Primary biliary cirrhosis (PBC) and primary sclerosing
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1 Mortality Attributable to Cholestatic Liver Disease in the United States Flavia D. Mendes, 1 W. Ray Kim, 2 Rachel edersen, 3 Terry Therneau, 3 and Keith D. Lindor 2 In the past 2 decades, important advances have been made in the treatment of cholestatic liver diseases, including primary biliary cirrhosis (BC) and primary sclerosing cholangitis (SC). Whether these new therapies have had demonstrable impact on mortality on a population-wide scale has not been evaluated. This study describes the age-specific and sex-specific mortality rates from BC and SC in the United States between 1980 and 1998, based on the Multiple Cause of Death files. Age-specific and sex- specific mortality rates from BC and SC were calculated. The multivariable oisson model was used to evaluate temporal changes in mortality rates. In 1998, the total age-adjusted and sex-adjusted BCrelated mortality rate was 0.24 per 100,000, and the age-adjusted and sex-adjusted SCrelated mortality rate was 0.23 per 100,000. During the observation period, BC-related mortality significantly decreased over time in women younger than 65 years, and in men of all age groups, whereas in older women this number increased over time. SC-related mortality remained essentially stable, except in men 65 years of age or older. Conclusion: Since the early 1980s, significant changes in mortality from BC have occurred. The most noticeable change was an increase in the age of death, which indicates prolongation of survival. These changes may be attributable to liver transplantation or ursodeoxycholic acid. In contrast, mortality from SC remained largely unchanged, highlighting the need for more effective therapeutic strategies. (HEATOLOGY 2008;47: ) rimary biliary cirrhosis (BC) and primary sclerosing cholangitis (SC) are chronic cholestatic disorders of the liver. BC is characterized histologically by portal inflammation and immune-mediated destruction of the intrahepatic bile ducts and serologically by the presence of antimitochondrial antibodies. 1 SC is characterized by progressive destruction of intrahepatic and extrahepatic bile ducts. 2 BC is a disease that affects primarily women, in a 9:1 ratio. The median age of diagnosis is 50 years (range, years). 1,3 In the first population-based study in the Abbreviations: MRR, mortality rate ratio; OLT, orthotopic liver transplantation; BC, primary biliary cirrhosis; SC, primary sclerosing cholangitis; UDCA, ursodeoxycholic acid. From the 1 Center for Liver Diseases, University of Miami Miller School of Medicine, Miami, FL; the 2 Division of Gastroenterology and Hepatology, Mayo Clinic College of Medicine; and the 3 Division of Biostatistics, Mayo Clinic College of Medicine, Rochester, MN. Received May 4, 2007; accepted December 6, Supported by grants from the National Institute of Diabetes and Digestive and Kidney Diseases (DK-34238, DK-61617). Address reprint requests to: W. Ray Kim, M.D., Division of Gastroenterology and Hepatology, 200 1st Street SW, Rochester, MN kim.ray@mayo.edu; fax: Copyright 2007 by the American Association for the Study of Liver Diseases. ublished online in Wiley InterScience ( DOI /hep otential conflict of interest: Nothing to report. United States, Kim et al. 4 reported an incidence of BC of 2.7 per 100,000 person-years and a prevalence of 40.2 per 100,000 persons. Based on these data, it was estimated that there would be 47,000 prevalent cases of BC in the US white population and that approximately 3,500 new cases would be diagnosed each year. 4 The overall median survival ranges between 10 and 15 years, with disease progression being more likely in patients with symptomatic disease, even though asymptomatic patients still have a lower overall median survival compared with an agematched and sex-matched healthy population. 1,3 In a study by rince et al., 5 only one-third of the deaths in asymptomatic patients with BC were liver related. Several reports demonstrate an increased risk of hepatocellular carcinoma in patients with BC; however, the crude frequency of hepatocellular carcinoma is still low at 0.7% to 3.6% (5.9%-11.1% in patients with advanced BC). 6-8 Although the incidence of BC in the United States has not changed for the past 20 years, 4 at least 2 therapeutic modalities have been shown to be effective in treating patients with BC. These include orthotopic liver transplantation (OLT) and ursodeoxycholic acid (UDCA). Liver transplantation, shown to improve survival of patients with end-stage liver disease from BC, 9 has been used widely in BC patients since the mid-1980s. UDCA 1241
