Is the Mayo Model for Predicting Survival Useful After the Introduction of Ursodeoxycholic Acid Treatment for Primary Biliary Cirrhosis?
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1 Is the Mayo Model for Predicting Survival Useful After the Introduction of Ursodeoxycholic Acid Treatment for Primary Biliary Cirrhosis? MATTHEW R. KILMURRY, 1 E. JENNY HEATHCOTE, 1 KAREN CAUCH-DUDEK, 1 KEITH O ROURKE, 2 ROBERT J. BAILEY, 3 LAURENCE M. BLENDIS, 1 CAMERON N. GHENT, 4 GERALD Y. MINUK, 5 S. CHRIS PAPPAS, 1 LINDA J. SCULLY, 6 URS P. STEINBRECHER, 7 LLOYD R. SUTHERLAND, 8 C. NOEL WILLIAMS, 9 AND LAWRENCE J. WOROBETZ 10 Treatment of patients with primary biliary cirrhosis eral prognostic indicators have been proposed and (PBC) using ursodeoxycholic acid (UDCA) leads to a re- prognostic indexes developed to predict survival. duction in serum bilirubin. The first objective of this Shapiro et al. 1 showed that serum bilirubin is a good study was to assess the performance of certain prognos- predictor of survival in PBC, and elevated serum bilirutic indicators for PBC after the introduction of treatbin levels have been used to decide when to refer pament with UDCA. Serum bilirubin is an important progtients for transplantation. 2 Other groups have develnostic indicator for PBC and an important component of the Mayo model for grading patients into risk categoseveral other variables to arrive at a predictive score. oped prognostic indexes that combine bilirubin with ries. In an analysis of patients enrolled in the Canadian multicenter trial, the Mayo score was calculated before The European model 3 uses serum bilirubin, serum al- and after treatment with UDCA. After treatment, the bumin, age, the presence of cirrhosis and cholestasis Mayo score continued to divide patients with PBC into on liver biopsy, and azathioprine use. The Yale model groups with varying risk. In addition, the serum biliru- combines age, serum bilirubin, hepatomegaly, and the bin alone was shown to do the same even after the intro- presence of portal fibrosis or cirrhosis. 4 A third model duction of treatment with UDCA. A second objective was developed for nonalcoholic cirrhosis and PBC uses seto establish whether UDCA had an effect on long-term (2- to 6-year) survival in patients with PBC. (HEPATOLOGY rum bilirubin, serum albumin, age, hepatitis B surface 1996;23: ) antigen, neurological complications, varices, Quicktime prolongation, ascites, and clinical icterus. 5 Primary biliary cirrhosis (PBC) is a chronic progresploys serum bilirubin, serum albumin, age, prothrom- The Mayo group 6 devised a further model which emsive cholestatic liver disease for which the only definibin time, and the presence of edema. The Mayo model tive treatment is orthotopic liver transplantation. One of the most difficult questions in the management of was based on data from a group of 312 patients inpatients with PBC is when to intervene with transnally cross-validated. 7 volved in a trial of D-penicillamine and has been exter- plantation to optimize quality and length of life. Sev- All of the models mentioned above use the patient s data collected at the time of referral to predict the remaining life span. Both the European and Mayo models Abbreviations: PBC, primary biliary cirrhosis; UDCA, ursodeoxycholic acid. have been revised to allow input of data from follow-up From the 1 Departments of Medicine, University of Toronto, Toronto, Onvisits to refine predictions. 8,9 Use of these new models tario; 2 Clinical Epidemiology Unit, The Toronto Hospital, Toronto, Ontario; seems to improve the ability to predict survival over 3 Department of Medicine, Royal Alexandria Hospital, Edmonton, Alberta; 4 University of Western Ontario, London, Ontario; 5 University of Manitoba, the short term (õ2 years) and thus to time the trans- Winnipeg, Manitoba; 6 University of Ottawa, Ottawa, Ontario; 7 University of plantation. British Colombia, Vancouver, British Colombia; 8 University of Calgary, Cal- Recently, ursodeoxycholic acid (UDCA) has been gary, Alberta; 9 Dalhousie University, Halifax, Nova Scotia; and 10 University of Saskatoon, Saskatoon, Saskatchewan, Canada. used in several trials as therapy for patients with Received February 3, 1995; accepted December 27, PBC All trials have consistently shown that UDCA Supported by grants from The Medical Research Council of Canada, MA- effectively lowers serum bilirubin levels. In the Cana , April 1988 to July 1993, Physician s Services, Inc., grant 90-27, May dian multicenter trial, patients treated with UDCA for 1, 1990 to April 30, 1992, and the Canadian Liver Foundation, June 1994 to August years had a significantly lower total serum bilirubin Address reprint requests to: E. Jenny Heathcote, M.D., The Toronto Hospi- than controls averaging a difference of greater than tal, Western Division, WW 4-828, 399 Bathurst St., Toronto, Ontario, M5T 37%. The maximal effect of UDCA on serum bilirubin 2S8 Canada. levels is seen within 3 months of the start of therapy. 14 Copyright 1996 by the American Association for the Study of Liver Diseases. Although UDCA has been shown to have a beneficial /96/ $3.00/0 biochemical effect, debate continues as to whether 1148
