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Poullos et al.
Multiphasic CT Reporting for HCC
Gastrointestinal Imaging
Original Research
Structured Reporting of
Multiphasic CT for Hepatocellular
Carcinoma: Effect on Staging and
Suitability for Transplant
Peter D. Poullos1 OBJECTIVE. The purpose of this study is to evaluate whether use of a standardized radi-
Joseph J. Tseng1 ology report template would improve the ability of liver transplant surgeons to diagnose stage
Marc L. Melcher 2 T2 hepatocellular carcinoma (HCC) and determine patient suitability to undergo orthotopic
Waldo Concepcion2 liver transplant (OLT).
Andreas M. Loening 3 MATERIALS AND METHODS. In this retrospective study, a standardized template
was devised, and its use was mandated for reporting of liver CT findings for patients with
Jarrett Rosenberg 4
cirrhosis and HCC. Two surgeons analyzed 200 reports (100 before and 100 after template
Jüergen K. Willmann1
American Journal of Roentgenology 2018.210:766-774.
1
Department of Radiology, Division of Body Imaging,
H is a major cause of death among
patients with end-stage liver dis-
ease (ESLD). For patients with
HCC are prioritized by calculating the model
for end-stage liver disease (MELD) score on
the basis of bilirubin, creatinine, and interna-
Stanford University, 300 Pasteur Dr, Stanford, CA HCC and ESLD, potentially curative options tional normalized ratio (INR) values. MELD
94305-5621. Address correspondence to J. J. Tseng include surgical resection, ablation, and or- alone, however, does not reflect the progno-
(jtseng3@stanford.edu).
thotopic liver transplant (OLT). For trans- sis for HCC in patients [2] in whom tumor
2
Department of Surgery, Division of Multi Organ plant candidates who are ineligible for cura- progression, vascular invasion, and metastat-
Transplantation, Stanford University, Stanford, CA. tive resection, OLT is a desirable method for ic disease can preclude transplant. To rec-
simultaneously removing the HCC and re- tify this disadvantage, the United Network
placing the failing cirrhotic liver. OLT, how- for Organ Sharing, which organizes the Or-
3
Department of Radiology, Division of Body MRI,
Stanford University, CA.
ever, requires that the patient be placed on a gan Procurement and Transplantation Net-
4
Department of Radiology, Stanford University, waiting list. In 2016, a total of 14,750 pa- work (OPTN) in the United States, has cre-
Stanford, CA. tients were listed as waiting for transplant, ated an exception categorization that allows
but only 7841 transplants were performed; patients with HCC to obtain a higher MELD
AJR 2018; 210:766–774
1206 patients died while waiting, and an ad- score that more appropriately reflects their
0361–803X/18/2104–766 ditional 1404 patients were removed from medical urgency for liver transplant. Candi-
the list because they were too sick to under- dates meeting these criteria receive an ini-
© American Roentgen Ray Society go transplant [1]. tial MELD score equivalent of 22, and fur-
ther points are awarded based on laboratory The purpose of the present study is to template listed as a “body CT abdomen liver tri-
values [3]. evaluate whether the use of a standardized phasic” (Appendix 4) was also created for reports
To obtain points, HCC lesions must meet radiology report template would improve the assessing patients without stage T2 HCC (with
specific OPTN imaging-based criteria [4]. Le- ability of liver transplant surgeons to diag- this less detailed template hereafter referred to as
sions are designated OPTN class 1 (definite- nose stage T2 HCC and suitability for OLT. the “non-OPTN template”). Before template im-
ly benign) through class 5 (definitely HCC), plementation, radiologists used their own personal
depending on their size and arterial enhance- Materials and Methods style of dictation to create reports.
