Abstract
Background
To evaluate the safety and efficacy of ultrasound-guided (US-guided) omental biopsy in patients with liver cirrhosis and compare these with the noncirrhotic patients.
Methods
We retrospectively studied the US-guided omental biopsies (73 males, 14 females with mean age 52.71 ± 15.90 y) between January 2012 and December 2018. Patients with biopsy-proven liver cirrhosis (n = 31) who underwent omental biopsy were included in Group 1, and patients without any features of the chronic liver disease (n = 56) were included in Group 2. The technical success, diagnostic parameters, complications, imaging appearance, and histopathology spectrum were compared between the two groups. Also, univariate analysis was done to evaluate the association of a parameter with histopathology.
Results
The technical success, sample adequacy, diagnostic accuracy of Group 1 were 100%, 96.77%, and 96.77%, respectively, and for Group 2, these were 100%, 98.21%, and 98.21%, respectively. The sensitivity, specificity, positive predictive value, negative predictive value of Group 1 were 95%, 100%, 100%, 91.67%, respectively, and for Group 2, these were 97.92%, 100%, 100%, 88.89%, respectively. There was one complication of abdominal wall hematoma in Group 1 (3.2%), which was managed conservatively. Smudged imaging appearance and nonspecific inflammation on histopathology were more common in Group 1, and there was a significant association of increased omental thickening with specific pathology in Group 1.
Conclusion
US-guided omental biopsy in patients with liver cirrhosis is safe and effective with comparable results to noncirrhotic patients.
Keywords: omentum, ulrasound, biopsy, cirrhosis
Abbreviations: CT, Computed Tomography; CTP, Child–Turcotte–Pugh; DA, Diagnostic Accuracy; HPE, Histopathology Examination; INR, International Normalized Ratio; NASH, Nonalcoholic Steatohepatitis; NPV, Negative Predictive Value; PPV, Positive Predictive Value; US, Ultrasound
Omental and mesenteric thickening is frequently seen on imaging in patients with chronic liver disease.1 It is difficult to differentiate the benign (e.g., granuloma, infection) and malignant etiologies (e.g., metastasis or primary malignancy) of thickening on imaging alone.2,22 So, biopsy plays an essential role, as the management varies with the pathological diagnosis.
Anterior peritoneal location and easy visibility make percutaneous ultrasound-guided (US-guided) omental biopsy feasible. It can be performed as a daycare procedure under local anesthesia without significant complications. These advantages make US-guided biopsy a preferable option compared to the conventional laparoscopic or laparotomy route.22
There are several studies on the risks, complications, and outcomes of various surgeries,3,4 liver biopsy,5 and central venous cannulation6 in patients with chronic liver disease. Similarly, there are studies published on omental biopsies in patients without chronic liver disease. However, we could not find any study describing the safety and efficacy of omental biopsies in patients with chronic liver disease.
In this study, we retrospectively evaluated the safety and efficacy of omental biopsies in patients with liver cirrhosis and compared these with the noncirrhotic group omental biopsies performed in our hospital. Also, we compared the histopathology spectrum and imaging appearance of omental thickening between two groups.
Materials and methods
Study Population
In this single-center retrospective study, data of all patients, who underwent omental biopsy from January 2012 to December 2018, were evaluated after proper institutional review board and ethical committee approval. A total of 87 patients who underwent percutaneous US-guided omental biopsy were assigned to one of the two groups: Group 1 (patient with cirrhosis) – were those with biopsy-proven liver cirrhosis, and Group 2 (patients without cirrhosis) – were those without any features of chronic liver disease on imaging/transient elastography/serological testing. Patients with refractory coagulation parameters were excluded from the study. The study population demographic characteristics are presented in Table 1. In total, 33 patients had a history of diffuse abdominal pain, and 25 had fever of unknown origin. And, 10 patients had a history of primary malignancy (five – ovarian, four – colonic, one – gastric). Furthermore, 19 patients had incidental omental thickening on routine surveillance imaging for hepatocellular carcinoma (HCC) in Group 1. The etiology of cirrhosis in Group 1 was cryptogenic in 7 (22.5%), ethanol related in 17 (54.8%), Hepatitis B related in two (6.4%), Hepatitis C related in two (6.4%), and non-alcoholic steatohepatitis (NASH) related in three (9.6%) patients. Child–Turcotte–Pugh classes were A in six (19.3%), B in 13 (41.9%), and C in 12 (38.7%) patients.
