Impact of a single-day multidisciplinary clinic on the management of patients with liver tumours

In recent decades, few fields of medicine have advanced as much as oncology, and the advent of new diagnostic and treatment modalities has rendered the management of patients highly personalized and complex. State-of-the art care for the oncology patient now often requires the prompt cooperation of physicians from several specialties. In most hospitals, multidisciplinary care consists of separate clinic visits with various specialists in conjunction with a weekly tumour board discussion. One reason for the emphasis on this approach is the accumulating evidence that multidisciplinary care leads to more favourable patient outcomes1–9. In this regard, contemporary recommendations support the management of oncologic patients by a multidisciplinary team including surgical oncologists, medical oncologists, ABSTRACT


INTRODUCTION
In recent decades, few fields of medicine have advanced as much as oncology, and the advent of new diagnostic and treatment modalities has rendered the management of patients highly personalized and complex.State-of-the art care for the oncology patient now often requires the prompt cooperation of physicians from several specialties.In most hospitals, multidisciplinary care consists of separate clinic visits with various specialists in conjunction with a weekly tumour board discussion.One reason for the emphasis on this approach is the accumulating evidence that multidisciplinary care leads to more favourable patient outcomes [1][2][3][4][5][6][7][8][9] .In this regard, contemporary recommendations support the management of oncologic patients by a multidisciplinary team including surgical oncologists, medical oncologists,

Purpose
Multidisciplinary cancer clinics may improve patient care.We examined how a single-day multidisciplinary liver clinic (mdlc) affected care recommendations for patients compared with the recommendations provided before presentation to the mdlc.

Methods
We analyzed the demographic and clinicopathologic data of 343 patients assessed in the Johns Hopkins Liver Tumor Center from 2009 to 2012, comparing imaging and pathology interpretation, diagnosis, and management plan between the outside provider (osp) and the mdlc.
Alterations in the interpretation of imaging occurred for 49 patients (18%) and of biopsy for 14 patients (10%).Referral to the mdlc resulted in a change of diagnosis in 26 patients (8%), of management plan in 70 patients (42%), and of tumour resectability in 7 patients (5%).Roughly half the patients (n = 174, e124 Current OnCOlOgy-VOlume 20, number 2, April 2013 Copyright © 2013 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).radiation oncologists, interventional radiologists, pathologists, and other specialties 10 .
Most hospitals that deliver cancer care have weekly tumour boards, but fewer have actual singleday multidisciplinary clinics.From the patient's perspective, a single-day multidisciplinary clinic visit is less stressful and more convenient than multiple visits to physicians of different specialties and may lead to faster delivery of care and higher adherence to physicians' recommendations 1,10,11 .Multidisciplinary clinics can, however, be more resource-intense and might require providers to deviate from their normal clinic routine.Multidisciplinary cancer clinics have been adopted for patients with breast 1-3 , gynecologic [12][13][14] , pancreatic 4,5 , lung 13,15 , skin [16][17][18] , head-and-neck 19,20 , and prostate malignancies [6][7][8][9] .Multidisciplinary clinics have even been proposed for patients with specific types of metastases 21 .
Primary and secondary malignancies of the liver may be particularly well suited to a single-day multidisciplinary clinic approach.Primary liver cancer is the 5th most common cancer in terms of mortality, with about 20,550 attributable deaths estimated in 2012, and its incidence is increasing.Treatment of primary and secondary malignancies has evolved to include systemic, intraarterial, and surgical options.In addition, patients with liver malignancies often have underlying steatosis, hepatitis, or cirrhosis.A singleday multidisciplinary clinic in which patients can be seen by various providers during one visit may therefore be of great benefit to patients with liver tumours.
Although outcomes of multidisciplinary clinics have been described for several cancer types [1][2][3][4][5][6][7][8][9][12][13][14][15][16][17][18][19][20] , no study to date has documented the outcomes of a single-day liver multidisciplinary clinic. The mltidisciplinary liver clinic (mdlc) at the Johns Hopkins Hospital (jhh) was established in 2009 so that patients with liver tumours could be evaluated by a range of specialists within the same visit day and site.We sought to evaluate the impact of a multidisciplinary liver tumour clinic on the diagnosis and treatment recommendations for patients with liver tumours.