2 HEPATOLOGY Vol. 23, No. 5, 1996 KILMURRY ET AL UDCA enhances long-term survival and slows the progression TABLE 1. Mean of Mayo Model Risk Variables at Baseline of the disease A recent combined analysis Mayo Model Canadian Trial that pooled data from 553 patients involved in the three (n Å 418) (n Å 222) largest trials of UDCA showed that UDCA has a signifi- Age (yr) 50.7 { { 11.8 cant effect on survival. 19 Total bilirubin (mmol/l) 54.4 { { 53.1* Because serum bilirubin is used in all described PBC Serum albumin (G/L) 35.0 { { 5.0 prognostic models, the question arises as to whether Prothrombin time (s) 10.7 { { 1.2 the models are still applicable in patients treated with Mayo risk score 5.07 { { 1.3 UDCA. More specifically, does the Mayo model still separate patients into high-, medium-, and low-risk * Data not normally distributed; median total bilirubin was 18 mmol/l. groups with differing survival curves? To test the validity of the Mayo model, data from the 2-year Canadian multicenter trial of UDCA, in addition to extended folof the Mayo model risk scores: low risk, õ5.37; intermediate low-up of up to 6 years, was used. Because the average length of follow-up was greater than 2 years, the origiscore limits were reported by Grambsch et al. 7 when cross- risk, between 5.37 and 6.42; and high risk, ú6.42. These risknal Mayo model was used, as opposed to the new timevalidating the Mayo model. The Mayo risk scores were deterdependent model. 9 Predictive curves from the Mayo mined for each patient at entry into the trial, at 3 months, model at baseline, at 3 months, and at 6 months were and at 6 months when the maximum decrease in serum bilicompared with the actual survival curves. rubin was evident. 12,14 The mean serum bilirubin for each In addition, the accrual of long-term follow-up data risk group at each time was compared between UDCAtreated on the survival status of patients involved in the trial groups and placebo groups to show the effect of UDCA afforded the opportunity to look at the effects of UDCA on these levels. The Kaplan-Meier 20 survival curve was plot- on survival for a period of up to 6 years. ted for each group, and the equality over strata was tested using the log-rank test. PATIENTS AND METHODS For comparison, the average predicted Mayo model survival curve was plotted for each risk group. The probability Data from 222 patients enrolled in the Canadian random- of survival at each year was calculated for every patient using ized controlled trial of UDCA were used. Eligibility for this the Mayo model. Within each risk group, the mean of these trial was based on standard biochemical, serological, and his- values was derived and graphed against time. tological criteria. 14 Patients were entered into the trial be- Survival was also correlated with serum bilirubin alone. tween April 1988 and July 1990; 111 patients were random- Patients were again divided into three risk groups according ized to UDCA and 111 to placebo. The patients were observed to Shapiro et al. 1 : low risk (serum bilirubin õ34 mmol/l); at 3-month intervals for 24 months. During each visit, blood intermediate risk (between 34 mmol/l and 102 mmol/l); and samples were obtained to evaluate serum bilirubin, alkaline high risk (ú102 mmol/l). Analysis was performed at both 0 phosphatase, aminotransferases, cholesterol, albumin, pro- and 6 months to determine the effect of lowering bilirubin thrombin time, complete blood cell count, and bile acids. Reg- levels after the introduction of UDCA therapy. The Kaplanular clinical assessment was performed to detect signs of Meier survival curve was computed for each group and the hepatic decompensation such as ascites, encephalopathy, and equality over strata was tested using the log rank test. peripheral edema. Survival analysis was performed using the data gathered Upon completion of the randomized controlled trial, the between 1988 and A Kaplan-Meier plot of the original first 100 patients randomized