Abstract
Background:
Guidelines recommend multiphasic computed tomography (CT) and/or contrast-enhanced magnetic resonance imaging (MRI) for the detection of hepatocellular carcinoma. The objectives of the study were to compare diagnostic parameters of non-contrast MRI against multiphase CT for diagnostic of hepatocellular carcinoma in patients who at risk of liver cancer considering Asia–Pacific clinical practice guidelines as the reference standard.
Methods:
Medical records of patients with chronic hepatic disease or have suspected liver cancer in surveillance of fewer than 100 days and underwent multiphasic CT, gadoxetic acid-enhanced MRI, and liver biopsy for diagnosis of liver cancer were included in analysis. Enhancement during the arterial phase and wash-out during a delayed phase or portal-venous considered as hepatocellular carcinoma in the multiphase CT. Mild-to-moderate hypersensitivity in imaging, presence of fat on out-of-phase imaging, non-enhancing capsule(s), mosaic appearance, hemorrhagic content, and/or nodule-in-nodule considered as hepatocellular carcinoma in MRI. Asia–Pacific clinical practice guidelines considered for biopsy/histopathology for detection of hepatocellular carcinoma.
Results:
For detection of hepatocellular carcinoma, non-contrast MRI had higher sensitivity (0.843 vs. 0.762, P < .001, q = 3.919) and accuracy (0.755 vs. 0.571, P < .001, q = 3.362) than the multiphase CT. While specificity was the same (0.864 vs. 0.809, P < .001, q = 2.584). Non-contrast MRI had 0-0.91 diagnostic confidence and multiphase CT had 0.49-0.81 diagnostic confidence for the detection of hepatocellular carcinoma.
Conclusions:
Non-contrast MRI easily facilitates the decision of chemotherapy and/or radiotherapy than multiphase CT in hepatocellular carcinoma.
Keywords: Asia–Pacific clinical practice guidelines, biopsy, computed tomography, hepatocellular carcinoma, liver cancer, magnetic resonance imaging
INTRODUCTION
Hepatocellular carcinoma is diagnosed by imaging modalities.1 Current guidelines recommend multiphasic computed tomography (CT) and/or contrast-enhanced magnetic resonance imaging (MRI) for diagnosis of liver cancer.2-7 However, there are chances of false-negative results1 which are corrected by alternative imaging methods, imaging modality with contrast-agent, or biopsies.2,3,7 Liver cirrhosis, blood flow redistribution, and hepatic parenchymal distortion may make false-positive results in these imaging methods,1 which can be corrected by contrast (gadoxetic acid)-enhanced MRI.8 According to these guidelines, CT, MRI, contrast-enhanced CT, biopsies, and contrast-enhanced MRI are required for the evaluation of hepatocellular carcinoma in suspected liver cancer patients.2-7 This method of diagnosis is very costly.1 Therefore, there is a need for single, non-invasive, and cost-effective diagnostic methods for the assessment of hepatocellular carcinoma.
The objectives of the retrospective study were to compare diagnostic parameters of non-contrast MRI against multiphase CT for the diagnostic of hepatocellular carcinoma in patients who at risk of liver cancer using the results of full-sequence gadoxetic acid-enhanced MRI and liver biopsy/histopathology (as per Asia–Pacific clinical practice guidelines for hepatocellular carcinoma) as the reference standard.
MATERIALS AND METHODS
Ethics Approval and Consent to Participate
The designed protocol (CHW/CL/15/2020 dated 26 February 2020) of the established study was approved by the radiology review board of the institute. The study reporting adheres to the strengthening the reporting of observational studies in epidemiology (STROBE) statement: cross-sectional studies, the law of the country, and the 2008V of Declarations of Helsinki. All the enrolled patients or their relatives (legally authorized person) signed an informed consent form regarding diagnosis, biopsies (if required), and the publication of the study in all formats of the publication including personal data and images irrespective of time and language during hospitalization.