METHODS
The Johns Hopkins Liver Tumor Center established the mdlc in 2009, aiming to evaluate patients with known or suspected tumours in the liver in the context of a single-day multidisciplinary clinic.Patient referrals are first screened by the clinical coordinator (SS) and then triaged by the clinical director (TMP).The coordinator obtains prior medical records, crosssectional imaging, pathology slides and reports, and other pertinent information.Every effort is made to acquire existing imaging and pathology studies, which are submitted to jhh for formal radiology and pathology review.The multidisciplinary clinic involves mostly new, but also routine follow-up, patient consultations.
In advance of the clinic, each patient's medical information, imaging studies, and pathology are reviewed, and the case is discussed at a multidisciplinary conference consisting of the providers scheduled to see the patient on the given clinic day.The board regularly consists of a surgical oncologist, medical oncologist, radiation oncologist, radiologist, pathologist, interventional radiologist, hepatologist, and transplant surgeon.On the day of the clinic visit, routine laboratory exams and, if necessary, repeat cross-sectional imaging are obtained.Patients are seen by the clinical team and consensus recommendations are communicated to them the same day during the clinic visit.On a typical day, patients undergo any additional necessary imaging and laboratory studies from 07h00 to 09h00; the multidisciplinary tumour board conducts formal case reviews from 09h00 to 10h00; and patients are seen sequentially or together by physicians from the various disciplines from 10h00 to 13h00, during which time full details of the tumour board recommendations are discussed with the patients.
The records of 389 patients seen in the clinic from April 28, 2009, to February 21, 2012, were systematically reviewed.Of those 389 patients, 46 were excluded because they did not represent new consultations or because data from the outside hospital records were missing such that comparisons with the mdlc recommendations were not possible.Demographic information for the 343 included patients (including age, sex, race, and distance from jhh) was extracted from the records, as were data about evaluation and treatment of the patient both by the prior outside provider (osp) and by the jhh mdlc.Clinically significant alterations in pathology or imaging interpretation, diagnosis, and management plan between the osp and the mdlc were recorded.The outside recommendations were determined by review of records from the outside institution, including clinic and hospital notes.A clinically significant alteration was defined as one that could potentially alter the patient's diagnosis, management plan, or outcome.The impact of those alterations on clinical assessment and recommendations were assessed.
Most patients did not undergo repeat imaging at the mdlc.However, repeat ct imaging was obtained in 61 patients (20.6%) within a median time interval of 1.9 months (iqr: 1.1-3.6 months), and repeat mr imaging was obtained in 29 (18.7%)within a median time interval of 1.1 months (iqr: 0.8-2.6 months).No patients underwent repeat positron-emission tomography or other imaging upon presentation to the mdlc.The most common reasons for repeat cross-sectional imaging were low-quality images or poor visualization of the hepatic mass or masses or vital structures.Of the 47 patients who did not undergo ct imaging at the outside institution, 11 (23.4%)underwent ct imaging at the liver clinic.Of the 188 patients who did not undergo mr imaging at the outside institution, 52 (27.7%) underwent mr imaging at the liver clinic.Fourteen patients (4.1%) underwent positronemission tomography at the clinic.
Approximately half the patients (n = 194, 56.6%) had undergone a biopsy of the liver mass before their presentation at the mdlc (Table i).Biopsy slides for most of those patients (n = 137, 70.6%) were rereviewed by the pathology department at the jhh mdlc.A new biopsy was performed at jhh for 9 of the patients (2.6%) attending the mdlc.