ment as well as the presence of washout, cap- Template Design
sule, threshold growth, or a combination of An institutional review board waiver was Report Collection
these features. Candidates must have at least granted for this study, and informed consent was Eighteen months after the start date, reports of
one OPTN class 5 lesion and stage T2 disease, waived because of the retrospective methods used. patients with HCC were collected for analysis, with
as defined by the Milan criteria (Appendix 1), The study was HIPAA compliant. an arbitrary goal of collecting 100 reports dictated
to qualify for exception points. To apply, the Two abdominal radiologists created the tem- before template implementation and 100 reports dic-
transplant team must complete standard Unit- plate for patients with stage T2 HCC (Appendix tated after template implementation. The lead author
ed Network for Organ Sharing documentation 3) to include all imaging details needed to apply requested that the radiology information technol-
that includes comprehensive imaging details for exception points. This template was derived in ogy team search the radiology information system
(Appendix 2). Surgeons rely on radiology re- part from templates freely available through the for multiphasic (late arterial, portal venous, and de-
ports that, unfortunately, often omit the de- Radiological Society of North America Informat- layed) liver CT reports containing the terms “cir-
tails required for these forms. Significant time ics Reporting website [11], and additional modifi- rhosis” and either “hepatocellular carcinoma” or
is spent reevaluating imaging studies because cations were made to mimic the required OPTN “HCC.” The search results were returned in a chron-
of information missing from the reports, es- documentation completed by the transplant team. ologically sorted order with the use of spreadsheet
sentially requiring a second radiologist to re- After creation of this template, the chief of clinical software (Excel, version 15.0, Microsoft) with an ac-
American Journal of Roentgenology 2018.210:766-774.
interpret the case (for example, at liver trans- transplantation reviewed and approved its use. Of companying word-processed document (Microsoft
plant tumor boards). importance, the surgeons surveyed in the present Word 2013, Microsoft) containing the reports.
Structured reporting has been endorsed study were unaware of our research intentions and Inclusion criteria (Table 1) were designed to fa-
by the American College of Radiology and their future role as report analysts. cilitate collection of a variety of reports for pa-
other professional societies as a method of tients who were close to meeting the Milan criteria,
communicating the most pertinent and use- Template Implementation for whom accurate staging would be particular-
ful information with the use of standardized On January 13, 2014 (the start date), an e-mail ly important. Exclusion criteria were designed to
language and formatting [5, 6]. Template cre- was sent to all radiology faculty and trainees, minimize reports including likely benign lesions
ation should be a multidisciplinary effort, designating our template mandatory for use in or early HCC. Although hyperenhancing lesions
and studies have shown that both referring reports regarding patients with stage T2 HCC. smaller than 1 cm and hypoenhancing lesions may
physicians and radiologists favor structured OPTN educational references were also included. probably represent HCC (according to the Liv-
over conventional nonstructured reports [7– The template was made available in a real-time er Imaging Reporting and Data System or OPTN
9]. Although widely adopted, the clinical radiology reporting platform (Power Scribe 360, class 4), these patients do not qualify for exception
impact of such templates has not been well Nuance) under the listing “body CT abdomen liver points and therefore were excluded. Likewise, we
studied in the literature. However, findings OPTN HCC.” This template will hereafter be re- excluded patients with advanced HCC, who also
from early studies are promising [10]. ferred to as the “OPTN template.” A less detailed do not qualify for exception points.
instruction regarding inclusion and exclusion cri- with each page containing only one unique re-
teria. The two authors then collected 20 reports to- Report Sanitization and Truncation port. Each surgeon, blinded to study goal and de-
gether, practicing selection using the inclusion and Reports were sanitized to remove all protect- sign, received a copy of this document, along with
exclusion criteria. The author who had received ed health information, clinical information, and a link to the electronic survey. Study survey data
instruction then collected 20 additional reports on dates. They were further truncated by deleting in- were collected and managed using research elec-
his own, which the lead author then reviewed for formation related to IV contrast medium and ra- tronic data capture tools (REDCap, version 6.9.3,
accuracy. Once trained satisfactorily, the author diation dose, as well as statements related to the Stanford University).
