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Year : 2020  |  Volume : 16  |  Issue : 5  |  Page : 1100-1105

Endoscopic ultrasound-guided sampling using core biopsy needle for diagnosis of left-lobe hepatocellular carcinoma in patients with underlying cirrhosis

1 Department of Ultrasound, The First Affiliated Hospital of Zhejiang Chinese Medical University, Hangzhou, China
2 Department of Ultrasound, College of Medicine, The First Affiliated Hospital, Zhejiang University, Hangzhou, China
3 Department of Ultrasound, College of Medicine, The First Affiliated Hospital, Zhejiang University; Key Laboratory of Precision Diagnosis and Treatment for Hepatobiliary and Pancreatic Tumor of Zhejiang Province, Hangzhou, China

Date of Submission08-Sep-2019
Date of Decision20-Mar-2020
Date of Acceptance28-Apr-2020
Date of Web Publication29-Sep-2020

Correspondence Address:
Tian-An Jiang
Department of Ultrasound, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou 310003; Key Laboratory of Precision Diagnosis and Treatment for Hepatobiliary and Pancreatic Tumor of Zhejiang Province, Hangzhou 310003
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcrt.JCRT_723_19

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 > Abstract 

Objective: The objective is to evaluate the application of endoscopic ultrasound-guided fine needle biopsy (EUS-FNB) in the diagnosis of the left-lobe hepatocellular carcinoma (HCC) in cirrhotic patients with contraindication to percutaneous biopsy.
Materials and Methods: Thirty-eight consecutive patients with liver cirrhosis and suspected left-lobe HCC and with contraindication for percutaneous biopsy undergoing EUS-FNB between January 2011 and December 2014 were included in this study. The final diagnosis was obtained through histopathology of surgical samples or clinical and imaging results with follow-up. Using the final diagnosis as the gold standard, the diagnostic performance of EUS-FNB for HCC detection was evaluated.
Results: Among 38 patients, EUS-FNB was successfully performed in 34 cases, in which adequate biopsy specimens were obtained for histopathological examination in 30. For the 30 patients with biopsy results, 25 cases were confirmed to have HCC, while five cases had benign lesions according to the final diagnosis. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy rates of EUS-FNB in the diagnosis of HCC were 88.0% (22/25), 100.0% (5/5), 100.0% (22/22), 62.5% (5/8), and 90.0% (27/30), respectively. Self-limiting bleeding occurred in three patients.
Conclusions: EUS-FNB is a sensitive and safe diagnostic modality for cirrhotic patients with suspected HCC located in the left lobe, especially those for whom percutaneous biopsy is contraindicated.

Keywords: Endoscopic ultrasound, fine-needle biopsy, hepatocellular carcinoma, liver cirrhosis

How to cite this article:
Chen F, Bao H, Deng Z, Zhao Q, Tian G, Jiang TA. Endoscopic ultrasound-guided sampling using core biopsy needle for diagnosis of left-lobe hepatocellular carcinoma in patients with underlying cirrhosis. J Can Res Ther 2020;16:1100-5

How to cite this URL:
Chen F, Bao H, Deng Z, Zhao Q, Tian G, Jiang TA. Endoscopic ultrasound-guided sampling using core biopsy needle for diagnosis of left-lobe hepatocellular carcinoma in patients with underlying cirrhosis. J Can Res Ther [serial online] 2020 [cited 2021 Apr 13];16:1100-5. Available from: https://www.cancerjournal.net/text.asp?2020/16/5/1100/296445