Table 1.
Demographic, Imaging, Histopathology, and Sample Characteristics of Study Population.
| Variable | Group 1 (n = 31) | Group 2 (n = 56) | P-value | |
|---|---|---|---|---|
| Age (years) | Mean ± SD | 51.03 ± 13.28 | 53.64 ± 17.22 | 0.467 |
| Gender | Males | 26 (83.9%) | 47 (83.9%) | 0.994 |
| Females | 5 (16.1%) | 9 (16.1%) | ||
| INR | Mean ± SD | 1.67 ± 0.77 | 1.175 ± 0.17 | 0.001 |
| Platelet count (× 109/L) | Median (Range) | 150 (22–459) | 308 (42–850) | 0.001 |
| Ascites | Present | 28 (90.3%) | 51 (91.1%) | 0.908 |
| Absent | 3 (9.7%) | 5 (8.9%) | ||
| Granuloma-tuberculosis | Type 1 | 1 | 3 | 0.353 |
| Type 2 | 12 | 7 | 0.0099 | |
| Type 3 | 0 | 0 | – | |
| Type 4 | 0 | 5 | – | |
| Total | 13 (41.9%) | 15 (26.7%) | 0.147 | |
| Malignant etiology | Type 1 | 1 | 12 | 0.257 |
| Type 2 | 6 | 15 | 0.0526 | |
| Type 3 | 0 | 3 | - | |
| Type 4 | 0 | 3 | - | |
| Total | 7 (22.6%) | 33 (58.9%) | 0.0011 | |
| Nonspecific inflammation | Type 1 | 1 | 0 | - |
| Type 2 | 10 | 7 | 0.811 | |
| Type 3 | 0 | 0 | - | |
| Type 4 | 0 | 1 | - | |
| Total | 11 (35.4%) | 8 (14.2%) | 0.0219 | |
| Omental thickness on imaging (cm) | Mean ± SD | 3.2 ± 1.008 | 3.59 ± 1.58 | 0.22 |
| Sample size (cm) | Median (range) | 1.055 (0.6–3) | 1.09 (0.7–3.5) | 0.573 |
| Sample adequacy | n (%) | 30 (96.7%) | 55 (98.2%) | 0.667 |
| Complications | n (%) | 1 (3.2%) | 0 | |
INR = international normalized ratio.
US-guided Omental Biopsy Procedure
Imaging (for a safe path without bowel or vessels) and coagulation parameter evaluation of patients was done. Therapeutic ascitic tap (up to 4–5 L) was done in patients with massive ascites, and correction of coagulation parameters was done in patients with platelet count < 50,000/μl and INR > 1.5 according to the recommendations of DeAngelis et al.7 Two cores were obtained using an automated (BARD Max-Core) or semi-automated biopsy gun (BARD MISSION), consisting of an 18-gauge biopsy needle (Figure 1, Figure 2) and 1.8-cm sample notch (BARD Peripheral Vascular Inc., Tempe, Arizona, USA). The patients were monitored in the daycare ward for 6 h, and screening US was done at 30 min after the procedure and prior to discharge.
Figure 1.
US- guided biopsy of in a 51-year-old man with history of fever for 3 months. HPE showed granuloma suggestive of tuberculosis. Arrow heads represent the biopsy needle, and arrows denote omental thickening.
Figure 2.
US- guided biopsy of in a 63-year-old woman with history of abdominal discomfort and weight loss. HPE showed pseudomyxoma peritonei. Arrow heads represent the biopsy needle, and arrows denote omental thickening.
Omental Thickening Types and Histopathological Examination (HPE) Categories
The omental thickening is categorized into four types (Figure 3) depending on the appearance on imaging (CT scan) according to Cooper et al.8: type 1 – omental caking: replacement of normal fat by large solid masses”, type 2 – smudged appearance: small nodules and finely infiltrated fat”, type 3 – cystic masses with lower attenuation ”, and type 4“ – multiple discrete nodules”. The patients in both groups were also categorized based on the histopathological examination (HPE) into those with specific pathology (granulomatous pathology and malignant pathology, subcategories) and those with non-specific inflammation for subgroup analysis.
Figure 3.
Axial CECT images showing various imaging types of omental thickening. (a) Omental caking. (b) Smudged appearance. (c) Cystic masses. (d) Multiple discrete nodules (arrows denote omental thickening).
