Comparison of tru-cut biopsy and fine-needle aspiration cytology in an experimental alcoholic liver disease model

Yasemen Adalı Hüseyin Avni Eroğlu Mustafa Makav Sunay Sibel Karayol Gülname Fındık Güvendi Mustafa Gök About the authors

SUMMARY

INTRODUCTION

Liver biopsies such as tru-cut (sharp needle) and fine-needle aspiration cytology (FNAC) are the most commonly preferred techniques to detect the grade and stage of certain liver diseases. In this study, we aimed to compare the efficiency of USG-guided tru-cut biopsy and fine-needle aspiration cytology in an experimental alcoholic liver disease model.

METHODS

Thirty-six female Wistar albino rats, 4-6 months old, and weighing from 190 to 250 g, were used in this study. The animals were randomly divided into six equal groups: G1 (control), G2 (tru-cut control), G3 (FNAC control), G4 (Alcoholic liver disease model), G5 (Alcoholic liver disease model + FNAC), and G6 (Alcoholic liver disease model + tru-cut biopsy). After a histopathological evaluation by light microscopy, the sensitivity, specificity, positive and negative predictive values of FNAC and tru-cut biopsy for the diagnosis of liver lesions were calculated.

RESULTS

No pathology was detected in G1 except for mild congestion. On the other hand, hepatocyte damage, periportal inflammation, congestion, and fatty changes were detected in all liver tissues of the alcoholic liver disease groups. The sensitivity of hepatocyte damage, inflammation, congestion, and fatty change parameters for FNAC were 33.3%, 80%, 0%, and 0%, respectively, while the sensitivity of the same variables for tru-cut were 66.7%, 40%, 100%, and 20%, respectively.

DISCUSSION

Both techniques were superior in some aspects. FNAC can be an attractive alternative to tru-cutbiopsy and applied in routine practice in the diagnosis of non-tumoral liver diseases.

Liver diseases, alcoholic; Biopsy, fine-needle; Biopsy; Aspiration Biopsy

RESUMO

INTRODUÇÃO

Biópsias hepáticas tais como por agulha tru-cut e por citologia aspirativa por agulha fina (CAAF) são as técnicas frequentemente preferidas para detectar o grau e o estágio de certas doenças hepáticas. Neste estudo, nosso objetivo foi comparar a eficiência da biopsia com agulha tru-cut guiada por ultrassom e a citologia aspirativa por agulha fina em um modelo experimental de doença hepática alcoólica.

MÉTODOS

Trinta e seis ratos Wistar albinos fêmeas, de 4 a 6 meses de idade e pesando entre 190 e 250g, foram utilizados neste estudo. Os animais foram divididos aleatoriamente em seis grupos: G1 (controle), G2 (controle tru-cut), G3 (CAAF), G4 (modelo de doença hepática alcoólica), G5 (modelo de doença hepática alcoólica + CAAF) e G6 (modelo de doença hepática alcoólica + biópsia tru-cut). Após uma avaliação histopatológica por microscopia de luz, foram calculados a sensibilidade, especificidade e os valores preditivos positivos e negativos da CAAF e biópsia por tru-cut para o diagnóstico de lesões hepáticas.

RESULTADOS

Nenhuma patologia foi detectada no G1, apenas leve congestão. Por outro lado, detectamos danos nos hepatócitos, inflamação periportal, congestão e alterações nos ácidos graxos nos tecidos hepáticos de todos os grupos de doença hepática alcoólica. As sensibilidades encontradas para os danos nos hepatócitos, inflamação, congestão e alterações nos parâmetros de ácidos graxos para a CAAF foram 33,3%, 80%, 0% e 0%, respectivamente, enquanto que as sensibilidades das mesmas variáveis para o método tru-cut foram 66,7%, 40%, 100% e 20%, respectivamente.

DISCUSSÃO

Ambas as técnicas foram superiores em alguns aspectos. A CAAF pode ser uma alternativa atraente à biópsia por tru-cut e aplicada como prática de rotina no diagnóstico de doenças hepáticas não tumorais.