 > Introduction Top

Liver cancers are the fourth-most common cause of cancer-related death and rank sixth in terms of incident cases.[1] The incidence is particularly high in Asia due to the high prevalence of hepatitis B virus infections.[2],[3],[4] Early diagnosis of hepatocellular carcinoma (HCC) is critical for treatment efficacy and long-term survival.[5],[6],[7],[8],[9],[10] When two separate triple-phase imaging tests fail to demonstrate the typical enhancement pattern of the suspicious mass, tissue samples are required for histological diagnosis. With real-time visualization of the needle, ultrasound-guided percutaneous core biopsy represents the standard approach for liver tissue acquisition, especially so in China.[11],[12],[13],[14] However, this method becomes problematic when liver lesions identified on computed tomography or magnetic resonance imaging (in HCC surveillance) are not readily visualized on trans-abdominal ultrasonography (US), which occurs at a relatively high frequency, particularly so for small lesions (<2 cm) in patients with underlying cirrhosis.[15],[16],[17],[18],[19] Intraperitoneal hemorrhage is the most serious adverse event of percutaneous liver biopsy, which may be caused by penetrating injury of a branch of the hepatic artery or portal vein, or by deep inspiration during the biopsy. A risk factor for hemorrhage occurring after liver biopsy is the presence of coagulation disorders, which are frequently seen in patients with advanced cirrhosis.[20],[21] Therefore, an alternative sampling technique is required for the situation mentioned above.

Currently, endoscopic ultrasound (EUS)-guided biopsy of nearby tissue that involves <5–7 cm of the upper and lower gastrointestinal tract is used to obtain a diagnosis of cancer in the digestive tract, pancreas, and mediastinum. When a core needle is used, both cytology and histology results can be obtained.[22],[23],[24]

Given its proximity to the organs, EUS appears to be a reliable tool for the evaluation of the left portion of the liver compared with traditional ultrasound (US) imaging. Hence, EUS-guided fine needle biopsy (EUS-FNB) method is a potential alternative for such patients, as it uses a relatively finer needle to minimize the distance between the lesions.[25],[26],[27],[28],[29]

Investigators began to use EUS-FNB on liver parenchyma and metastasis lesions to obtain more ideal safety statistics.[30],[31],[32],[33],[34],[35] However, only few studies on the use of EUS-FNB for the diagnosis of HCC with underlying cirrhosis have been performed.[36],[37] Especially in patients with coagulation risk factors, the safety of EUS-FNB is unknown. The aim of this study was to report our experience with EUS-FNB of suspected HCC in the left and caudate lobes as a possible alternative to ultrasound-guided percutaneous liver biopsy.

 > Materials and Methods Top


Retrospective data were collated for a cohort of 2532 patients with suspected primary liver tumor. Data on pathological findings and guide management decisions at our hospital between January 2011 and December 2014 were collected. In this cohort, 2398 patients successfully underwent percutaneous liver biopsy. However, for the remaining 134 cases with hepatitis B virus-related cirrhosis, percutaneous biopsy was contraindicated for one or more of the following reasons: (1) The tumor mass was invisible by traditional US; (2) poor accessibility (including interpositioning vessels or dilated biliary duct); (3) coagulation dysfunction (platelet count <50,000/mm 3 (90,000–450,000/mm 3; international normalized ratio >1.5 [0.85–1.25]); and (4) liver cirrhosis with moderate ascites.

After further clinical evaluation and informed consent communication, some patients received EUS-FNB as a possible diagnostic alternative. The exclusion criteria were as follows: (1) Mass present in right lobe (n = 64); (2) severe coagulopathy (platelet count: <30,000/mm 3 (90,000–450,000/mm 3] or international normalized ratio >3 [0.85–1.25]) (n = 8); (3) not willing to enroll in the study (n = 5); (4) invisibility of the lesion by EUS (n = 3); (5) lack of safety accessibility (n = 13); (6) not having a sufficiently long clinical follow-up period of at least 1 year without surgical resection (n = 3).

Consequently, a total of 38 patients were included in this study.