Among the 309 patients who came to the mdlc with a clinical diagnosis from the osp, that diagnosis was altered in 26 (8.4%), with unknown or indeterminate diagnoses decreasing to 10 (2.9%) from 31 (9.0%).Of the diagnostic changes, 17 (65.4%)resulted from a change in imaging interpretation by the members of the mdlc; 1 (3.8%), from a change in pathology; 1 (3.8%), from a combination of pathology and imaging reinterpretation; 1 (3.8%), from a combination of negative screening for a primary tumour and pathology reinterpretation; and 6 (23.1%), because of clinical impression.Of the altered diagnoses, 6 (23.1%) changed from indeterminate to benign; 6 (23.1%), from indeterminate to malignant; 11 (42.3%), from one malignant diagnosis to another type of malignant diagnosis; 2 (7.7%), from malignant to benign; and 1 (3.8%), from one benign diagnosis to a another type of benign diagnosis.
Of the 267 patients whose outside cross-sectional imaging was re-reviewed at the jhh mdlc, 49 (18.4%) received an altered interpretation.The most common alteration was a change in diagnosis (n = 30, 61.2%).In 18 studies, an indeterminate diagnosis changed to a probable radiologic diagnosis.The change was from benign to malignant in 5 patients, from a malignant diagnosis to a different malignant diagnosis in 6 patients, and from a benign diagnosis to a different benign diagnosis in 1 patient.In 10 patients (20.4%), there was a change in the number of lesions; in 2 (4.1%), a change in the lesion location or locations; in 2 (4.1%), a change in determination of the primary lesion; and in 1 (2.0%), a change concerning patency of the portal vein.For several patients, multiple alterations pertained to single image, or a single change pertained to multiple imaging modalities.
Of the 137 patients whose outside pathology slides were re-reviewed at jhh, 14 (10.2%) received an altered pathology diagnosis.For 1 patient (7.1%), the pathology interpretation changed from one benign diagnosis to another benign diagnosis, and for 2 patients (14.3%), from one malignant diagnosis to a different malignant diagnosis.Among the alterations in biopsy reads, 1 diagnosis (7.1%) changed from adenoma to normal liver; 2 (14.3%), from malignant to indeterminate; and 3 to malignant.In 4 patients, the diagnosis changed from adenocarcinoma not otherwise specified to cholangiocarcinoma.
A management plan was known to have been formulated for 168 patients (49.0%) at their outside institution.After evaluation at the jhh mdlc, 70 of those patients (41.7%) received alterations to the recommended management plan.Resection was recommended for 4 patients who were initially deemed inoperable by the osp, and a recommendation against resection was given to 5 patients, contrary to the outside recommendation.Three patients who were a Magnetic resonance cholangiopancreatography, octreotide scintigraphy, and single-photon-emission computed tomography, among others.b Computed tomography (ct) imaging was repeated at the multidisciplinary liver clinic (mdlc) for 61 patients (20.6%) receiving ct imaging at the outside provider (osp), with a median time interval of 1.9 months (interquartile range: 1.1-3.6).Magnetic resonance imaging (mri) was repeated at the mdlc for 29 patients (18.7%) receiving mri at the osp, with a median time interval of 1.1 months (interquartile range: 0.8-2.6).No patients underwent repeat positron-emission tomography (pet) or other imaging at the mdlc.In addition, 5 ct, 2 mri, and 2 pet studies ordered in the mdlc were performed at an osp for various reasons (for example, insurance coverage).c A biopsy ordered by the outside provider was performed at The Johns Hopkins Hospital for 2 patients (before they presented at the multidisciplinary liver clinic).nos = not otherwise specified.