2 1242 MENDES ET AL. HEATOLOGY, April 2008 therapy slows disease progression and reduces the need for liver transplantation in patients with BC. 10 It was approved in the United States for BC in 1997, although its effectiveness had been reported in the literature as early as With these significant advances in the treatment of BC, improvement in survival of patients with BC is expected. However, such impact on BC-related mortality has not been evaluated on a population-wide scale. SC affects men more commonly than women, and the median age of diagnosis is approximately 40 years. The median survival is 12 years from diagnosis. Its association with inflammatory bowel disease is well known. 2 In a US population-based study, the estimated overall age-adjusted and sex- adjusted incidence of SC was 0.90 per 100,000 person-years (1.25 in men and 0.54 in women), and the prevalence was 13.6 per 100,000 (20.9 men and 6.3 women). In this study, the estimated 10-year survival of patients with SC was 65%, compared with an expected survival of 94%. 12 Cholangiocarcinoma is the most feared complication and occurs in 7%-15% of patients with SC, with an annual incidence of 0.5% to 1%. Liver transplantation has achieved overall excellent outcomes, including long-term survival and improvement in quality of life in patients with advanced SC. 13 However, SC tends to recur in the allograft, which sometimes leads to graft failure, retransplantation, or death. 14 Furthermore, no medical treatment has been shown effective in slowing disease progression or time to liver transplantation in patients with SC. 15 In practice, however, UDCA may be being used off label, although its efficacy in patients with SC has not been demonstrated. 16 In this study, we used detailed death certificate data to describe the age-specific mortality rates from BC and SC in the United States between the years of 1980 and 1998 and to evaluate their time trends. The comparison between BC and SC provides helpful insight into the impact of advances in therapy for these diseases over time. atients and Methods Data Source. Data on mortality were obtained from the Multiple Cause of Death files, which comprise all death certificates issued in the United States (approximately 2 million annually). Data on all calendar years between 1980 and 1998 were obtained from the National Center for Health Statistics (Hyattsville, MD). Available data elements included age (in 5-year increments), sex, race (white, African, and other), and place of birth and death, and all listed (immediate, contributing, and underlying) causes of death on the death certificate. The timeframe of analysis ( ) was chosen because the diagnostic coding system used for the data was consistent during the period; the coding system was changed to the International Classification of Diseases 10th version (ICD-10) in Case Ascertainment. The Multiple Causes of Death files used the International Classification of Diseases 9th version (ICD-9) for diagnostic coding. Death records with a BC diagnosis was identified with the code 5716 (biliary cirrhosis), whereas the code 5761 (sclerosing cholangitis) was used for SC deaths. We considered a death BC-related or SC-related if either diagnosis was listed as the underlying or immediate cause of death or underlying/immediate cause of death was cirrhosis, portal hypertension and its complications (esophageal varices, ascites, hepatorenal syndrome, hepatic coma), hepatocellular carcinoma/cholangiocarcinoma, acute liver failure, or unspecified disorder of liver, and BC or SC was also listed as a contributing cause of death. Records in which BC or SC was listed but the immediate or underlying cause of death was not liver related were thought to represent deaths in which BC or SC was incidental and did not contribute to the death. Data Analysis. Data from the Multiple Cause of Death file were analyzed using SAS version 8.2 (SAS Institute Inc., Cary, NC). Mortality rates, namely incidence rates of deaths, attributable to BC or SC were calculated, considering the entire population of the United States to be at risk. Denominator age-specific, sex-specific, and race-specific person-years were based on the 2000 census. For the estimation of data variability, we assumed that, given a fixed number of person-years, the number of cases would follow a oisson distribution, which allowed the estimation of standard errors and the calculation of 95% confidence intervals for the mortality rates. Because there were only a small number of decedents of nonwhite race, all races were combined in the estimation of mortality rates and subsequent analyses. Also, only those deaths in which the age was 20 years or older were included in the analysis. The impact of age, sex, and calendar year was examined using the generalized linear model assuming a oisson error structure. In the oisson analysis modeling, both BC-related death and SC-related death, the natural log of the national population for a given age/sex combination was used as an offset. Thus, all models are age-adjusted and sex-adjusted to the national population. Interactions among these variables were examined to define whether there were differences in the temporal trend in incidence rates of BC-related and SC-related death across sex.