were offered the opportunity placebo group was compared with a plot of the original treatto enter an open trial of treatment with UDCA. Ninety-one ment group using end-points updated to August The of the 100 patients agreed to participate and were followed groups were compared using the log rank test. at 3 monthly intervals for a further 2 years, until July Between June 1994 and August 1995, the status of the RESULTS patients who were originally enrolled in the randomized trial The characteristics of patients in this trial and the was reviewed. This follow-up involved record review and teleoriginal study used to develop the Mayo model are phone contact with physicians to determine survival status, occurrence of liver transplantation, and UDCA use. In addiaverage, about 5 years older and had lower baseline shown in Table 1. 7 The Canadian patients were, on tion, it was ascertained that no patients received methotrexrisk scores. ate or colchicine. Survival analysis was calculated from the date of entry into the randomized controlled trial to the date Mayo risk scores were calculated for 203 of the 222 of death or transplantation. All deaths, whether due to liver- patients at baseline and for 188 patients at 6 months. related causes or not, were treated as failures. Patients who Of the 19 scores not calculated at baseline, 2 were bereceived a liver transplant were considered failures at the cause of missing bilirubin levels, 3 were a result of time of the transplantation. Patients lost to follow-up were missing albumin levels, 8 were because of missing procensored at the last known date of contact. thrombin times, and 6 were a result of missing edema The original patients from the development of the Mayo scores. At 6 months, the uncalculated scores were a model were compared with the patients in the Canadian study with respect to the parameters that constitute the result of 7 missing bilirubin levels, 4 missing albumin Mayo risk score. 7,14 levels, 3 missing prothrombin times, 7 missing edema To assess the usefulness of the Mayo model after treatment scores, 8 patient withdrawals, and 5 deaths. At basewith UDCA, patients in the placebo group and the treatment line for those randomized to UDCA, 77 patients were group were each divided into three risk groups on the basis in the low-risk group, 10 were in the medium-risk
3 1150 KILMURRY ET AL. HEPATOLOGY May 1996 TABLE 2. Mean Serum Bilirubin Levels According to Mayo Risk Group at Baseline and 6 Months for Placebo-Treated Patients Baseline 6 Months Mayo Risk Group (mmol/l) (mmol/l) Low 17.8 { { 13.8 Medium 49.6 { { 99.6 High 98.7 { { 66.7 group, and 13 were in the high-risk group. For those randomized to placebo, there were 79 patients in the low-risk group, 12 in the medium-risk group, and 12 FIG. 1. Comparison of actual survival (estimated by Kaplanin the high-risk group. At 6 months, the numbers of UDCA-treated patients distributed between the three groups were 74, 10, and 10, respectively. The number of placebo patients distributed between the three groups were 72, 11, and 11, respectively. Meier) with the average Mayo model predicted survival for the placebo group at baseline. long-term follow-up in the groups as originally random- Tables 2 and 3 show the mean serum bilirubin levels ized. In the group originally randomized to UDCA for each Mayo risk group at baseline and 6 months. treatment, there were 30 patients with calculated After treatment with UDCA for 6 months, the serum Mayo risk scores who reached endpoint (19 deaths and bilirubin levels fell in all three UDCA groups, while in 11 transplants). In the low-risk group, 1 patient died the placebo groups, the bilirubin levels rose. Because of each of the following diseases: pancreatic cancer, the bilirubin values are skewed, the standard devia- cardiovascular disease, breast cancer, tuberculosis, tions are large. lung cancer, asthma, and liver disease; 4 patients un- For those randomized to placebo, the Mayo model derwent liver transplantation. The medium-risk group divided the patients into three distinct groups with dis- consisted of 3 deaths, all due to liver disease, and 5 tinct survival curves. The log rank test at both baseline patients who underwent liver transplantation. In the and 6 months showed that the three curves were statis- high-risk group, 8 patients died as a result of liver tically significantly different (P õ.0001). Comparison disease, 1 died of congestive heart failure, and 2 underwith the predicted curves provided a reasonable fit went liver transplantation. Of those patients receiving (Figs. 1 and 