After informed consent was obtained, all patients underwent EUS by two experienced investigators with an oblique-forward-viewing electronic linear array echoendoscope (Pentax FG 32 UA, Pentax Inc., Tokyo, Japan) connected to a processor with a color Doppler function (SSD-5000; Aloka, Tokyo, Japan). All inspections were performed in the following order: After identification of the surrounding structures, the left lobe and hilum of the liver were examined from the gastric body and fundus. The right lobe of the liver was imaged from the duodenum and antrum. Once any suspicious mass was observed, the vascularity of the lesion and surrounding area was assessed by color flow Doppler prior to FNB. Next, the echo of the mass and the vascularity, size, and location were recorded.

Endoscopic ultrasound-guided fine needle biopsy procedure

If the lesion was considered appropriate for sampling, puncture was performed via the gastric wall or duodenum with a 22-gauge FNB device (Echotip ProCore; Wilson-Cook Medical, Winston-Salem, NC, USA), which features a hollowed-out reverse bevel at the tip of the needle. The stylet was then removed after puncturing the lesion. The needle was moved to and fro 10–15 times within the lesion and finally withdrawn from the lesion guided by real-time EUS imaging. The application of suction was performed at the discretion of the endosonographers. Given that our institutions do not have an on-site pathologist, the procedure was repeated until whitish material became visible macroscopically. A maximum of four passes was made for each lesion. The procedure was considered successful if the punctures had been completed as described above. Successful sample collection was defined as having ample sample material to make a diagnosis at the cytological or histological level.

Cytology and histology

A portion of each pass of the sample was processed for both cytological and histological analysis. Slides were fixed with alcohol and stained with hematoxylin-eosin (HE) stain for cytological analysis and used to describe the diagnosis based on cytology and degree of malignancy in each specimen. The material for histological analysis was formalin-fixed, embedded in paraffin, sectioned, and stained with HE and periodic acid-Schiff. For all cases where appropriate histological specimens were obtained, immunohistochemical (IHC) studies were performed using the Arginase-1, Hepatocyte paraffin 1, Glypican-3, AFP, pCEA, and CD10 markers.

Final diagnosis

Clinical data, including data reflecting a minimum of 12 months of follow-up in those patients who required such observation, was also gathered. The final diagnosis was based on at least one of the following findings: (1) resected specimen from patients undergoing laparoscopic operation or surgery; (2) histopathological findings with definitive proof of malignancy in patients and clinical/imaging follow-up compatible with malignant disease; (3) cytological and histological findings lacking proof of malignancy; and (4) no progression in the size of the lesion on follow-up imaging and an uneventful clinical course of disease for at least 12 months.

Statistical analysis

Classification parameters, including gender and location of mass, were expressed as frequencies and proportions. Continuous variables were summarized as means with standard deviations (SD). A diagnostic accuracy analysis was performed, and sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) were calculated. Qualitative data were analyzed using the Chi-square test, whereas quantitative data were analyzed by the t-test. A probability (P) value of <0.05 was considered to indicate statistical significance. All statistical analyses were performed using SPSS software (version 17.0; SPSS Inc., Chicago, IL, USA).

 > Results Top

Between January 2011 and December 2014, 38 consecutive patients with hepatitis B virus-related cirrhosis met the inclusion criteria and underwent EUS-FNB for suspected HCC in the left hepatic lobe. The mean age of the patients was 55.7 years (SD ± 11.8), and the study included 35 men and 3 women. The Child-Pugh scores were distributed as follows: Twelve patients were categorized as Class A, 22 patients as Class B, and four patients were categorized as Class C. Eleven patients were posthepatectomy.

Final diagnosis

The final diagnosis was HCC in 30 cases, hyperplastic nodule in six cases, and focal inflammation in two cases. This final diagnosis was based on surgically or laparoscopically obtained specimens in 24 patients, among which the cytological or histological findings indicated malignancy in six and no proof of malignancy in eight patients, together with a clinical follow-up of at least 12 months.