3 HEATOLOGY, Vol. 47, No. 4, 2008 MENDES ET AL Results Table 1. Mortality Attributable to BC and SC BC SC Number of all deaths 11,860 23,985 Number of deaths attributable to the disease 7,913 (67%) 8,081 (34%) Mean age at death in years Age group (1.2%) 41 (0.5%) (1.9%) 361 (4.5%) ,459 (31.1%) 1,992 (24.6%) 65 5,210 (65.8%) 5,687 (70.4%) Sex Female Male 6,414 (81.1%) 4,159 (51.5%) Race White 7,417 (93.7%) 7,145 (88.4%) African 360 (4.5%) 680 (8.4%) Other (Asian, acific Islander, Native American, and Alaskan) 136 (1.7%) 256 (3.2%) Concomitant cirrhosis/portal hypertension diagnosis 6,020 (76.1%) 3,901 (48.3%) Concomitant HCC/CCC diagnosis 230 (3%) 1,002 (12.4%) HCC, hepatocellular carcinoma; CCC, cholangiocarcinoma. Deaths of BC and SC. A total of 11,860 records of potential BC-related deaths were found in the Multiple Cause of Death file, but only 7,913 (67%) met our definition of BC-related death and were included in the analysis. Of those, 6,414 (81.1%) were women, and 1,499 (18.9%) were men. The mean age at death was 65.6 ( 13.9) years. Most were of white race (93.7%). African- Americans accounted for 4.5%; others, which included Asian, acific Islander, Native American, and Alaskan, for 1.7% (Table 1). A total of 23,985 records of potential SC-related deaths were found in the Multiple Cause of Death file, but only 8,081(34%) met our definition of SC-related death and were included in the analysis. Of those, 4,159 (51.5%) were men, and 3,922 (48.5%) were women. The mean age at death was 68.8 ( 16.2). Most were of white race (88.4%), African-Americans accounted for 8.4%, and others, which included Asian, acific Islander, Native American, and Alaskan, for 3.2% (Table 1). The total age-adjusted BC-related mortality in 1998 was per 100,000. As expected, BC mortality was much higher in women (0.365 per 100,000) than in men (0.082 per 100,000). In contrast, mortality attributable to SC was higher in men (0.271 per 100,000) than in women (0.186 per 100,000), with the sex difference being much less dramatic with SC than with BC. The total age-adjusted SC-related mortality in 1998 was per 100,000. Time Trends in BC-Related and SC-Related Mortality. Figure 1 illustrates age-specific mortality for women and men for representative calendar years (1980, 1986, 1992, and 1998). In general, mortality from BC increased with age in both sexes. In women, BC mortality in the 1980s had a bimodal pattern, with a first peak in the late 50s and early 60s and the second rise in the 70s. Into the 1990s, the first peak disappeared, giving rise to a pattern of uniform increase with age. BC mortality in men did not show a consistent pattern, in part because of the fewer number of deaths. Figure 2 displays the same information for SC mortality. Mortality attributable to SC also increased with age. There did not seem to be any longitudinal pattern to SC mortality in men or women. Trend in mortality is further analyzed in Figs. 3 and 4, which show mortality rates by calendar year. Figure 3 demonstrates that in women between 40 and 64 years of age, death attributable to BC decreased from 0.4 per 100,000 in 1980 to 0.2 per 100,000 in In contrast, in women in the older age group ( 65 years), the rate increased over time from 0.93 per 100,000 in 1980 to 1.48 per 100,000 in In the youngest age group, the Fig. 1. BC-related deaths for females and males. BC, primary biliary cirrhosis.