Hepatopatias alcoólicas; Biópsia por agulha fina; Biópsia

INTRODUCTION

Alcoholic liver disease (ALD) is known as a progressive disease that worsens with the prolonged use of alcohol11. Osna NA, Donohue TM Jr, Kharbanda KK. Alcoholic liver disease: pathogenesis and current management. Alcohol Res. 2017;38(2):147-61. . The main risk factors of ALD are genetic and metabolic traits, sex, obesity, and volume and duration of alcohol use22. Rehm J, Samokhvalov AV, Shield KD. Global burden of alcoholic liver diseases. J Hepatol. 2013;59(1):160-8. . ALD represents a wide-range spectrum of liver pathologies such as steatosis, steatohepatitis, steatofibrosis-cirrhosis, cholestasis, alcoholic foamy degeneration, megamitochondria, perivenular fibrosis-central hyaline sclerosis, and siderosis33. Celli R, Zhang X. Pathology of alcoholic liver disease. J Clin Transl Hepatol. 2014;2(2):103-9. . Steatosis (fatty changes), which is generally seen in 90% of heavy drinkers, is the first liver response to alcohol44. Orman ES, Odena G, Bataller R. Alcoholic liver disease: pathogenesis, management, and novel targets for therapy. J Gastroenterol Hepatol. 2013;28(Suppl 1):77-84. . Alcohol shows its pathogenesis in different pathways by increasing NADH/NAD+ in the hepatocytes, disrupting fatty acid oxidation, increasing triglyceride synthesis, upregulating lipogenic enzymes, leading to lymphocyte recruitment, increasing gut permeability, translocation of bacterial products such as LPS into the portal circulation, triggering neutrophilic infiltration, secretion of cytokines and chemokines, and inhibiting the anti-fibrotic action of natural killer cells44. Orman ES, Odena G, Bataller R. Alcoholic liver disease: pathogenesis, management, and novel targets for therapy. J Gastroenterol Hepatol. 2013;28(Suppl 1):77-84.

5. Albano E, Vidali M. Immune mechanisms in alcoholic liver disease. Genes Nutr. 2010;5(2):141-7.
- 66. Thiele GM, Freeman TL, Klassen LW. Immunologic mechanisms of alcoholic liver injury. Semin Liver Dis. 2004;24(3):273-87. .

Ultrasonographic imaging (USG), computed tomography (CT), or magnetic resonance imaging (MRI) are frequently and effectively used techniques to evaluate benign and malignant diseases of the liver, including in the diagnosis and grading of alcoholic liver disease77. Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001;344(7):495-500. , 88. Campbell MS, Reddy KR. Review article: the evolving role of liver biopsy. Aliment Pharmacol Ther. 2004;20(3):249-59. . However, histopathological examinations are more reliable in cases where a radiological examination is insufficient to guide diagnosis and treatment99. Niaz A. Response of interferon alone and with ribavirin in patients of chronic hepatitis C. J Coll Physicians Surg Pak. 2003;13(8):433-5. . On the other hand, liver biopsies such as tru-cut (sharp needle) biopsy and fine-needle aspiration cytology (FNAC) are the most commonly preferred and performed techniques to detect the grade and stage of certain liver diseases. Therefore, these methods are candidates for the “gold standard method”1010. Lam WW, Chu WC, Tse GM, Ma TK, Tang AP. Role of fine needle aspiration and tru cut biopsy in diagnosis of mucinous carcinoma of breast: from a radiologist’s perspective. Clin Imaging. 2006;30(1):6-10. , 1111. Li GP, Gong GQ, Wang XL, Chen Y, Cheng JM, Li CY. Fine needle aspirating and cutting is superior to Tru-cut core needle in liver biopsy. Hepatobiliary Pancreat Dis Int. 2013;12(5):508-11. . The role of liver biopsy in alcoholic liver disease is to provide accurate clinical data, facilitate diagnosis, and predict the severity, grade, and stage of the disease by using semi-quantitative tools33. Celli R, Zhang X. Pathology of alcoholic liver disease. J Clin Transl Hepatol. 2014;2(2):103-9. .