Study Population
From 1 December 2017 to 14 September 2019, the study retrospectively searched medical records of patients with the chronic hepatic disease who underwent contrast (gadoxetic acid)-enhanced MRI and liver biopsy to detect liver cancer which was found by multiphasic CT or have suspected liver cancer in surveillance of fewer than 100 days while attending at the parent hospital and the referring hospitals. The study found 355 such records of patients. Among them 103 patients treated by chemotherapy and/or radiotherapy and not performed biopsies (if required). Complete medical records of 51 patients were not available. Therefore, data of these patients were not considered for analysis. A total of 248 nodules of 201 patients were included in the study.
Multiphasic CT
All examinations performed by a multidetector CT scanner (SOMATOM Sensation 64, Siemens Healthineers, Forchheim, Germany) with 2-5 mm a reconstruction thickness, 120-130 kV, and 360-365 mA. Examinations included unenhanced late hepatic arterial (25-40 s), portal venous (70-95 s), and delayed (175-185 s) phases. 1.75 mL/kg, 300 mg/mL concentrated Iodine (not exceeding 150 mL) was injected by a power injector (OptiVantage®, Guerbet, Villepinte, France) at 3.5-4 mL/s for contrast-enhanced images.1 Images performed by a radiologist (at least 7 years of experience in hepatic imaging) of institutes.
Image analysis of multiphase CT
An enhancement during the arterial phase (Figure 1) and wash-out during portal-venous (Figure 2) or delayed phase (Figure 3) is considered as hepatocellular carcinoma. Nodules with none of these characters are considered benign nodules.1 Images analyzed by radiologists (at least 7 years of experience in hepatic imaging) of institutes.
Figure 1.
The multiphase computed tomography of hepatitis B positive 49-years-old man. The arrow indicates 1.7 cm enhancement during the arterial phase in the seventh segment of the liver.
Figure 2.
The multiphase computed tomography of hepatitis B positive 49-years-old man. The arrow indicates a 1.1 cm wash-out during portal-venous.
Figure 3.
The multiphase computed tomography of hepatitis B positive 51-years-old man. The image is wash-out during the delayed phase.
MRI Technique
MRI examinations performed by a 3.0 T MRI scanner (Skyra, Siemens Healthineers, Forchheim, Germany). 0.1 mL/kg gadoxetic acid injected by a power injector and hepatobiliary phase imaging obtained after 20 min of injection. T1-weighted imaging (T1WI), T2-weighted imaging (T2WI), diffusion-weighted imaging (DWI), out-of-phase imaging, and hepatobiliary phase imaging are derived for diagnosis purposes.1 Images performed by radiologists (at least 7 years of experience in hepatic imaging) of institutes.
Image Analysis of MRI
Mild-to-moderate hypersensitivity on T2WI (Figure 4), hyperintensity on DWI (Figure 5), hyperintensity on hepatobiliary phase imaging (Figure 6), fat content on out-of-phase imaging, hemorrhagic content, mosaic appearance, nodule-in-nodule, and/or non-enhancing capsule(s) was considered as hepatocellular carcinoma. Nodules with none of these characters are considered benign nodules.9 Images analyzed by radiologists (at least 7 years of experience in hepatic imaging) of institutes.
Figure 4.
Magnetic resonance imaging (T2WI) of hepatitis B positive 50-years-old man. The arrow indicates mild hypersensitivity.
Figure 5.
Diffusion-weighted magnetic resonance imaging of hepatitis B positive 50-years-old man. The arrow indicates hyperintensity.
Figure 6.
Hepatobiliary phase magnetic resonance imaging in 51-years-old women with cirrhosis other than hepatitis B or C. The arrow indicates hyperintensity.
Full-Sequence Gadoxetic Acid-Enhanced MRI
After at least 2 weeks of non-contrast MRI and the multiphase CT imaging, a full-sequence gadoxetic acid-enhanced MRI was performed by the same radiologists and T1WI, T2WI, DWI, out-of-phase, and hepatobiliary phase images derived for diagnosis purposes.1 Also, diagnosis made as per the above-mentioned criteria of hepatocellular carcinoma. Images analyzed by radiologists (at least 7 years of experience in hepatic imaging) of institutes.
