 by Readcube (Labtiva Inc.), Wiley Online Library on [09/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License JORNET-­RIUS et al. 509 F I G U R E 1 Histopathologic examination of the hepatic mass and intramuscular abdominal wall nodule in a dog with hepatocellular carcinoma. (A, B) Hepatocellular adenoma. The neoplasm is well demarcated with adjacent normal liver and formed pseudolobular structures composed of regular thick trabecula. (C) Hepatocellular carcinoma effacing muscle and adipose tissue and showing loss of lobar architecture, irregular thickness of trabeculae (>5 hepatocytes thick), and moderate fibrous desmoplasia. (D) Randomly distributed areas of lytic necrosis and hemorrhage within the intramuscular hepatocellular carcinoma. (E) Ki-­67 immunostaining of the hepatic mass showed mild positivity (on average 2.9 positive nuclei/HPF). (F) Ki-­67 immunostaining of the intramuscular mass showed a highly increased positivity on average 21.1 positive nuclei/HPF. different needle sizes with paired necropsy biopsies found a low In the present case, the histologic features of the surgically agreement between core-­n eedle and wedge biopsies. 6 This obser- excised liver mass were consistent with HCA. However, one and a vation was related to the small size of the samples obtained with half years after the core-­needle biopsy, a slowly growing abdominal core-­n eedle biopsies. Therefore, obtaining 3–­12 portal triads and wall nodule appeared in the region of the needle tract. This mass multiple biopsies is recommended to enhance the likelihood of a was diagnosed as a well-­differentiated HCC cytologically, and sub- correct diagnosis. 6 sequently, the final diagnosis was confirmed by histopathologic | 1939165x, 2023, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/vcp.13221 by Readcube (Labtiva Inc.), Wiley Online Library on [09/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 510 JORNET-­RIUS et al. F I G U R E 2 CT and ultrasound images of the abdomen of a dog with hepatocellular carcinoma 17 months after the core-­needle biopsy. (A) Ultrasound with a 15 MHz linear transducer. The nodule was mildly heterogeneous, hypoechoic, well defined, and embedded in the rectus abdominis muscle. (B) A postcontrast transverse image in a soft-­tissue window at the level of the third lumbar vertebra. The nodule was located in the rectus abdominis muscle and did not extend into the peritoneal cavity. No further nodules were identified. (C) Postcontrast sagittal CT reconstruction in the soft tissue window. The soft tissue-­attenuating nodule (white arrow) is located around 8 cm caudal to the liver. CT, computed tomography. evaluation. Additionally, both specimens were later reviewed by the abdominal wall mass compared with the initial liver mass could another ECVP-­boarded pathologist in a blinded fashion, confirming support the hypothesis of a malignant transformation during the both diagnoses. seeding process. However, the ability of the Ki 67 to differentiate Malignant transformation of an HCA into an HCC is a rare but HCA from HCC has only been evaluated in human liver samples.9 7 well-­known complication in human medicine ; however, to the au- Although most HCA tumors have had low Ki 67 expression (<4%), thors' knowledge, this is the first report of possible malignant trans- up to 50% of HCC cases had Ki 67 expression <4%, limiting its use- formation associated with needle tract seeding in dogs. Malignant fulness.9 A study in dogs evaluating the usefulness of Ki 67 in the transformation has been reported in 4.2% of human patients with cytologic identification of liver tumors found a significant increase HCA.7 In human medicine, although the natural history of this pro- in Ki 67 expression in hepatic neoplasia compared with nontumoral gression is not well defined, multiple risk factors have been associ- lesions, suggesting that the concurrent use of cytology and Ki 67 ated with malignant transformation, including male gender, a tumor immunocytochemistry could improve the diagnostic accuracy of size >5 cm, oral