FNAC is a simple, rapid, less expensive, and relatively safe investigation, while tru-cut biopsy is more expensive and takes more time1212. Willard MD, Weeks BR, Johnson M. Fine-needle aspirate cytology suggesting hepatic lipidosis in four cats with infiltrative hepatic disease. J Feline Med Surg. 1999;1(4):215-20. . Additionally, FNAC causes less tissue damage and has fewer complications than tru-cut biopsy. Compared to FNAC, the risk of complications such as hemorrhage, tumor seeding, infection, fistula formation, bleeding, perforation, and pain can be encountered more in tru-cut biopsy1111. Li GP, Gong GQ, Wang XL, Chen Y, Cheng JM, Li CY. Fine needle aspirating and cutting is superior to Tru-cut core needle in liver biopsy. Hepatobiliary Pancreat Dis Int. 2013;12(5):508-11. . Despite its advantages, such as the high sensitivity and specificity rates and reducing the need for other biopsy techniques such as tru-cut, in some types of lesions, FNAC may not provide enough cellular details1313. Joudeh AA, Shareef SQ, Al-Abbadi MA. Fine-needle aspiration followed by core-needle biopsy in the same setting: modifying our approach. Acta Cytol. 2016;60(1):1-13. .

Considering the current literature, FNAC is generally used for lesions suspected of malignancy in the liver, not in benign lesions1414. Nasit JG, Patel V, Parikh B, Shah M, Davara K. Fine-needle aspiration cytology and biopsy in hepatic masses: a minimally invasive diagnostic approach. Clin Cancer Investig J. 2013;2:132-42. , 1515. Nazir RT, Sharif MA, Iqbal M, Amin MS. Diagnostic accuracy of fine needle aspiration cytology in hepatic tumours. J Coll Physicians Surg Pak. 2010;20(6):373-6. . Therefore, in this study, we aimed to compare the efficiency of USG-guided tru-cut biopsy and fine-needle aspiration cytology concerning some histological parameters such as inflammation, hepatocyte damage, congestion, and fatty change and intended to detect the sensitivity, specificity, positive/negative predictive values, and diagnostic accuracy of the two methods in an experimental alcoholic liver disease model.

METHODS

After the study was approved by the Local Ethics Committee of Animal Experiments of the Kafkas University (Ethical Approval Date 17.02.2016 and Number: 2016/053), thirty-six female Wistar albino rats, 4-6 months old and weighing 190 to 250g, were purchased from the Ataturk University Medical Experimental Research and Application Center and used in this study. Female rats are chosen for the study because they are more prone to alcoholic damage1616. Gao B, Bataller R. Alcoholic liver disease: pathogenesis and new therapeutic targets. Gastroenterology. 2011;141(5):1572-85. .

The rats were housed in an animal room maintained at a temperature of 22-25 °C, in 12-hours light periods, and were fed ad-libitum. Then, the rats were randomly divided into the following six experimental groups (n=6 per group):

Group 1: (1st control group) Nothing was done. The animals were only fed ad-libitum for 28 days (n=6).

Group 2: (2nd control group) Nothing was applied. The animals were only fed ad-libitum for 28 days, followed by tru-cut biopsy (n=6).

Group 3: (3rd control group) Nothing was applied. The animals were only fed ad-libitum for 28 days, followed by FNAC (n=6).

Group 4: Alcoholic liver disease was inducted by applying Ethanol (7 g/kg/day) + Water (50%) for 28 days (n=6).

Group 5: Alcoholic liver disease was inducted by applying Ethanol (7 g/kg/day) + Water (50%) for 28 days, followed by FNAC (n=6).

Group 6: Alcoholic liver disease was inducted by applying Ethanol (7 g/kg/day) + Water (50%) for 28 days, followed by tru-cut biopsy (n=6).

Ethanol was administered considering the time to create subchronic damage using the dosage modified per Bharrhan et al.’s study1717. Bharrhan S, Koul A, Chopra K, Rishi P. Catechin suppresses an array of signalling molecules and modulates alcohol-induced endotoxin mediated liver injury in a rat model. PLoS One. 2011;6(6):e20635. . At the end of the 28-days, the rats were not fed overnight. After applying the anesthesia protocol, the samples were taken by USG-guided tru-cut biopsy or FNAC. After the interventions, the rats were subjected to cervical vertebra dislocation according to ethical rules.