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previously denied transplantation were considered eligible.Two patients previously offered transplantation were not considered transplantable after review at the mdlc.For 8 patients, chemotherapy was added to the management plan, and for 3, a change in the type of chemotherapy was recommended.Intraarterial therapy was offered to 28 patients, and 4 patients were counselled not to undergo intraarterial therapy as recommended by the osp.Plans for 5 patients were changed from no treatment or palliation to some form of treatment and, for 6 patients, from some form of treatment recommendation to no treatment or palliation.

DISCUSSION
The importance of coordinated multidisciplinary care has been increasingly emphasized for oncology patients with a wide array of cancers including breast, pancreatic, and prostatic [1][2][3][4][5][6][7][8][9] .Weekly tumour boards and single-day multidisciplinary clinics both allow a variety of providers to review and contribute to the care plan of patients with cancer, but these two approaches have some important  differences.Specifically, some investigators have expressed concern that tumour boards do not allow for an in-depth review of each individual case because, often, many cases are reviewed in a short time period 22 .Furthermore, weekly tumour boards may not allow for an actual clinical appraisal of the patient by the various providers and do not provide patients with the opportunity to express their preferences and views to the entire team in the context of multiple therapeutic options 23 .In contrast, during a single-day multidisciplinary clinic, the patient's information can be reviewed by a team of providers in "real time" and the providers can all interact with the patient.In turn, the patient can meet with the various teams in the course of the one day.Improved outcomes have been associated with the use of single-day multidisciplinary clinics for patients with breast and pancreatic cancer 3,4 .
The present study is important because, to our knowledge, it is the first report the impact of a singleday multidisciplinary clinic for patients with liver tumours.Notably, we found that the osp management plan was altered for 41.7% of the patients who visited the mdlc.In fact, a number of those alterations to the  therapeutic plan were based on the clinical expertise of the providers, a re-review of pathology, or a reinterpretation of cross-sectional imaging.
Interpretation of the imaging obtained at an outside institution was changed for a significant number of patients (n = 49, 18.4%).Although some of the interpretation differences in the cross-sectional imaging included a change in tumour location or number, it is important to note that the diagnosis was actually changed in a subset of the patients (n = 30, 61.2%).It can be challenging to distinguish between benign and malignant liver disease and to identify and differentiate lesions in the setting of a steatotic ("fatty") or cirrhotic liver 24,25 .Heiken et al. 26 reported that 10%-20% of solid benign tumours may display atypical features that could be confused with hepatocellular carcinoma, cholangiocarcinoma, or hypervascular metastases.In addition, hepatocellular adenoma can often have a varied appearance, and certain subtypes such as infiltrative hepatocellular carcinoma can frequently be missed completely by inexperienced radiologists 27,28 .Although the causes are undoubtedly multifactorial, the interpretive changes reported in the present study are likely a result of having specialized radiologists whose primary focus is hepatobiliary disease review the images.
A change in the pathology interpretation of outside slides was also not infrequent (10.2%).Most commonly, the pathology diagnosis was changed because of a reinterpretation of the immunohistochemistry staining done at the outside institution.In a previous study, Bomeisl et al. 29 reported that a change in management was suggested for 2.6% of patients (n = 2) based on the results of a pathology second opinion, and that a major disagreement in the pathology findings arose for 9% (n = 7).In another study, Layfield et al. 30 reported a 16% overall rate of diagnosis disagreement in second-opinion reviews of outside cytology specimens, with the greatest number of cases coming from lung, thyroid, and liver.
Pathology reassessment may be particularly important for patients with liver tumours.Several investigators have reported on the difficulty of differentiating dysplastic nodules, hepatic adenoma, and hepatocellular carcinoma 31,32 , and of separating primary liver cancers from metastatic disease 33 .The Association of Directors of Anatomic and Surgical Pathology recommend a second-opinion review of outside pathology specimens before initiation of treatment, including radiation, chemotherapy, or surgery 34 .Our data support the importance of having outside pathology re-reviewed before arriving at a final clinical diagnosis and initiating therapy.
By offering a single-day mdlc, we provide patients greater access to expertise, resources, and clinical trials.For example, for many patients, the change in their management plan was a result of the presence at the mdlc of providers with significant expertise in chemotherapy and intraarterial therapy [35][36][37][38] .For patients who had seen only an outside surgical provider, the change in the treatment recommendations might partly have arisen from a lack of sufficient expertise among the outside providers with respect to the administration of chemotherapy and intraarterial therapy for hepatobiliary tumours.
Besides the therapeutic benefits, a single-day multidisciplinary clinic offers a more patient-centered approach to delivering cancer care, which may also facilitate faster initiation of treatment 39 .Other authors have shown that patients prefer a one-stop clinic to a multiple-visit approach 39,40 .In addition, Frost et al. 41 reported that patients seen in a multidisciplinary clinic were significantly more satisfied than patients who did not receive multidisciplinary care.As health care increasingly shifts to a more patient-centred focus, we believe that demand for single-day multidisciplinary cancer clinics such as the mdlc will only increase.
Our study has several limitations, a major one being its retrospective single-institution nature.Although we were able to collect data on patients prospectively from the initiation of the clinic in 2009, we were not able to compare the mdlc patients with liver tumour patients treated at jhh before 2009.A comparison of the mdlc's findings and therapeutic recommendations compared with those for patients treated at jhh outside the confines of the clinic was not feasible.Specifically, after initiation of the multidisciplinary clinic, patients who were thought likely to benefit from a multimodality approach were preferentially triaged to the clinic.As a result of that selection bias, direct comparisons between the multidisciplinary and non-multidisciplinary patients would not be appropriate.However, a direct comparison was not necessary to meet the primary objective of the present study, which was to assess the relative "value added" of the mdlc.
Information on patient evaluation of, and satisfaction with, the multidisciplinary clinic was collected only from a subset of patients-all of whom "strongly agreed" that the multidisciplinary clinic was "better" than a more traditional clinic appointment during which the patient sees only one provider.More comprehensive patient satisfaction data are needed, and those data are currently being prospectively collected.