Technical Success and Follow-up
Technical success is defined as the completion of the US-guided biopsy and obtaining at least two cores. A review of HIS records was performed to assess for any complications after discharge. Society of Interventional Radiology (SIR) standards9 were used to define and grade the complications. Early complications were defined as those occurring within 24 h, and delayed, those occurring more than 24 h. The patients were followed-up for confirmation of diagnosis based on open surgical biopsy or treatment response.
Statistical Analysis
The Mann–Whitney U-test or the independent t-test was used for continuous data and Fisher's exact probability test for categorical data. Histopathology spectrum and imaging appearance of omental thickening were correlated using the chi-square test. Univariate analysis was done to evaluate any independent association between various parameters and the histopathology outcome using SPSS v.23.0 (IBM Corp., Armonk, NY, USA). P-values less than 0.05 were considered statistically significant. Sensitivity, specificity, positive and negative predictive values, and diagnostic accuracy were calculated using a 95% confidence interval.
Results
The two groups were comparable in the demographic characteristics and the presence of ascites with a statistically significant difference in the preprocedural platelet count and INR levels (Table 1). The US-guided omental biopsy was technically successful in all patients (100%) in our study. Among the 10 patients with a history of primary tumor, eight had a metastatic tumor on histopathology and two had a new primary tumor. Among the 19 patients in Group 1 with incidental omental thickening, eight patients had nonspecific inflammation, eight had granulomatous pathology, and three had malignant pathology. Two patients underwent repeat biopsies due to inadequate sample size in the first biopsy. The final histopathology spectrum of both groups is given in Table 1.
The omental biopsy findings were confirmed by response to antitubercular therapy in 28 patients, and response to chemotherapy in 40 patients. Among the patients with non-specific inflammation, three in Group 1 and eight in Group 2 underwent laparoscopic biopsy. Eight patients had a concordant diagnosis, with discordant diagnosis in three (one in each group had tuberculosis (TB) and one in Group 2 had malignancy). Five cirrhotic patients with nonspecific inflammation showed resolution of omental thickening on follow-up imaging after 1 month. The overall sensitivity, specificity, positive predictive value, negative predictive value, and diagnostic accuracy were 97.1%, 100%, 100%, 89.4%, and 97.7%, respectively, with comparable values in the two groups (Table 2).
Table 2.
Comparison of Diagnostic Parameters Between Two Groups.
| Parameter | Group 1 | Group 2 |
|---|---|---|
| Sensitivity (95% CI) | 95% (75.1–99.8%) | 97.9% (88.9–99.9%) |
| Specificity (95% CI) | 100% (71.5–100%) | 100% (63.0–100%) |
| Positive predictive value | 100% | 100% |
| Negative predictive value (95% CI) | 91.6% (61.9–98.6%) | 88.8% (53.4–98.2%) |
| Diagnostic accuracy (95% CI) | 96.7% (83.3–99.9%) | 98.2% (90.4–99.9%) |
On univariate analysis, significant association of increased omental thickening with specific pathology was seen in Group 1 (Table 3). On intragroup comparison of various imaging types, significant association of type 4 with granulomatous pathology (p = 0.033) and type 2 with nonspecific inflammation (p = 0.0289) was seen in Group 2. On intergroup comparison of the three subcategories, we found type 2 imaging pattern was associated with granulomatous pathology in Group 1. Overall, type 2 imaging pattern was significantly more common in Group 1 (p = 0.00029), and in HPE, malignant pathology was more common in Group 2 and nonspecific inflammation in Group 1 (Table 1).
Table 3.
Univariate Analysis of Different Variables in Both Groups.
| Group | Variable | Specific pathology (68) | Nonspecific inflammation (19) | P value |
|---|---|---|---|---|
| Group 1 | Sample size (cm) | 1.164 (0.93–3.0) | 0.947 (0.6–2.81) | 0.27 |
| Omental thickness (cm) | 3.72 ± 0.79 | 2.78 ± 0.98 | 0.007 | |
| Albumin (g/dL) | 3.15 ± 0.82 | 2.61 ± 0.71 | 0.061 | |
| Bilirubin (mg/dL) | 2.72 (0.2–11.9) | 2.66 (0.3–10.5) | 0.952 | |
| CTP score | 9.0 ± 2.96 | 9.12 ± 2.17 | 0.899 | |
| Spleen size (cm) | 13.3 (8.7–18.5) | 14.4 (10.8–18.9) | 0.255 | |
| Varices present | 14 | 9 | 0.675 | |
| Group 2 | Sample size (cm) | 1.26 (0.83–2.97) | 0.92 (0.7–3.5) | 0.19 |
| Omental thickness (cm) | 3.69 ± 1.61 | 3.15 ± 1.45 | 0.341 |
CTP = Child–Turcotte–Pugh.