Endoscopic ultrasound

The EUS findings for the 38 patients are provided in [Table 1]. Thirty-eight patients underwent evaluation with EUS for suspected HCC in the left hepatic lobe. For all 38 patients, EUS successfully identified 44 hepatic lesions ranging in size from 0.6 to 3.5 cm (1.88 ± 0.72 cm). EUS also identified additional lesions (compared with the previous imaging) in 5.3% (2 of 38) of the patients, in whom all of the lesions were <1.5 cm in size. Five patients had multiple lesions and for such patients, only the largest tumor was included for imaging analyses. Fifteen and 12 masses were located in segments 2 and 3, respectively. The remaining eight and three masses were located in segments 4 and 1, respectively. Compared with the benign lesions identified in the underlying liver cirrhosis, HCC lesions were more often hypoechoic on EUS (P = 0.003) and larger in size (P = 0.012).
Table 1: Endoscopic ultrasound-guided fine-needle biopsy

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Endoscopic ultrasound-fine needle biopsy results

EUS-FNB was performed in 38 patients to identify the largest liver lesions [Figure 1]. We abandoned the FNB procedure for one lesion, which was 0.9 cm in size and located in segment 4a and another lesion for which the puncture route was approximately 3 cm; therefore, we could not precisely adjust the needle to the target. During the puncture procedure, two patients (both lesions were beneath the capsule with cirrhosis background) bled immediately after the first and the second passes. Therefore, we stopped the procedure instantaneously. However, in one of these two patients, the procedure was abandoned after sufficient tissue was obtained to fulfill the histology diagnosis. The platelet counts of the two patients were 6500/mm 3 and 4300/mm 3, respectively, with INRs of 1.0 and 1.5, respectively. Neither of the two patients took anticoagulant drugs.
Figure 1: Histopathologically confirmed hepatocellular carcinoma in a 58-year-old man after right lobe hepatectomy. (a) Magnetic resonance presents an abnormally long T2 signal in the left lobe. (b) Conventional US could not identify the nodule in the cirrhotic background. (c) Endoscopic ultrasound reveals a small 1-cm hyperechoic nodule. (d) Endoscopic ultrasound-fine needle biopsy was performed. (e) Cytological findings of hepatocellular carcinoma. (f) Histological examination confirms hepatocellular carcinoma

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In total, the puncture procedure was successful in 34 patients with 34 lesions. The successful sample collection rate was 88.2% (30/34). Among these samples, a histologic diagnosis was obtained for 79.4% (27/34) of the samples. Nevertheless, a high-quality tissue core was not present in all adequate samples. Instead, only 58.8% (20/34) of FNB samples could fulfill the IHC examination. The pathological examination revealed benign results in eight cases and malignant results in 22 cases. Three of the eight cases of EUS-FNB that resulted in a benign diagnosis were later confirmed to be false negative. The rate of correct diagnosis when the results of histological and cytological diagnostic work-ups were combined was 72.9% (27/34). In patients from whom samples could be collected, the sensitivity, specificity, PPV, NPV, and accuracy were 88% (22/25), 100% (5/5), 100% (22/22), 62.5% (5/8), and 90% (27/30), respectively.

The diagnostic performance of EUS-FNB using a core biopsy needle with respect to the size and location of the lesion is presented in [Table 2] and [Table 3].
Table 2: Endoscopic ultrasound-guided fine-needle biopsy performance with respect to the size of the lesions (n=38)

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Table 3: Endoscopic ultrasound-guided fine-needle biopsy performance with respect to the lesion location (n=38)

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A significant reduction in the correct diagnostic rate was noted for lesions with a diameter of ≤10 mm compared with those with a diameter of >10 mm (P = 0.035). A reduced correct diagnosis rate was also found for lesions located in segment IV compared with those located in the other 3 segments (P = 0.046).

Adverse events

No major adverse events requiring surgical or interventional measures were observed. Self-limiting local bleeding occurred in two patients and was observed immediately after the first and second puncture, separately. These two patients were hospitalized and closely monitored. Further intervention such as blood transfusion was necessary in neither of the cases. In one patient, we observed approximately 3 mm of liquid around the left lobe approximately 5 min after the puncture procedure. The situation was carefully observed for 6 h and no further additional treatment was needed.