4 1244 MENDES ET AL. HEATOLOGY, April 2008 than that in women aged 20 to 39 years (41.7 1/MRR, MRR 0.024). With regard to a time trend, in women older than 65 years of age, each decade in calendar year was associated with a 29% increase in BC mortality, whereas in younger women, the mortality rate decreased by approximately half (MRR 0.53). In men, as in women, BC mortality increased with age. BC mortality in men showed a significant reduction over time, regardless of their age, although the decrease was more pronounced in the 40 to 64 and 20 to 39 age groups (MRR 0.42 and 0.48, respectively) than in the older counterpart (MRR 0.78). Mortality attributable to SC also increased significantly with age in both men and women. Overall, there was much less noticeable calendar year effect in SC mortality. The model did show that the SC mortality decreased significantly in women between 40 and 64 years of age and men older than 65 years. However, the effect size was small (0.85 for the former and 0.90 for the latter). Fig. 2. SC-related deaths for females and malesw. SC, primary sclerosing cholangitis. low mortality rate makes it difficult to appreciate a trend graphically; however, the oisson model also showed a decrease over time (see later discussion). In men 40 to 64 years of age, the BC death rate decreased from 0.1 per 100,000 in 1980 to 0.03 per 100,000 in Mortality rates also decreased in men of the other age groups. With regard to SC, Fig. 4 shows that the death rate in men older than 65 years of age decreased over time from 1.5 per 100,000 in 1980 to 0.93 per 100,000 in In men of the other age groups, SC mortality did not change over time. In women, there was no discernible trend in SC mortality. These findings were formally examined in oisson regression models, shown in Tables 2 (BC) and 3 (SC). The mortality rate ratio (MRR) calculation showed that BC mortality in women increased with age. For example, BC mortality in women older than 65 years was 1.77 times higher than that in women aged 40 to 64 years (1.77 1/MRR, MRR 0.56), and 41.7 times higher Discussion Several epidemiological factors may contribute to changes in mortality rates of a given disease. First, if the disease incidence changes, morbidity and mortality secondary to the disease will be affected accordingly. In the case of BC and SC, there is no firm evidence that their incidence has changed over time. 4,12 Second, if there is a shift in disease severity affecting the case fatality rate, mortality rates in the population may change, even if the incidence remains the same. Third, similarly, if there is effective treatment that alters survival of patients, it may alter mortality rates. In the case of cholestatic liver diseases, therapeutic modalities that may have affected mortality rates on the population level include liver transplantation and UDCA. Liver transplantation has been widely used since the mid-1980s, and it has been shown to be an effective treatment for end-stage liver disease caused by both BC and SC, with excellent outcomes reported. Survival after liver transplantation for BC are on the order of 85%- 90% and 70%-80% after 1 and 5 years, 17 respectively, and for SC, reported 1-year and 5-year survival rates are as high as 94% and 86%, respectively. 18 UDCA has been shown in randomized controlled trials to delay disease progression and to improve survival free of liver transplantation in patients with BC, especially for those started on treatment while early-stage disease is present. 10,19-24 UDCA also has been actively studied for the treatment of SC; however, no effect on delaying disease progression or the need for liver transplantation has been shown, 25 and further studies are on-
5 HEATOLOGY, Vol. 47, No. 4, 2008 MENDES ET AL Fig. 3. Time trend in BC-related mortality. BC, primary biliary cirrhosis. going, looking at the effects of high-dose UDCA in these patients. Because the incidence of BC in the United States has remained stable for the past 20 years, 4 the trend observed in BC-related mortality suggests that there was a beneficial effect of both OLT and UDCA. The mortality change observed in the mid-1980s is probably attributable to the more widespread use of liver transplantation. The stronger effect noted in younger women may be explained by the fact that younger patients are more likely to undergo liver transplantation. One may speculate that the increased mortality observed in older women could represent an effect of UDCA on delaying disease progression; however, because disease progresses at an older age, these patients may be less likely to benefit from liver transplantation. However, UDCA s effect might be more readily determined in a future study that looks at similar rates in the decade after its approval and more widespread use ( ). Interpretation of data on SC is more difficult than that for BC. In spite of the significant -values in the oisson models, inspection of Figs. 3 and 4 shows that the curves for SC are largely flat over time. The less pronounced time trend on SC-related mortality may represent the lack of medical treatment that is able to impact on disease progression. Another possible explanation is the fact that the death certificate data for sclerosing cholangitis include an unknown proportion of non-sc cases. otential scenarios of secondary sclerosing cholangitis that may be included in the data are cases of bile duct complications after surgery of the gallbladder or bile ducts and those of cholangiocarcinoma occurring in non-sc patients. Because of the rapid adoption of laparoscopic surgery during the 1980s and 1990s, there may have been Fig. 4. Time trend in SC-related mortality. SC, primary sclerosing cholangitis.