2). In the UDCA-treated group, the three UDCA, 1 patient who died and 4 who received transgroups again had distinct survival curves at baseline plants were not included in the analysis because data and 6 months, and the survival curves were statisti- needed to calculate Mayo risk scores were missing. cally distinct (P õ.0001) (Fig. 3). The predicted curves The group originally randomized to placebo had 34 showed a good match with the actual survival curves events (12 deaths and 22 transplants). In the low-risk after 6 months of treatment with UDCA (Fig. 4). The group, 1 patient died of each of the following diseases: analysis at 3 months was very similar to that at 6 cardiovascular disease, pneumonia, lymphoma, a months; therefore, it was not included. When the pa- stroke, viral meningitis, and liver disease; 9 patients tients were divided into three risk groups according to their serum bilirubin levels, the survival curves remained distinct in both the UDCA-treated and placebo patients at 6 months into the trial (Figs. 5 and 6). In addition, the curves were statistically different for both groups (P õ.0001). At baseline, the graphs were very similar to the graphs at 6 months; thus, they too were excluded. Figure 7 shows the probability of survival over the TABLE 3. Mean Serum Bilirubin Levels According to Mayo Risk Group at Baseline and 6 Months for UDCA-Treated Patients Baseline 6 Months Mayo Risk Group (mmol/l) (mmol/l) Low 18.6 { { 16.9 Medium 49.5 { { 16.1 High { { 87.5 FIG. 2. Comparison of actual survival (estimated by Kaplan- Meier) with the average Mayo model predicted survival for the placebo
4 HEPATOLOGY Vol. 23, No. 5, 1996 KILMURRY ET AL FIG. 3. Comparison of actual survival (estimated by Kaplan- Meier) with the average Mayo model predicted survival for the UDCA group at baseline. FIG. 5. Plot of survival (estimated by Kaplan-Meier) after dividing into risk groups, according to serum bilirubin for the placebo underwent liver transplantation. The medium-risk group consisted of 4 deaths, all due to liver disease; 5 received liver transplants. In the high-risk group, 2 patients died as a result of liver disease and 8 under- went liver transplantation. In the placebo group, 5 patients who died were not included in the analysis be- cause data needed to calculate Mayo risk scores were missing. Two placebo patients and 1 UDCA patient underwent transplantation for intractable pruritus while the rest received a transplant for end-stage liver disease. The mean length of follow-up for all patients was 3.95 years (range, years). Of the original 222 patients, 13 UDCA-treated patients and 14 placebo patients were lost to follow-up at some point after com- pletion of the trial. The probability of survival with 2 years of treatment with UDCA was not significantly different from the group randomized to placebo when follow-up was continued for 6 years (P ú.05); however, the sample size of the trial was not designed to allow for survival analysis. Sixty-one of those patients originally in the treatment group continued treatment with UDCA after com- pletion of the trial at 2 years, whereas 35 of those origi- nally in the treatment group stopped UDCA for at least 6 months after completion of the trial. Fifty-three pa- tients received UDCA for at least 6 months after they had completed 2 years on placebo in the trial. Thirtynine patients never received UDCA. We were unable to establish what treatment the other 34 patients received after completing the trial. DISCUSSION The original Mayo model was developed to predict survival probability of patients with PBC at initial di- agnosis, allowing for appropriate counseling and edu- cation of patients and their families. 6 Subsequently, it has also been used as a guide to help predict the appropriate time to intervene with transplantation. The methods described above are the same as those used in the original development of the model with the exception that liver transplantations as well as deaths were considered failures in the present study. 6 Patients from the population originally used to create the Mayo model died without transplantation. Because the model has been recommended to time the need for transplantation, we decided to consider patients receiving transplants as endpoints. FIG. 4. Comparison of actual survival (estimated by Kaplan- FIG. 6. Plot of survival (estimated by Kaplan-Meier) after dividing Meier) with the average Mayo model predicted survival for the UDCA into risk groups, according to serum bilirubin for the UDCA