There was one early complication of abdominal wall hematoma. The patient had a platelet count of 138 × 109/L and INR of 1.56 before the procedure. His CTP score was 11, and he had moderate ascites. The CT angiogram revealed no contrast extravasation, and the patient was managed conservatively. On median follow-up of 1.3 years (1 month–2.7 years), there were no delayed complications after discharge, and no evidence of abdominal wall tumoral seeding was seen in the follow-up scans.
Discussion
Portal hypertension, hypoalbuminemia, and increased aldosterone levels are considered as the causes of mesenteric/omental edema in cirrhosis. With the increase in severity, the edema changes in appearance from focal infiltrative to diffuse mass-like appearance. This appearance can mimic benign or malignant pathology, which cannot be differentiated without a tissue diagnosis.1,22
The diagnostic parameters of image-guided omental biopsy in noncirrhotic population was variably reported in literature10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22: sensitivity (75–95.5%), specificity (86–100%), PPV (100%), NPV (50–78.3%), DA (84%–100%), and sample adequacy (85.7%–100%). Our sensitivity (95%), specificity (100%), PPV (100%), NPV (91.6%), DA (96.7%), and sample adequacy (96.7%) in the cirrhotic group are comparable with the noncirrhotic group in our study, as well as with the published literature. A more detailed summary of studies on image-guided omental biopsy is presented in Table 4.
Table 4.
Summary of the Studies Published on Image-guided Omental Biopsy.
| Parameter | Pombo et al. (11), 1997 | Gottlieb et al, (12), 1998 | Kim et al. (13), 2000 | Spencer et al. (14), 2001 | Ho et al. (15), 2003 | Vardareli et al. (16), 2004 | Hewitt et al. (17), 2005 | Souza et al. (18), 2009 | Govindarajan et al. (19) 2010 | Lee et al. (20), 2011 | Wang et al. (21), 2013 | Hill et al. (22), 2017 | Vadvala et al. (23), 2017 | Present study 2018 |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Patients | n = 25 | n = 52, extravisceral masses in peritoneal cavityOnly FNAC – 26Only biopsy – 12Both FNAC and biopsy – 16 | n = 27 | n = 35, all patients with known or suspected (complex pelvic masses) malignancy | n = 23 | n = 19, all were tuberculous peritonitis patients | n = 12, all were carcinoma breast patients | n = 111 | n = 173 | n = 45 | n = 153 | n = 181 | n = 18694 – omental biopsies88 – mesenteric biopsies | n = 87 |
| Guidance | CT – 25 | USG – 52 | USG – 27 | CT – 31USG – 4 | USG – 23 | CT – 8USG – 11 | CT – 9USG – 3 | CT – 91USG – 20 | USG – 173 | USG – 45 | USG – 153 | CT – 132USG – 49 | CT – 172USG – 14 | USG – 87 |
| Sample adequacy | 96% | 96.15% | 100% | 92% | 91.3% | 94.74% | 85.7% | 89% | 98% | 97.7% | 91.5% | 100% | 98.92% | 97.7% |
| Histopathology spectrum | 19 (76%) – malignant (metastatic)6 (24%) – benign (tuberculosis – 5, actinomycosis – 1) | 37 (71.1%) – malignant2 (3.8%) – abscesses1 (1.9%) – hemangioma1 (1.9%) – fibrous tissue/scar9 (17.3%) – no specific pathology | 15 (55.5%) – malignant8 (29.6%) – tuberculosis4 (14.8%) – chronic granulomatous inflammation | 27 (77.1%) – metastatic with definite primary7 (20%) – poorly differentiated carcinoma with peritoneal or ovarian origin1 (2.8%) – cecal carcinoma | 19 (82.6%) – malignant1 (4.3%) – fibrosis1 (4.3%) – benign lymph node1 (4.3%) – chronic inflammation | 19 (100%) – tuberculosis | 3 (25%) – metastatic carcinoma breast9 (75%) – new primary mullerian tumor | 83 (75%) – malignant4 (3.6%) – suspicious of malignancy8 (7%) – benign results4 (3.6%) – atypical cells | 82 (47%) – malignant58 (34%) – granulomatous29 (16.7%) – nonspecific pathology | 17(37.7%) – malignant12 (26.6%) – tuberculosis15 (33.3%) – nonspecific inflammation | 85 (55.5%) – malignant49 (32.0%) – tuberculosis8 (5.2%) – chronic peritoneal infections | 166 (92%) – malignant15 (8%) – benign13 (7.1%) – granulomatous1 (0.5%) – Erdheim–Chester1 (0.5%) – fat necrosis | 77 (81.9%) – malignant15 (15.9%) – non-neoplastic | Cirrhotic group (n = 31):13 (41.9%) – granuloma7 (22.5%) – malignant11 (35.4%) – nonspecific inflammationNoncirrhotic group (n = 56):15 (26.78%) – granuloma33 (58.9%) – malignant8 (14.2%) – nonspecific inflammation |