6 1246 MENDES ET AL. HEATOLOGY, April 2008 Table 2. BC-Related Deaths Females Males Age group [0.019, 0.034] [0.011, 0.032].01 Age group [0.51, 0.62] [0.25, 0.37].01 Age group Calendar year 0.53 [0.37, 0.77] [0.26, 0.86] Calendar year 0.53 [0.49, 0.58] [0.36, 0.50] Calendar year 1.29 [1.22, 1.36] [0.69, 0.87].01 NOTE. Calendar year is in decades. The MRR for the age groups, as well as the -values, use the older age group as a reference group. an increased incidence of secondary sclerosing cholangitis, which may in part explain the high proportion of SC-related deaths in women, not in keeping with the male preponderance of the disease. Mortality from those patients may have obscured a reduction in mortality in patients with SC, for example, secondary to OLT. Conversely, cholangiocarcinoma occurring in older patients without SC may have been erroneously classified as SC in the past, which may occur less frequently as diagnostic accuracy improves over time. This may have produced a trend in the reduction of mortality in the older age group. One may note a noticeable discrepancy between the estimated number of incident cases (for example, 3,500 new BC cases per year among white Americans 4 ) versus the number of deaths reported here (for example, 470 BC deaths per year on average). There may be several explanations for this gap between the incidence and mortality for BC and SC. First, there are patients with asymptomatic disease that remains undiagnosed at the time of death. The frequency with which this occurs may not be estimated based on currently available data. Second, it is well known that even patients with symptomatic BC do not die of liver-related causes. According to rince et al., 5 31% and 57% of deaths in BC patients are liver related in asymptomatic and symptomatic patients, respectively. In the current data, 7,913 of 11,860 deaths (67%) in subjects with a BC diagnosis were determined to be liver related. Clearly, not all patients with BC die of it, and death certificates of decedents who had BC but did not die of it may lack the BC diagnosis. Third, the Olmsted County population from which the estimates for BC and SC incidence was derived was predominantly of Scandinavian descent, the geographic area with the highest reported incidence of BC. 26 Finally, the death certificate data entail inaccuracies, and relevant deaths may have been omitted or misclassified. 27 As pointed out earlier, this bias is likely greater for SC deaths. In summary, the impression that the death rate for BC/SC appears to be only a fraction of their estimated incidence is likely a result of several factors, including lack of diagnosis, deaths of causes unrelated to their liver disease, and geographic heterogeneity of the US population. It is likely that there is some underestimation in our data (that is, death certificate diagnosis) of the true mortality of liverrelated causes with diagnosed BC and SC. The magnitude of this underestimation remains unknown, and it represents the main limitation of this study. However, it must be pointed out that the main focus of the study is the time trend in mortality, not necessarily the absolute number of deaths. Thus, as long as this underestimation remains consistent over time, we believe that our observation about the trend is valid. The trend in the population-wide outcome of BC and SC observed in this study was recently corroborated Table 3. SC-Related Deaths Females Males Age group [0.019, 0.036] [0.017, 0.029].01 Age group [0.15, 0.20] [0.14, 0.18].01 Age group Calendar year 0.73 [0.53, 1.01] [0.89, 1.42] Calendar year 0.85 [0.75, 0.97] [0.93, 1.14] Calendar year 1.04 [0.98, 1.12] [0.84, 0.96].01 NOTE. Calendar year is in decades. The MRR for the age groups, as well as the -values, use the older age group as a reference group.