contraceptive intake, and genetic mutations.7,8 In identifying liver neoplasia.10 Nevertheless, this study did not include this dog, the presence of a 10-­fold increase in Ki 67 expression by any HCA cases; therefore, the ability of using Ki 67 expression to | 1939165x, 2023, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/vcp.13221 by Readcube (Labtiva Inc.), Wiley Online Library on [09/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License JORNET-­RIUS et al. 511 F I G U R E 3 Well-­differentiated hepatocellular carcinoma in the abdominal wall of a dog. (A, B, D) Fine-­needle aspiration of the abdominal wall mass. (C, E, F) Imprint touch cytology of the same mass. Modified rapid Romanowsky-­stain (Quick Panoptic). (A, B) Sheets of polygonal to rounded epithelial cells with a perivascular arrangement. (C, D) Moderate to high nucleus-­to-­cytoplasm ratio and mild to moderate anisocytosis and anisokaryosis. (D–­F ) Round centrally placed nuclei with coarsely stippled chromatin. Amphophilic with distinct cytoplasmic borders. Occasional clear intracytoplasmic vacuoles are present. (D) A Hepatocellular aggregate shows a perivascular arrangement and an atypical mitotic figure (center). (E) The group of hepatocytes shows moderate anisocytosis and anisokaryosis, with one to multiple prominent nucleoli. A macronucleus is observed (top right). (F) An atypical mitotic figure is seen at the center of the image. differentiate between HCC and HCA remains unknown in veterinary examinations. Histologic evidence of extrahepatic metastasis and medicine.10 vascular/adjacent parenchyma invasion are key diagnostic criteria for The morphologic features of a WD-­HCC often overlap with malignancy. 2 However, these features are not always present and; those of benign HCA neoplasms, and less frequently, benign pro- therefore, the presence of other features such as cellular pleomor- liferations such as nodular hyperplasia, and regenerative nodules, phism, mitotic figures, multiple nucleoli, and variation in thickness are challenging to distinguish on either histopathologic or cytologic of the trabeculae, has to be evaluated.11 Useful cytologic features in | 1939165x, 2023, 3, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/vcp.13221 by Readcube (Labtiva Inc.), Wiley Online Library on [09/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 512 JORNET-­RIUS et al. the diagnosis of WD-­HCC are the dissociation of hepatocytes, acinar Claudia Viñeta https://orcid.org/0000-0001-8668-5538 or palisading arrangements, the presence of naked nuclei and cap- Alicia García-­Ferrer https://orcid.org/0000-0003-1238-522X illaries, multinuclearity, increased N:C ratios, and mild anisocytosis Bárbara Serrano https://orcid.org/0000-0003-4062-6211 and anisokaryosis.12 Therefore, we cannot completely rule out that Alberto Marco https://orcid.org/0000-0003-1680-0822 the initial diagnosis of HCA, in this case, might have been a misdiag- Anna Palomares https://orcid.org/0000-0002-8334-7346 nosis of a well-­differentiated HCC with subsequent seeding. Rosa Novellas https://orcid.org/0000-0003-2392-9202 Needle-­tract seeding is a known complication associated with Yvonne Espada https://orcid.org/0000-0003-1556-6587 percutaneous needle biopsies in both humans and animals, and al- Xavier Roura https://orcid.org/0000-0002-1098-2381 though its incidence is rare, the development of needle tract metas- Laia Solano-­Gallego https://orcid.org/0000-0001-8479-4896 tases following biopsies has been described in almost every type of neoplasm in human medicine.13 In veterinary medicine, it has been REFERENCES described in the urinary bladder, urethral, and prostatic transitional 1. Patnaik AK, Hurvitz AI, Lieberman PH. Canine hepatic neoplasms: a cell carcinoma14–­17 pancreatic carcinoma,18 pericardial mesotheli- clinicopathologic study. Vet Pathol. 1980;17:553-­564. 2. Trigo FJ, Thompson H, Breeze RG, Nash AS. The pathology of liver oma,19 renal cell carcinoma, 20 carcinomatosis, 21 and pulmonary ad- tumours in the dog. 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