trained by the lead author collected the remaining thorax, pancreas, adrenals, kidneys and ureters,
160 reports, which were then reviewed once more bowel, lymph nodes, abdominal wall, and bones. Response Tabulation
by the lead author to determine adherence to the All that remained (when included) was text de- Questions 1–9 elicited yes or no responses,
inclusion and exclusion criteria. scribing liver morphologic findings, hepatic vas- whereas questions 10–12 offered a third response
To find 100 pretemplate reports meeting inclu- culature, liver lesions, gallbladder, and biliary option (unsure) because they inquired about the
sion criteria, we reviewed 497 reports dating up to
TABLE 2: Reasons for Report Exclusion Among Abdominal CT Studies
27 months before the start date. To find 100 post-
template reports, we reviewed 382 reports dating up Reason for Report Exclusion Before Template After Template
to 20 months after the start date. A total of 397 pre-
Not likely HCC 169 123
template and 182 posttemplate reports were exclud-
ed (Fig. 1). Detailed reasons for exclusion are listed Nonabdominal CT 95 88
in Table 2. If a single patient had multiple unique Prior hepatic surgery 26 2
reports, those were not excluded. All posttemplate Prior OLT 23 7
reports meeting inclusion criteria were included, re-
Too many lesions 19 17
gardless of whether the OPTN template was used.
It was decided a priori to do an intention-to-treat Metastatic disease 14 7
analysis, avoiding overoptimistic estimates of tem- Indeterminate lesion 13 17
plate effectiveness resulting from inclusion bias. Maximum lesion diameter < 1 cm 11 4
Ninety-five pretemplate and 88 posttemplate
Technically limited 9 4
reports were eliminated because they were not
for abdominal CT. These included interventional Maximum lesion diameter > 10 cm 7 1
radiology procedures and CT scans of the chest Infiltrative HCC 5 0
that were inadvertently captured in our radiology Tumor thrombus 4 5
information system search results. In the pretem-
OPTN class 3 2 7
plate group, the two most common reasons for ex-
clusion of abdominal CT reports were lesions that Hypoenhancing HCC 0 0
were unlikely to represent HCC (n = 169) and pre- Total 397 282
vious hepatic surgery (n = 26). In the posttemplate Note—HCC = hepatocellular carcinoma, OLT = orthotopic liver transplant, OPTN = Organ Procurement
group, the most common reason for exclusion of Transplantation Network.
ability to draw conclusions on the basis of report obtained after that date. Of the 100 re-
American Journal of Roentgenology 2018.210:766-774.
TABLE 5: Total Number of Positive Responses and Interobserver Agreement (Kappa Value) Between Two Surgeons
for Reports Obtained Before and After Template Implementation
Positive Responses (%) Kappa Value
Before Template After Template
Before After Overall
Question Number and and Topic Surgeon 1 Surgeon 2 Surgeon 1 Surgeon 2 p Template Template Overall 95% CI
Question 1: cirrhosis 97 93 95 92 0.52 0.37 0.59 0.5 0.216–0.762
Question 2: portal hypertension 74 86 88 87 0.042 0.27 0.41 0.32 0.159–0.489
Question 3: no. of lesions 98 76 98 88 0.038 0.04 −0.04 0.01 −0.046 to 0.122
Question 4: size of lesions 95 82 96 93 0.03 0.10 0.14 0.12 0.045–0.313
Question 5: enhancement 93 80 94 91 0.049 −0.12 0.07 −0.05 −0.113 to 0.074
Question 6: tumor thrombus 10 31 57 63 < 0.001 0.22 0.46 0.46 0.327–0.567
Question 7: PV patency 80 68 72 65 0.22 0.49 0.52 0.51 0.379–0.631
Question 8: SMV patency 37 37 34 37 0.76 0.70 0.72 0.71 0.597–0.805
Question 9: OPTN mentioned 8 2 82 81 < 0.001 0 0.63 0.84 0.755–0.900
Question 10: OPTN correct (% of question 9) 50 0 100 96 < 0.001 — — — —
Question 11: HCC 80 80 95 93 0.025 0.31 0.14 0.27 0.131–0.415
Question 12: Milan criteria 78 80 89 96 < 0.0001 0.25 0.40 0.34 0.249–0.444
American Journal of Roentgenology 2018.210:766-774.