Imaging during FNAC

The samples were obtained by the FNAC technique following local anesthesia using a 20 cc injection syringe with 21G needle from the non-vascular area of the liver with the guide of an ultrasonography (USG) device (Toshiba Aplio XG).

Imaging during tru-cut biopsy

The samples were obtained by the tru-cut biopsy technique following local anesthesia using a 18G tru-cut needle from the liver tissue with the guidance of USG (Toshiba Aplio XG).

The harvested tru-cut biopsy and hepatectomy samples were fixed in 10% buffered formaldehyde solution for 24 hours for pathological examinations. They were dehydrated in graded alcohol series and embedded in paraffin wax. Then, four-μm thick sections of paraffin blocks were obtained and stained with hematoxylin & eosin (H&E). The sections were evaluated by light microscopy (Clinical Microscope BX46, Olympus, Japan). The cytological materials were also analyzed by light microscopy both as direct smear and thin-prep method, which is a cell replication method. Since direct smears revealed more diagnostic features than the thin-prep method during the microscopic evaluation, direct smear was used for cytology findings that constitute the main framework of the study. The hepatectomy materials, tru-cut biopsies, and FNAC preparations of all experimental groups were evaluated for histopathological assessments of the following parameters: congestion, inflammation, hepatocyte damage, and steatosis (fatty change).

Statistical Analysis

The sensitivity, specificity, positive and negative predictive values of FNAC and tru-cut biopsy in the diagnosis of liver lesions were determined using histopathological diagnoses of the liver tissues as the gold standard.

RESULTS

Per the histopathological evaluation, no histopathological changes were detected in Group 1 (1st control group) except for mild congestion ( Figure 1A ). Group 2 and Group 3 had similar histopathological properties to Group 1 in terms of hepatocyte damage, periportal inflammation, congestion, and changes in fatty parameters (no histopathological changes were detected except mild congestion). On the other hand, hepatocyte damage, periportal inflammation, congestion, and fatty changes were detected in the liver tissues of the ethanol-administrated group (Group 4) ( Figure 1B-C ).

FIGURE 1
THE HISTOPATHOLOGICAL MICROGRAPHS OF GROUP 1 AND 4.

A: Group 1, mild congestion (H&E, 200x); B: Group 4, periportal inflammation (H&E, 200x); C: Group 4, microvesicular steatosis and hepatocyte damage (H&E, 400x).


The sensitivity, specificity, diagnostic accuracy, positive and negative predictive values of the histopathological parameters (hepatocyte damage, inflammation, congestion, and fatty change) of Group 5 and Group 6 ( Figure 2A-B ) are shown in Table 1 and Table 2 .

FIGURE 2
THE HISTOPATHOLOGICAL MICROGRAPHS OF GROUP 5 AND 6.

A: Group 5, hepatocyte damage (H&E, 400x); B: Group 6, hepatocyte damage (H&E, 400x).


TABLE 1
THE SENSITIVITY, SPECIFICITY, POSITIVE AND NEGATIVE PREDICTIVE VALUES OF GROUP 5 (ALD WITH THE FNAC-APPLIED GROUP)

TABLE 2
THE SENSITIVITY, SPECIFICITY, POSITIVE AND NEGATIVE PREDICTIVE VALUES OF GROUP 6 (ALD WITH THE TRU-CUT-APPLIED GROUP)

The sensitivities of hepatocyte damage, inflammation, congestion, and changes in fatty parameters for FNAC were 33.3%, 80%, 0%, and 0%, respectively, while, the sensitivities of the same variables for the tru-cut biopsy were 66.7%, 40%, 100%, and 20%, respectively. On the other hand, the diagnostic accuracy of congestion was the same both for tru-cut and FNAC (100%). The diagnostic accuracies of tru-cut biopsy regarding fatty changes (33.3% vs. 16.7%) and hepatocyte damage (66.7% vs. 33.3%) were higher than those of FNAC, while the diagnostic accuracy of FNAC concerning inflammation (83.3% vs. 50%) was higher than the tru-cut biopsy method.

The positive predictive values of FNAC in terms of hepatocyte damage, inflammation, and congestion were 100%, whereas it was 0% regarding fatty changes. However, the positive predictive values of the tru-cut biopsy method were 100% for all histopathological parameters. On the other hand, the negative predictive values of hepatocyte and congestion of both techniques were 0%, while negative predictive values of inflammation (50% vs. 25%) and fatty changes (33.3% vs. 20%) were higher in the FNAC compared to the tru-cut biopsy method.