Liver Biopsy/Histopathology
The results of full-sequence gadoxetic acid-enhanced MRI were confirmed by liver biopsy followed by histopathology for hepatocellular carcinomas and benign nodules as per Asia–Pacific clinical practice guidelines for hepatocellular carcinoma.3
Diagnostic Performance
The ratio of the sum of true positive hepatocellular carcinoma present and true negative hepatocellular carcinoma absent (benign nodule present) to nodules studied is considered as sensitivity. The ratio of numbers of true positive hepatocellular carcinoma present by imaging modality to positive hepatocellular carcinoma detected by Asia–Pacific clinical practice guidelines for hepatocellular carcinoma considered as specificity and the ratio of numbers of true negative hepatocellular carcinoma absent (benign nodule present) by imaging modality to negative hepatocellular carcinoma detected by Asia–Pacific clinical practice guidelines for hepatocellular carcinoma considered as accuracy.
Clinical Significance
Clinical significance evaluated by detecting beneficial scores for hepatocellular carcinoma as per Eq. 1:
 |
True positive hepatocellular carcinoma: Hepatocellular carcinoma detected by imaging modality and confirmed by Asia–Pacific clinical practice guidelines for hepatocellular carcinoma.
False-positive hepatocellular carcinoma: Hepatocellular carcinoma detected by imaging modality but did not confirm by Asia–Pacific clinical practice guidelines for hepatocellular carcinoma.
Statistical Analysis
The Statistical Package for the Social Sciences (SPSS) version 25 (IBM Corp.; Armonk, NY, USA) was used for statistical analysis purposes. The Chi-square independence test was performed for categorical variables and 1-way analysis of variance following Tukey’s test (considering critical value [q] > significant) performed for continuous variables.1 All the results considered significant at a 95% CI.
RESULTS
Demographical and Clinical Characteristics of Patients
A total of 139 (69%) male and 62 (31%) female patients with a mean age of 55.45 ± 11.45 years were included in the analysis. Among enrolled patients, 161 (81%) patients were reported hepatitis B positive. The demographic and clinical conditions of the patients at the time of admission are reported in Table 1.
Table 1.
Demographical and Clinical Characteristics of Patients at the Time of Admission
| Characteristics | Population | |
|---|---|---|
| Patients | 201 | |
| Nodules studied | 248 | |
| Age (years) | Minimum | 35 |
| Maximum | 78 | |
| Mean ± SD | 55.45 ± 11.45 | |
| Gender | Male | 139 (69) |
| Female | 62 (31) | |
| Nodule size (cm) | 1.32 ± 1.22 | |
| Alcoholic | Current | 84 (42) |
| Previous | 52 (26) | |
| None | 65 (32) | |
| Hepatitis B positive | 161 (81) | |
| Hepatitis C positive | 11 (5) | |
| Hepatitis B and C positive | 2 (1) | |
| Cirrhosis other than hepatitis B and/or C | 27 (13) | |
| Alpha fetoprotein (ng/mL) | 51.12 ± 15.12 | |
| Protein-induced by vitamin K absence (ng/mL) | 32.11 ± 6.15 | |
Categorial data demonstrate as frequency (percentage) and continuous data demonstrate mean ± SD.
Multiphasic CT
Out of 248 nodules, enhancement during the arterial phase on 115 nodules, wash-out during portal-venous on 63 nodules, wash-out during delayed phase on 21 nodules, and 49 cases did not report any types of characteristics.
MRI Analysis
Among 248 cases for nodules, mild-to-moderate hypersensitivity on T2WI reported in 65 cases, hyperintensity on DWI reported in 58 cases, hyperintensity on hepatobiliary phase imaging reported in 54 cases, fat content on out-of-phase imaging reported in 11 cases, non-enhancing capsule(s) reported on 3 cases, hemorrhagic content reported on 3 cases, mosaic appearance reported on 2 cases, nodule-in-nodule reported on 3 cases, and 49 cases did not report any types of characteristics.
Reference Standard
Out of 248 nodules, full-sequence gadoxetic acid-enhanced MRI and biopsy/histopathology as per Asia–Pacific clinical practice guidelines for hepatocellular carcinoma reported hepatocellular carcinoma in 199 nodules and a benign nodule on 49 nodules. The study flow chart of the retrospective analyses is presented in Figure 7.
Figure 7.