CONCLUSIONS
Our study notes a significant impact of a single-day mdlc on patient care.A change in imaging interpretation occurred in 18.4% of patients, and a change in pathology interpretation, in 10.2%.Patient assessment in the mdlc led to a change in management plan for 41.7% of patients, and of patients who were ultimately followed at our institution, 13.7% were enrolled in clinical trials.Although the foregoing changes might not be fully attributable to the multidisciplinary format, a large benefit of the mdlc is its role as a central location for physicians to discuss information and to review new radiology and pathology interpretations.This "360 review" of all data, imaging, and records by a team of experts makes the mdlc is an important means of delivering expert opinion about the diagnosis and management of benign and malignant liver disease.Our institution's experience supports the feasibility and effectiveness of a single-day mdlc and demonstrates the impact of the clinic on patient care.
(21.4%), from indeterminate Current OnCOlOgy-VOlume 20, number 2, April 2013 Copyright © 2013 Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).

figure 1 A
figure 1 A modified Venn diagram depicts the overlap of changes in treatment, imaging, or pathology (or a combination), and diagnosis.Imaging or pathology (or both) changed in 29 patients without changes in diagnosis or treatment; in 17 patients with a change in diagnosis; in 15 with a change in treatment; in 2 with a change in both diagnosis and treatment.In 6 patients, the diagnosis changed without a change in treatment, imaging, or pathology; in 47, treatment changed without such a change; and in 3, diagnosis and treatment both changed without a change in imaging or pathology.In 2 patients, resectability changed because of a change in imaging or pathology, and in 5, resectability changed without a change in imaging or pathology.Changes in imaging include only those recorded on official radiology reports.

figure 2 (
figure 2 (A) Scan of a 56-year-old woman at an outside provider (osp) was interpreted as perfusion changes (arrow), with no mass.(B) Review of images at the multidisciplinary liver clinic (mdlc) revealed a left portal vein tumour thrombus (arrow) consistent with infiltrative hepatocellular carcinoma with portal vein involvement.The patient subsequently underwent intraarterial therapy.(C) Scan of a 28-year-old man with newly diagnosed colon cancer at an osp was interpreted as hepatic hemangiomas (arrows).(D) Review of images at the mdlc revealed T2-intense signal in the left hemi-liver lesion, with nodular enhancement compatible with hemangioma.The right liver lesion was consistent with metastatic disease, however.Patient subsequently underwent colon resection with simultaneous liver resection and received adjuvant systemic therapy.(E) Accurate diagnosis is vital in guiding therapy.This neuroendocrine neoplasm looks similar to a hepatocellular carcinoma.Careful histologic examination and special staining techniques are keys to correctly classifying this liver tumour.
Multimed Inc.Following publication in Current Oncology, the full text of each article is available immediately and archived in PubMed Central (PMC).

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table i
Patient management and leading diagnosis at the outside provider and the multidisciplinary liver clinic

table ii
Outcome and alterations in patient care as a result of the multidisciplinary liver clinic (mdlc) visit a Patient revisited the mdlc for a follow-up [n (%)] 174 (50.7)Patient care delivered at jhh [n (%)] jhh = The Johns Hopkins Hospital.