DISCUSSION

Only a few studies compare FNAC and tru-cut biopsy in non-tumoral liver diseases. In this study, we performed tru-cut biopsy and FNAC to rats with experimental alcoholic liver disease and observed that tru-cut biopsy had higher sensitivity and diagnostic accuracy concerning hepatocyte damage when compared to FNAC. However, positive predictive values were similar for both methods. For inflammation, FNAC had higher sensitivity, diagnostic accuracy, and negative predictive value than tru-cut biopsy. For congestion and changes in fatty parameters, it was detected that tru-cut biopsy had higher sensitivity, diagnostic accuracy, and positive predictive value.

For any hepatic disease, the radiological, serological (such as alpha-fetoprotein), and clinical findings, among others, are not precisely and reliably able to differentiate benign and malign lesions; these methods can only increase the accuracy of the diagnosis1414. Nasit JG, Patel V, Parikh B, Shah M, Davara K. Fine-needle aspiration cytology and biopsy in hepatic masses: a minimally invasive diagnostic approach. Clin Cancer Investig J. 2013;2:132-42. . At some point, liver biopsies become inevitable for the evaluation of patients and the management of the diseases1818. Gor N, Salem SB, Jakate S, Patel R, Shah N, Patil A. Histological adequacy of EUS-guided liver biopsy when using a 19-gauge non-Tru-Cut FNA needle. Gastrointest Endosc. 2014;79(1):170-2. . Most liver biopsies are applied under radiological guidance, and the choice of the biopsy needle depends on the radiologist. Naturally, the experience of the radiologist may influence management. This decision also depends on many variants including the size and location of the tumor, and the risk of possible complications1919. Stewart CJ, Coldewey J, Stewart IS. Comparison of fine needle aspiration cytology and needle core biopsy in the diagnosis of radiologically detected abdominal lesions. J Clin Pathol. 2002;55(2):93-7. . Currently, there are two commonly accepted and used techniques to obtain diagnostic material, namely, fine needle aspiration cytology (FNAC) and tru-cut biopsy. The FNAC technique usually provides a sample for cytological examination, whereas tru-cut biopsy primarily delivers a sample for histological assessment. Each method has different advantages and disadvantages, and both are considered safe1919. Stewart CJ, Coldewey J, Stewart IS. Comparison of fine needle aspiration cytology and needle core biopsy in the diagnosis of radiologically detected abdominal lesions. J Clin Pathol. 2002;55(2):93-7. . Therefore, the sensitivity and specificity rates of these two techniques should be available for choosing the appropriate one.

There have been adequate scientific data about both tru-cut biopsy and FNAC techniques in the literature reporting the advantages and complications, as well as the rates of sensitivity and specificity. Ding et al.2020. Ding W, He XJ. Fine needle aspiration cytology in the diagnosis of liver lesions. Hepatobiliary Pancreat Dis Int. 2004;3(1):90-2. performed a study with 46 hepatocellular carcinoma patients to distinguish primary and metastatic tumors and emphasized that FNAC is a useful technique. Li et al.1111. Li GP, Gong GQ, Wang XL, Chen Y, Cheng JM, Li CY. Fine needle aspirating and cutting is superior to Tru-cut core needle in liver biopsy. Hepatobiliary Pancreat Dis Int. 2013;12(5):508-11. performed a tru-cut biopsy and FNAC techniques with 18G and 21G needles, respectively, on 94 patients with unresectable malignant tumors, and reported that the 21G FNAC and 18G tru-cut biopsy procedures were substantially similar. However, the safety of the 21G FNAC was found superior to that of 18G tru-cut biopsy. Tissues obtained by either of these two techniques are sufficient for any pathological and molecular diagnosis. Another study performed by Kaçar Özkara et al.2121. Kaçar Özkara S, Ozöver Tuneli I. Fine needle aspiration cytopathology of liver masses: 101 cases with cyto-/histopathological analysis. Acta Cytol. 2013;57(4):332-6. in 2013 pointed out that FNAC had a high sensitivity rate, especially in hepatic neoplasia. However, they also stressed that combined cyto-histopathology is superior to FNAC.