Study flow diagram.
Diagnostic Performance
Non-contrast MRI detected benign nodules exactly as those detected by full-sequence gadoxetic acid-enhanced MRI and biopsy/histopathology as per Asia–Pacific clinical practice guidelines for hepatocellular carcinoma (P = .192). While there were differences in diagnostic parameters between imaging modalities and full-sequence gadoxetic acid-enhanced MRI and biopsy/histopathology as per Asia–Pacific clinical practice guidelines for hepatocellular carcinoma (Table 2).
Table 2.
Diagnostic Parameters of Imaging Modalities
| Parameters | Reference | Non-Contrast Magnetic Resonance Imaging | The Computed Tomography | Comparisons Between Non-Contrast Magnetic Resonance Imaging and the Computed Tomography | ||
|---|---|---|---|---|---|---|
| Nodules studied | 248 | 248 | *P Value | 248 | *P Value | P Value |
| True positive hepatocellular carcinoma present | 199 (80) | 172 (69) | .007 | 161 (65) | .001 | .339 |
| True negative hepatocellular carcinoma absent (benign nodule present) | 49 (20) | 37 (15)** | .192 | 28 (11) | .013 | .287 |
| False positive hepatocellular carcinoma present | 0 (0) | 27 (11) | <.0001 | 38 (15) | <.0001 | .183 |
| False negative hepatocellular carcinoma absent (benign nodule present) | 0 (0) | 12 (5) | .001 | 21 (9) | <.0001 | .149 |
Data demonstrate as frequency (percentage).
The chi-square independence test was used for statistical analysis.
A P < .05 was considered significant.
*With respect to Reference.
**Insignificant difference with respect to Reference.
Reference: Full-sequence gadoxetic acid-enhanced magnetic resonance imaging and biopsy/histopathology as per the Asia–Pacific clinical practice guidelines for hepatocellular carcinoma.
For detection of hepatocellular carcinoma, non-contrast MRI had higher sensitivity (P < .001, q = 3.919) and accuracy (P < .001, q = 3.362) than the multiphase CT. While specificity was the same (P < .001, q = 2.584). The detailed diagnostic parameters of imaging modalities are reported in Table 3.
Table 3.
Sensitivity, Specificity, and Accuracy of Imaging Modalities for the Detection of Hepatocellular Carcinoma
| Parameters | Reference1 | Non-contrast Magnetic Resonance Imaging2 | The Computed Tomography3 | Comparison | |||
|---|---|---|---|---|---|---|---|
| P | q Value | q Value | q Value | ||||
| Nodules Studied | 248 | 248 | 248 | Between 1 and 2 | Between 1 and 3 | Between 2 and 3 | |
| Sensitivity | 1 | 0.843 | 0.762 | <.0001 | 7.641 | 11.599 | 3.919 |
| Specificity | 1 | 0.864 | 0.809* | <.0001 | 6.343 | 8.928 | 2.584 |
| Accuracy | 1 | 0.755 | 0.571 | <.0001 | 4.483 | 7.844 | 3.362 |
Data demonstrate mean ± SD.
ANOVA following Tukey’s test was used for statistical analysis.
A P < .05 and q > 3.314 were considered significant.
*Insignificant difference with respect to non-contrast magnetic resonance imaging.
Reference: Full-sequence gadoxetic acid-enhanced magnetic resonance imaging and biopsy/histopathology as per the Asia–Pacific clinical practice guidelines for hepatocellular carcinoma.
Clinical Significance
Non-contrast MRI had 0-0.91 diagnostic confidence for the detection of hepatocellular carcinoma and above 0.91 diagnostic confidence, there were chances of overdiagnosis. The multiphase CT had 0.49-0.81 diagnostic confidence for the detection of hepatocellular carcinoma. Below 0.49 diagnostic confidence, multiphase CT had no importance for the detection of hepatocellular carcinoma and above 0.81 diagnostic confidence, multiphase CT had chances of overdiagnosis (Figure 8).
Figure 8.
Beneficial score analysis. Images analyzed by the radiologists (a minimum of 7 years of experience in hepatic imaging) of institutes.