7 HEATOLOGY, Vol. 47, No. 4, 2008 MENDES ET AL by a study by Lee et al., 28 in which all patients who were registered or who underwent transplantation in the United States between 1995 and 2006 were analyzed. Their data are in support of this study in 2 ways. First, similar to our observation, there was a statistically significant decrease in the number of patients wait-listed for BC over time, whereas no such trend was seen with SC. Second, the average number of patients wait-listed for BC and SC in the United States was 368 and 465 per year, respectively. These numbers are similar to the number of deaths observed in this study, which indicate that our death certificate data are unlikely to be inaccurate by a large measure. In conclusion, over a nearly 2-decade period, significant changes in mortality were observed, the most pronounced of which was the decreased mortality observed in younger women ( 65 years old) with BC. We postulate that these trends are attributable to advances in the treatment of cholestatic liver diseases with the advent of OLT and UDCA for the treatment of BC. In contrast, the increased mortality in older women with BC points to the fact that those treatment modalities are not curative. Mortality trends in SC in general are less discernible, which may indicate lack of effective treatment options for patients with SC. References 1. Kaplan MM, Gershwin ME. rimary biliary cirrhosis. N Engl J Med 2005;353: Lee YM, Kaplan MM. rimary sclerosing cholangitis. N Engl J Med 1995; 332: Kaplan MM. rimary biliary cirrhosis. N Engl J Med 1996;335: Kim WR, Lindor KD, Locke GR 3rd, Therneau TM, Homburger HA, Batts K, et al. Epidemiology and natural history of primary biliary cirrhosis in a US community. Gastroenterology 2000;119: rince MI, Chetwynd A, Craig WL, Metcalf JV, James OF. 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A multicenter, controlled trial of ursodiol for the treatment of primary biliary cirrhosis. UDCA-BC Study Group. N Engl J Med 1991;324: Bambha K, Kim WR, Talwalkar J, Torgerson H, Benson JT, Therneau TM, et al. Incidence, clinical spectrum, and outcomes of primary sclerosing cholangitis in a United States community. Gastroenterology 2003; 125: Saldeen K, Friman S, Olausson M, Olsson R. Follow-up after liver transplantation for primary sclerosing cholangitis: effects on survival, quality of life, and colitis. Scand J Gastroenterol 1999;34: Maheshwari A, Yoo HY, Thuluvath J. Long-term outcome of liver transplantation in patients with SC: a comparative analysis with BC. Am J Gastroenterol 2004;99: LaRusso NF, Shneider BL, Black D, Gores GJ, James S, Doo E, et al. rimary sclerosing cholangitis: summary of a workshop. HEATOLOGY 2006;44: Harnois DM, Angulo, Jorgensen RA, Larusso NF, Lindor KD. Highdose ursodeoxycholic acid as a therapy for patients with primary sclerosing cholangitis. Am J Gastroenterol 2001;96: Carithers RL Jr. Liver transplantation. American Association for the Study of Liver Diseases. Liver Transpl 2000;6: Graziadei IW, Wiesner RH, Marotta J, orayko MK, Hay JE, Charlton MR, et al. Long-term results of patients undergoing liver transplantation for primary sclerosing cholangitis. HEATOLOGY 1999;30: Combes B, Luketic VA, eters MG, Zetterman RK, Garcia-Tsao G, Munoz SJ, et al. rolonged follow-up of patients in the U.S. multicenter trial of ursodeoxycholic acid for primary biliary cirrhosis. Am J Gastroenterol 2004;99: Corpechot C, Carrat F, Bahr A, Chretien Y, oupon RE, oupon R. The effect of ursodeoxycholic acid therapy on the natural course of primary biliary cirrhosis. Gastroenterology 2005;128: ares A, Caballeria L, Rodes J. Excellent long-term survival in patients with primary biliary cirrhosis and biochemical response to ursodeoxycholic acid. Gastroenterology 2006;130: oupon RE, Lindor KD, Cauch-Dudek K, Dickson ER, oupon R, Heathcote EJ. Combined analysis of randomized controlled trials of ursodeoxycholic acid in primary biliary cirrhosis. Gastroenterology 1997; 113: Shi J, Wu C, Lin Y, Chen YX, Zhu L, Xie WF. Long-term effects of mid-dose ursodeoxycholic acid in primary biliary cirrhosis: a meta-analysis of randomized controlled trials. Am J Gastroenterol 2006;101: ter Borg C, Schalm SW, Hansen BE, van Buuren HR. rognosis of ursodeoxycholic acid-treated patients with primary biliary cirrhosis: results of a 10-yr cohort study involving 297 patients. Am J Gastroenterol 2006; 101: Lindor KD. Ursodiol for primary sclerosing cholangitis. Mayo rimary Sclerosing Cholangitis-Ursodeoxycholic Acid Study Group. N Engl J Med 1997;336: Selmi C, Invernizzi, Zuin M, odda M, Gershwin ME. Genetics and geoepidemiology of primary biliary cirrhosis: following the footprints to disease etiology. Semin Liver Dis 2005;25: Manos MM, Leyden WA, Murphy RC, Terrault NA, Bell B. The limitations of conventionally-derived chronic liver disease mortality rates: results of a comprehensive assessment. HEATOLOGY. In press. 28. Lee J, Belanger A, Doucette JT, Stanca C, Friedman S, Bach N. Transplantation trends in primary biliary cirrhosis. Clin Gastroenterol Hepatol 2007;5:
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