| Complications | 0 | 0 | 24 patients developed transient bleeding, which stopped spontaneously. | 0 | 2 complications (8.69%) – 1 mesenteric hematoma and 1 abdominal wall cellulitis | 0 | 0 | 3 minor complications (2.7%)1 – severe pain1 – hypotension during procedure1 – small hematoma anterior to mass | 0 | 0 | 2 (1.3%)- bleed, which stopped with transducer pressure | 0 | No complications in omental biopsy group | Bleed – 1 (1.12%) conservatively managed |
| Sensitivity, specificity, PPV, NPV, DA | Sensitivity – 89.5%, specificity – 100%, DA – 92% | Sensitivity – 93%, specificity – 100%, DA – 94% | DA – 100% | Sensitivity – 95%, specificity – 100% | Sensitivity – 93%, specificity – 86%, NPV – 50% | Sensitivity: 75–90% specificity: 83–100%, DA – 84%<! – Para Run – on – > | DA – 92.8% | Sensitivity – 99%, PPV – 100%, DA – 99% | Sensitivity – 95.5%, specificity – 100%, PPV – 100%, NPV – 50% | Sensitivity – 97.1%, specificity – 100%, PPV – 100%, NPV – 89.4%, DA – 97.7% |
CT, computed tomography; DA, diagnostic accuracy; FNAC, fine needle aspiration cytology; NPV, negative predictive value; PPV, positive predictive value; US, ultrasound.
The complication rates after omental biopsies were reported from 0 to 8.69% in various studies.10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22 We had one complication of abdominal wall hematoma in Group 1 (3.2%) and none in Group 2. The preprocedural uncorrected platelet counts and INR were significantly different between the two groups. However, the complication rate in the cirrhotic group is within the threshold suggested by “ACR–SIR–SPR Practice Parameter for the Performance of Image-Guided Percutaneous Needle Biopsy.'23
We found a significant number of patients with omental thickening in the cirrhotic group to be having nonspecific inflammation, that is, a spectrum that is different from the noncirrhotic population. On univariate analysis, we found the omental thickness to be significantly higher in cirrhotic patients with a specific pathology (3.72 ± 0.79 cm) than those with nonspecific inflammation (2.78 ± 0.98 cm). Although the albumin levels in the cirrhotic patients with nonspecific inflammation were lower, there was no statistically significant difference. This could be due to the relatively small sample size.
Our study has certain limitations like single-center, retrospective nature, and smaller sample size. Another limitation is the noninclusion of an open surgical biopsy for all patients. This was not feasible as US-guided omental biopsy is proven to have high specificity and PPV. Also, open surgical biopsy is associated with significant morbidity and mortality in cirrhotic patients. Only patients with a negative result and high suspicion or persistent thickening on follow-up imaging underwent open laparoscopic biopsy.
In conclusion, US-guided biopsy of the omentum in cirrhotics is an effective method with an acceptable complication rate after correction of coagulation parameters. The histopathology spectrum of omental thickening is significantly different between cirrhotic and noncirrhotic population. Further larger prospective studies are required to evaluate the causes of differences in the spectrum.
Main Points
This is the first study on the safety and efficacy of omental biopsies in cirrhotic patients.
US-guided biopsy of the omentum in cirrhotics is an effective method with an acceptable complication rate after correction of coagulation parameters.
The histopathology spectrum of omental thickening is significantly different between cirrhotic and noncirrhotic population.
Conflicts of interest
The authors have none to declare.
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.jceh.2019.10.003.
Appendix A. Supplementary data
The following is the supplementary data to this article:
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