DISCUSSION
The study reported high sensitivity and accuracy for non-contrast MRI than multiphase CT for the detection of liver cancer but both had the same specificity. The results of the current study agreed with the results of the retrospective study,1 EASL (European Association for the Study of the Liver) clinical practice guidelines on liver cancer,2 multicenter prospective trials,10,11 and observational study.12 Arterial and transitional phase hypersensitivity have an important role in the detection of hepatocellular carcinoma through non-contrast MRI.9 The multiphase CT has a lack of differentiating dysplastic nodules from small hepatocellular carcinoma.11 Gadoxetic acid-enhanced MRI improves sensitivity,13,14 but decreases specificity.9,13,15 The study recommended a non-contrast MRI in the diagnosis of liver cancer.
The combined multiphasic CT and non-contrast MRI had better diagnostic parameters (sensitivity, specificity, and accuracy) than the multiphasic CT and non-contrast MRI alone (data are not shown) but the current Liver Imaging and Data Reporting System do not allow integrated interpretation across imaging modalities.16 Therefore, the combination of multiphasic CT and non-contrast MRI is not valid.
The study reported 12 and 21 false-negative results by non-contrast MRI and the multiphase CT. These nodules lacked hallmarks of hepatocellular carcinoma and/or deemed indeterminate.1 Small hepatocellular carcinomas do not show washout.10 Also, non-contrast MRI and multiphase CT reported 27 and 38 cases as false-positive. These results were due to AP shunt showing arterial phase hyperenhancement without washout, focal hyperintensity on T2WI in the liver. Liver cirrhosis, blood flow redistribution, and hepatic parenchymal distortion lead to enhancement of benign nodules.17 There is a lack of consensus for exact imaging modalities for the detection of hepatocellular carcinoma.
Non-contrast MRI had high hepatocellular carcinoma detectability than the multiphase CT. The results of the current agreed with consistent with the results of the retrospective study1 and EASL clinical practice guidelines on liver cancer.2 Non-contrast MRI makes easier the decision making of chemotherapy and/or radiotherapy in patients with suspected liver cancer.
There are several limitations of the study that have to be reported, for example, retrospective study and lack of dynamic trial. The study did not compare results with multiphase MRI. However, this is beyond the scope of clinical practice for liver cancer. The study used 3.0 T MRI but it is expensive than 1.5 T MRI.18 The reference standard included biopsies and histopathology but biopsies may have sampling error.10 False-positive results detected by full-sequence gadoxetic acid-enhanced MRI and biopsy/histopathology did not discuss.
CONCLUSION
Non-contrast MRI had high sensitivity and accuracy than the multiphase CT for the detection of hepatocellular carcinoma. Also, non-contrast MRI may facilitate the easy decision making of chemotherapy and/or radiotherapy in patients with suspected liver cancer. The dynamic study is required to state the superiority of non-contrast MRI in the detection of liver cancer.
Funding Statement
This study was supported by the Wuhan Municipal Health Commission (No: WX13A06).
Footnotes
Ethics Committee Approval: The designed protocol (CHW/CL/15/2020 dated 26 February 2020) of the established study was approved by the radiology review board of the institute.
Informed Consent: Signed an informed consent form regarding diagnosis, biopsies (if required), and the publication of the study in all formats of the publication including personal data and images irrespective of time and language during hospitalization.
Peer-review: Externally peer-reviewed.
Author Contributions: Concept – Y.W., L.H.; Design - Y.W., L.H.; Supervision - L.X.; Resource – Y.W., L.H., L.X.; Materials – Y.W., L.H., L.X., Z.S., C.Y., W.X.; Data Collection and/or Processing – Z.S., C.Y.; Literature Search – Y.W., L.H., L.X., Z.S., C.Y., W.X.; Critical Reviews – Y.W., L.H., L.X., Z.S., C.Y., W.X.
Acknowledgments: Authors are thankful for the medical and non-medical staff of the Central Hospital of Wuhan, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China and the First Affiliated Hospital of Hunan College of Traditional Chinese Medicine (Zhuzhou Hospital of Traditional Chinese Medicine) Zhuzhou, Huan, China.
Conflict of Interest: The authors have no conflict of interest to declare.
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