Most of the related studies generally report that FNAC is a successful technique and can be used for the diagnosis of hepatic tumors. It was stated that FNAC is a suitable method to be used for open biopsy or when surgery is not possible2222. Barbhuiya M, Bhunia S, Kakkar M, Shrivastava B, Tiwari PK, Gupta S. Fine needle aspiration cytology of lesions of liver and gallbladder: an analysis of 400 consecutive aspirations. J Cytol. 2014;31(1):20-4. . Sattar et al.2323. Sattar A, Khan AM, Anjum S, Naqvi A. Role of ultrasound guided fine needle aspiration cytology in diagnosis of space occupying lesions of liver. J Ayub Med Coll Abbottabad. 2014;26(3):334-6. performed a study on 450 patients with focal hepatic lesions and determined that USG-guided FNAC was a rapid, safe, easy, and uncomplicated method for diagnosis. A comprehensive study2424. Reddy CV, Goud YG, Poornima R, Deshmane V, Madhusudhana BA, Gayathridevi M. Role of FNAC in hepatic lesions: risk of track metastases. South Asian J Cancer. 2015;4(1):35-7. performed in 2015 on 755 patients with malignant and benign hepatic lesions detected that the diagnostic accuracies of FNAC and tru-cut biopsy were in the range of 58.8%-98.9%. Additionally, no complication had been reported in this study. On the other hand, Nazir et al.1515. Nazir RT, Sharif MA, Iqbal M, Amin MS. Diagnostic accuracy of fine needle aspiration cytology in hepatic tumours. J Coll Physicians Surg Pak. 2010;20(6):373-6. detected a diagnostic accuracy and specificity between 95.2% and 100%. According to these authors, FNAC was a cheap, easy, and safe method. However, they claimed that tru-cut biopsy should be the gold-standard method.

In light of these findings, we observed that these tests were each superior in some aspects and equivalent regarding different features. We consider that the selection of the diagnostic method in alcoholic liver disease according to the histopathological parameters is a central point for a patient-based individualized approach. For instance, if the “inflammation” parameter is to be evaluated, FNAC should be preferred, while tru-cut biopsy should be at the forefront for the assessment of “fatty changes.” This way, it will be possible to make a more suitable selection of the biopsy methods in terms of patient comfort, complication risk, ease of application, and cost.

In conclusion, we think that FNAC can be an attractive alternative to the tru-cut biopsy method and applied in routine practice in the diagnosis of non-tumoral liver diseases. To get the best results, a combined approach of FNAC and tru-cut biopsy may also be used.

Study Limitation

This study has some limitations. First, the biopsy techniques could also be performed on other liver diseases such as hepatocellular carcinoma and/or cirrhosis, or any other hepatic illness in addition to alcoholic liver disease. Second, a prospective study on patients with hepatic diseases could yield better results. Third, clinical, radiological, and serological findings could be obtained and compared with the biopsy results. Lastly, we did not perform a detailed observation of the complications because we had cervical dislocation immediately after the procedures.

Acknowledgment

This study is funded by Kafkas University (Project number: 2016-TS-56).