The five items that improved were pres- implementation (p < 0.001). Subgroup analy- Transplantability
ence or absence of portal hypertension, sis reveals that four of 47 OPTN template re- Before implementation of the template,
number of lesion(s), size of the lesion(s), en- ports (8.5%) did not mention OPTN. None of 20% (surgeon 1) or 22% (surgeon 2) of the
hancement characteristics, and the presence these four patients, however, had T2 disease, reports studied were perceived as not con-
or absence of tumor thrombus. Of these five so not using the OPTN template was a cor- taining enough information for the surgeons
items, the most statistically significant im- rect decision. One patient had a 6.6-cm le- to decide whether the patient met the Milan
provement was the mention of tumor throm- sion, another patient had six tumors, a third criteria. This value decreased to 4% (surgeon
bus, which increased from 10% (surgeon 1) patient had a lesion with questionable wash- 1) or 11% (surgeon 2) after template imple-
or 31% (surgeon 2) before template imple- out, and the last patient had a lesion that was mentation (p < 0.0001) (Fig. 3).
mentation to 57% (surgeon 1) or 63% (sur- actually OPTN class 4, although that was
geon 2) after template implementation (p < not explicitly stated. In contrast, 12 of the 53 Satisfaction
0.001). Subgroup analysis after template im- non–OPTN-template reports (22.6%) did not Before template implementation, surgeon
plementation showed that 91% (surgeon 1) or mention OPTN. Of those 12 reports, seven 1 was satisfied or very satisfied with 3% of
89% (surgeon 2) of the 47 OPTN template (58%) were for patients with T2 disease, and the reports. However, this value increased to
reports reported the presence or absence of therefore should have mentioned OPTN. 50% for reports created after template im-
tumor thrombus, compared with 74% (sur- Surgeon 1 stated that of the 8% of pre- plementation (p < 0.0001). Before template
geon 1) or 68% (surgeon 2) of the 53 non- template reports that mentioned OPTN, implementation, surgeon 2 was satisfied or
OPTN template reports (for surgeon 1, p = 50% were correctly classified. Of the 82% of very satisfied with 30% of the reports. This
0.035; for surgeon 2, p = 0.015). One patient posttemplate reports that mentioned OPTN, value increased to 80% for reports created
in the pretemplate group and one patient in 100% were correctly classified. Surgeon 2 after template implementation (p < 0.0001)
the posttemplate group had a tumor throm- stated that of the 2% of the pretemplate re- (Fig. 4). When multivariate analysis was per-
bus. The three items for which no improve- ports that mentioned OPTN, 100% were cor- formed, the items that were correlated with
ment was seen were presence or absence of rectly classified. Also, of the 81% of post- report satisfaction were portal hypertension,
cirrhosis, portal vein patency, and superior template reports that mentioned OPTN, 96% tumor thrombus, portal vein patency, and
mesenteric vein patency. were correctly classified. OPTN class (p < 0.001 for all).
100 100
80 80
Percentage of Responses
Percentage of Responses
60 60
40 40
20 20
0 0
Before After Before After Before After Before After
Template Template Template Template Template Template Template Template
Surgeon 1 Surgeon 2 Surgeon 1 Surgeon 2
Fig. 2—Bar graph of reader response to survey question 11 (“Assuming imaging Fig. 3—Bar graph of reader response to survey question 12 (“Based purely on this
description is correct, does patient have hepatocellular carcinoma?”). report, in absence of contraindications to transplant, can you determine whether
or not this patient falls within Milan criteria and qualifies for MELD priority
score?”). MELD = model for end-stage liver disease.