 > Discussion Top

Due to the high frequency applied, the depth of EUS examination is limited to 5–7 cm. The right lobe of the liver cannot be observed routinely. This study demonstrated that EUS-FNB can provide an image-and pathology-based diagnosis of hepatic left-lobe primary malignancies in cases where routine US-guided percutaneous biopsy is contraindicated. The higher the imaging resolution, the better access to lesions in the left lobe of the liver. This opportunity is particularly enabled by the lack of vascular structures and an interposed bowel.

Percutaneous liver biopsy is still an important diagnostic method for malignant hepatic tumors. However, in some patients, it is not easy to do the biopsy under US guidance, particularly when lesions are small (<2 cm) and/or when lesions are difficult to distinguish from the tissue background, such as that observed in liver cirrhosis. The procedure is also difficult in patients with a large body habitus.

In this study, EUS identified 20 lesions, which were as small as 0.6 cm in size, where previous findings on percutaneous US had been negative. EUS identified additional lesions compared with the previous imaging examination in 5.3% (2/38) of the patients. Our investigation demonstrated that HCC typically appears hypoechoic on EUS, whereas benign lesions were relatively isoechoic or hyperechoic.

In this study, EUS-FNB was performed in 388 patients who were contraindicated for routine US-guided percutaneous biopsy. Among these difficult cases, EUS-FNB was a relatively accurate (72.9%) and very feasible (97.3%) technique. Histological evaluation using HE and IHC was possible for 20 of 37 patients (54.1%). The technical factor could explain the significant decrease in diagnostic yield when the lesion size was ≤ 10 mm. The core needle we used had a side hole, and the length from the tip to the proximal end of the side hole is 6 mm for 22-gauge needles. During the stroke, it is difficult to keep the side hole inside the small lesion to prevent contamination. Given the difficulties experienced when adjusting the puncture angle in the cirrhotic tissue and given the fact that the left lobe surrounding the ascites could slightly move during the procedure, it is difficult to precisely target a small lesion over a relatively longer distance. We suggest that caution should be taken when performing EUS-FNB for lesions that are small (<1 cm) and/or located in segment IV.

Patients with the following features represented patients with increased bleeding risks: (1) liver cirrhosis (n = 37); (2) poor coagulation function (n = 8); and (3) moderate ascites (n = 3). The puncture procedure was complicated in three cases by self-limiting bleeding. Two of the patients were hospitalized for closer monitoring, but given the context, this finding appears to be an acceptable result.

EUS-FNB appears to be safer than percutaneous biopsy in patients with coagulopathy disorders and advanced liver cirrhosis. Lesions beneath the liver capsule and HCC nodules exhibiting increased tumor vascularity could not be excluded as a reason for this finding. However, these features would increase the risk of possible seeding of tumor cells into the peritoneal cavity. The impact of tumor cell nidation in the peritoneum should be critically evaluated with longer surveillance.

Our findings differ from previous reports of EUS-FNA on liver lesions. In contrast to previous studies, we followed the clinical procedure prospectively when designing the study. After including all the possible patients in the EUS-FNB examination, the present study was anticipated to provide data on sensitivity, specificity, PPV, and NPV.

However, our study had several limitations. Small sample size and lack of a control group are the major shortcomings of this study, and the study might also be limited by its statistical strength. Furthermore, not all patients underwent surgery to confirm the final pathological results.

 > Conclusions Top

It is reasonable to conclude that EUS-FNB with core biopsy needle is a sensitive and safe method for diagnosis of suspected HCC in the left hepatic lobe in patients with underlying liver cirrhosis when routine percutaneous ultrasound-guided liver biopsy is unsafe or impossible.


This work was supported by Zhejiang provincial basic public welfare research program (grant number: LGD19C04007 to Fen Chen).

Financial support and sponsorship

The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflicts of interest

There are no conflicts of interest.

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  [Table 1], [Table 2], [Table 3]


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