REFERENCES

  • 1
    Osna NA, Donohue TM Jr, Kharbanda KK. Alcoholic liver disease: pathogenesis and current management. Alcohol Res. 2017;38(2):147-61.
  • 2
    Rehm J, Samokhvalov AV, Shield KD. Global burden of alcoholic liver diseases. J Hepatol. 2013;59(1):160-8.
  • 3
    Celli R, Zhang X. Pathology of alcoholic liver disease. J Clin Transl Hepatol. 2014;2(2):103-9.
  • 4
    Orman ES, Odena G, Bataller R. Alcoholic liver disease: pathogenesis, management, and novel targets for therapy. J Gastroenterol Hepatol. 2013;28(Suppl 1):77-84.
  • 5
    Albano E, Vidali M. Immune mechanisms in alcoholic liver disease. Genes Nutr. 2010;5(2):141-7.
  • 6
    Thiele GM, Freeman TL, Klassen LW. Immunologic mechanisms of alcoholic liver injury. Semin Liver Dis. 2004;24(3):273-87.
  • 7
    Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001;344(7):495-500.
  • 8
    Campbell MS, Reddy KR. Review article: the evolving role of liver biopsy. Aliment Pharmacol Ther. 2004;20(3):249-59.
  • 9
    Niaz A. Response of interferon alone and with ribavirin in patients of chronic hepatitis C. J Coll Physicians Surg Pak. 2003;13(8):433-5.
  • 10
    Lam WW, Chu WC, Tse GM, Ma TK, Tang AP. Role of fine needle aspiration and tru cut biopsy in diagnosis of mucinous carcinoma of breast: from a radiologist’s perspective. Clin Imaging. 2006;30(1):6-10.
  • 11
    Li GP, Gong GQ, Wang XL, Chen Y, Cheng JM, Li CY. Fine needle aspirating and cutting is superior to Tru-cut core needle in liver biopsy. Hepatobiliary Pancreat Dis Int. 2013;12(5):508-11.
  • 12
    Willard MD, Weeks BR, Johnson M. Fine-needle aspirate cytology suggesting hepatic lipidosis in four cats with infiltrative hepatic disease. J Feline Med Surg. 1999;1(4):215-20.
  • 13
    Joudeh AA, Shareef SQ, Al-Abbadi MA. Fine-needle aspiration followed by core-needle biopsy in the same setting: modifying our approach. Acta Cytol. 2016;60(1):1-13.
  • 14
    Nasit JG, Patel V, Parikh B, Shah M, Davara K. Fine-needle aspiration cytology and biopsy in hepatic masses: a minimally invasive diagnostic approach. Clin Cancer Investig J. 2013;2:132-42.
  • 15
    Nazir RT, Sharif MA, Iqbal M, Amin MS. Diagnostic accuracy of fine needle aspiration cytology in hepatic tumours. J Coll Physicians Surg Pak. 2010;20(6):373-6.
  • 16
    Gao B, Bataller R. Alcoholic liver disease: pathogenesis and new therapeutic targets. Gastroenterology. 2011;141(5):1572-85.
  • 17
    Bharrhan S, Koul A, Chopra K, Rishi P. Catechin suppresses an array of signalling molecules and modulates alcohol-induced endotoxin mediated liver injury in a rat model. PLoS One. 2011;6(6):e20635.
  • 18
    Gor N, Salem SB, Jakate S, Patel R, Shah N, Patil A. Histological adequacy of EUS-guided liver biopsy when using a 19-gauge non-Tru-Cut FNA needle. Gastrointest Endosc. 2014;79(1):170-2.
  • 19
    Stewart CJ, Coldewey J, Stewart IS. Comparison of fine needle aspiration cytology and needle core biopsy in the diagnosis of radiologically detected abdominal lesions. J Clin Pathol. 2002;55(2):93-7.
  • 20
    Ding W, He XJ. Fine needle aspiration cytology in the diagnosis of liver lesions. Hepatobiliary Pancreat Dis Int. 2004;3(1):90-2.
  • 21
    Kaçar Özkara S, Ozöver Tuneli I. Fine needle aspiration cytopathology of liver masses: 101 cases with cyto-/histopathological analysis. Acta Cytol. 2013;57(4):332-6.
  • 22
    Barbhuiya M, Bhunia S, Kakkar M, Shrivastava B, Tiwari PK, Gupta S. Fine needle aspiration cytology of lesions of liver and gallbladder: an analysis of 400 consecutive aspirations. J Cytol. 2014;31(1):20-4.
  • 23
    Sattar A, Khan AM, Anjum S, Naqvi A. Role of ultrasound guided fine needle aspiration cytology in diagnosis of space occupying lesions of liver. J Ayub Med Coll Abbottabad. 2014;26(3):334-6.
  • 24
    Reddy CV, Goud YG, Poornima R, Deshmane V, Madhusudhana BA, Gayathridevi M. Role of FNAC in hepatic lesions: risk of track metastases. South Asian J Cancer. 2015;4(1):35-7.

Publication Dates

  • Publication in this collection
    11 Sept 2020
  • Date of issue
    Aug 2020

History

  • Received
    26 Jan 2020
  • Accepted
    15 Mar 2020
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