formation as well as surgeon satisfaction. pressions were compared with arthroscopic MRI examinations. By utilizing a 12-item
Specifically, we improved the ability of sur- findings, and the overall accuracy increased structured reporting template for brain MRI
geons to diagnose HCC and assess suitability from 53% to 76% when readers used the examinations of patients with known or sus-
for MELD exception points. structured template as opposed to traditional pected multiple sclerosis, the authors were
Our results are concordant with those of reports. Dickerson et al. [13] also compared able to show that reports obtained after tem-
other studies that have shown that structured the differences in report thoroughness and plate implementation yielded a significant in-
reports provide superior description and satisfaction between reports obtained before crease in multiple sclerosis–relevant findings
evaluation of the clinical question and im- and after template implementation that de- and positive ratings by neurologists. Reports
prove the confidence of referring physicians scribed multiple sclerosis findings on brain obtained after template implementation men-
[7–9, 12]. Brook et al. [12] compared struc-
tured versus traditional reports of multipha-
sic CT for the ability to assess for resectabil- 100
ity of pancreatic carcinoma. They found that
structured reports provided more complete
reporting of 12 key features (7.3 of 12 fea- 80
Percentage of Responses
APPENDIX 1: Milan Criteria for Liver Transplant for Patients With Hepatocellular Carcinoma
The Milan criteria for patient suitability to undergo liver transplant for hepatocellular carcinoma include the following [15]:
• Single tumor less or equal to 5 cm
• Presence of two to three tumors, none of which exceed 3 cm
• No indication of vascular invasion, extrahepatic manifestations, or both
APPENDIX 2: Standardized Paperwork Required for Placement of Patients on Transplant Waiting List
Figures 5–7 are templates provided by United Network of Organ Sharing (UNOS) for centers to use when recording hepatocellular carci-
noma imaging findings. Documentation of these findings is required by UNOS when applying for model for end-stage liver disease (MELD)
exception points for patients with end-stage liver disease and hepatocellular carcinoma who require placement on a transplant waiting list.
They are not to be submitted with the report, and centers may choose to develop their own documentation methods.
American Journal of Roentgenology 2018.210:766-774.
Fig. 5—Optional reporting template for MRI. OPTN = Organ Procurement Fig. 6—Optional reporting template for CT. OPTN = Organ Procurement
Transplantation Network, SI = signal intensity. © 2018 UNOS. Used with permission. Transplantation Network, SI = signal intensity. © 2018 UNOS. Used with permission.
APPENDIX 3: Standard Reporting Template for APPENDIX 4: Template for Patients Without Stage T2
Hepatocellular Carcinoma (HCC) Hepatocellular Carcinoma (HCC)
Assessment
LIVER:
LIVER: Morphology:
Cirrhosis: Focal lesions:
Portal hypertension: Hepatic vasculature:
Liver lesions: REMAINING ABDOMEN:
Largest lesion size: Biliary tree:
Lesion location: Gallbladder:
Late arterial hyperenhancement: Spleen:
Portal venous phase washout: Pancreas:
Portal venous phase pseudocapsule enhancement: Adrenal glands:
Delayed phase washout: Kidneys and ureters:
Delayed pseudocapsule enhancement: Gastrointestinal tract:
Tumor thrombus: Peritoneal cavity:
Largest axial dimension: (This does not include the pseudocapsule in Vasculature:
measurement)
Lymph nodes:
Largest CC dimension:
American Journal of Roentgenology 2018.210:766-774.
Abdominal wall:
Contrast phase used for measurement:
Musculoskeletal:
Size on prior study:
IMPRESSION:
Prior study date:
1. Number of HCC lesions:
Infiltrative hepatocellular carcinoma:
2. Largest lesion size:
Portal vein:
3. Findings meet OPTN criteria class:
Superior mesenteric vein:
4. Cirrhotic changes:
Splenic vein:
5. Portal hypertension:
Hepatic venous system:
Note—OPTN = Organ Procurement Transplantation Network.
Hepatic arterial system:
REMAINING ABDOMEN:
Biliary tree:
Gallbladder:
Spleen:
Pancreas:
Adrenal glands:
Kidneys and ureters:
Gastrointestinal tract:
Peritoneal cavity:
Vasculature:
Lymph nodes:
Abdominal wall:
Musculoskeletal:
IMPRESSION:
1. Number of HCC lesions
2. Largest lesion size:
3. Findings meet OPTN criteria class:
4. Cirrhotic changes:
5. Portal hypertension:
Note—CC = craniocaudal, OPTN = Organ Procurement Transplantation Network.