5 1152 KILMURRY ET AL. HEPATOLOGY May 1996 the beneficial effect of UDCA on PBC. Another study suggested that the serum hyaluronic acid value and the serum level of type III amino terminal peptide of procollagen served as better predictors than serum bilirubin and the Mayo score 21 ; however, these laboratory tests are not routinely available. The long-term survival of patients treated with UDCA versus those who were initially randomized to placebo showed no significant difference at 2 years (Fig. 7), because the sample size of this study was not designed to assess an effect on survival. Using the intent to treat principle in this study, no survival advantage was observed at 4 or 6 years; however, after the initial FIG. 7. Time to end-point using Kaplan-Meier estimates, according to the groups as initially randomized (P ú.05). open trial of UDCA, others continued or started UDCA 2 years of randomization, some patients entered an outside the open trial, and still others stopped or never began UDCA. The collaborative analysis pooled results The Mayo model effectively divided the placebo- and from 553 patients in three studies using the same dose UDCA-treated patients at baseline and at 6 months of UDCA and showed a distinct survival advantage in into three groups with distinct survival curves. Herein favor of the patients originally randomized to the lies the usefulness of the Mayo model. There was rea- UDCA group. 19 sonable matching of the actual survival curves of the The number of patients referred to this UDCA trial placebo group with the Mayo-model predicted curves who were in the medium- and high-risk categories for (Figs. 1 and 2). The imperfect match may be because the Mayo risk score or for serum bilirubin alone were the patients in our randomized controlled trial had much smaller than for the low-risk groups. This was lower risk scores than the original Mayo patients used probably because subjects in these categories were to create the model. In particular, the trial patients more likely to be referred for liver transplantation had significantly lower serum bilirubin levels (Table rather than for a 2-year randomized controlled trial. 1), because patients with high bilirubin levels were re- Although both the Mayo risk score and serum bilirubin ferred for transplantation rather than a clinical trial. appeared reliable predictors at baseline and 6 months As a result, there were far fewer patients entered into from visual inspection of the survival plots, the small the trial with medium- and high-risk scores at baseline numbers of medium- and high-risk patients make it as compared with the numbers in the low-risk group. difficult to assess performance of the model for the upper-risk Additionally, because patients receiving transplants groups. Other factors should be taken into con- were considered endpoints thus preceding their sub- sideration when assessing a high-risk patient for suitability sequent deaths the Mayo model would be expected for liver transplantation. to underestimate risk. At the present time, UDCA is the most promising The results of applying the Mayo model to patients drug for the treatment of PBC, as shown by the recent treated with UDCA supports the usefulness of the collaborative analysis. 19 The observation that the Mayo model for predicting survival (Fig. 4). Although UDCA model and serum bilirubin remain useful in differenti- has a definite effect on serum bilirubin levels, the ating low-, medium-, and high-risk patients after treatment effect does not eliminate the predictive power of the with UDCA supports the value of these prognoseffect model. The continued success of the model in differenti- tic markers. ating low-, medium-, and high-risk patients suggests that it is still a useful tool for the monitoring of disease Acknowledgment: Study medications were kindly progression, even in patients on UDCA therapy. 7 provided by Interfalk Canada and Jouveinal Inc., Que- Serum bilirubin levels for the different Mayo risk bec, Canada. groups were what would be expected at baseline and 6 months in the placebo and UDCA groups, given the REFERENCES effect of UDCA on serum bilirubin (Tables 2 and 3). 1. Shapiro JM, Smith H, Schaffner F. Serum bilirubin: a prognostic Total serum bilirubin was used to divide the patients factor in primary bilirubin cirrhosis. Gut 1979;20: into three groups according to risk. 1 After the introducral 2. Neuberger J, Gunson B, Buckels J, Elias E, McMaster P. Refertion of patients with primary bilirubin cirrhosis for liver trans- of treatment with UDCA, the survival curves replantation. 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