Levels of alkaline phosphatase and bilirubin are surrogate end points of outcomes of patients with primary biliary cirrhosis: an international follow-up study
Open accessAbstract
Background & aims Noninvasive surrogate end points of long-term outcomes of patients with primary biliary cirrhosis (PBC) are needed to monitor disease progression and evaluate potential treatments. We performed a meta-analysis of individual patient data from cohort studies to evaluate whether patients' levels of alkaline phosphatase and bilirubin correlate with their outcomes and can be used as surrogate end points.Methods We performed a meta-analysis of data from 4845 patients included in 15 North American and European long-term follow-up cohort studies. Levels of alkaline phosphatase and bilirubin were analyzed in different settings and subpopulations at different time points relative to the clinical end point (liver transplantation or death).Results Of the 4845 patients, 1118 reached a clinical end point. The median follow-up period was 7.3 years; 77% survived for 10 years after study enrollment. Levels of alkaline phosphatase and bilirubin measured at study enrollment (baseline) and each year for 5 years were strongly associated with clinical outcomes (lower levels were associated with longer transplant-free survival). At 1 year after study enrollment, levels of alkaline phosphatase that were 2.0 times the upper limit of normal (ULN) best predicted patient outcome (C statistic, 0.71) but not significantly better than other thresholds. Of patients with alkaline phosphatase levels ≤ 2.0 times the ULN, 84% survived for 10 years compared with 62% of those with levels >2.0 times the ULN (P < .0001). Absolute levels of alkaline phosphatase 1 year after study enrollment predicted patient outcomes better than percentage change in level. One year after study enrollment, a bilirubin level 1.0 times the ULN best predicted patient transplant-free survival (C statistic, 0.79). Of patients with bilirubin levels ≤ 1.0 times the ULN, 86% survived for 10 years after study enrollment compared with 41% of those with levels >1.0 times the ULN (P < .0001). Combining levels of alkaline phosphatase and bilirubin increased the ability to predict patient survival times. We confirmed the predictive value of alkaline phosphatase and bilirubin levels in multiple subgroups, such as patients who had not received treatment with ursodeoxycholic acid, and at different time points after study enrollment.Conclusions Levels of alkaline phosphatase and bilirubin can predict outcomes (liver transplantation or death) of patients with PBC and might be used as surrogate end points in therapy trials.
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Alkaline phosphatase and total bilirubin are the two most important prognostic indicators in primary biliary cholangitis.
“In the current trial, bezafibrate was associated with a rapid and sustained decrease in alkaline phosphatase level and a parallel decrease in total bilirubin, the two most important prognostic indicators in primary biliary cholangitis.25”
From A Placebo-Controlled Trial of Bezafibrate in Primary Biliary Cholangitis (2018) · cites this paper as [25]
The Discussion (p. 11) says alkaline phosphatase and bilirubin strongly correlate with death and liver transplantation in patients with PBC, supporting their prognostic importance. The paper does not establish that they are the two most important indicators relative to other prognostic measures. The bezafibrate result is presented as the citing trial’s own finding, not as a finding attributed to this source. (LLM, conf=0.84)
Experimental — accuracy not yet measuredSerum bilirubin has been recognised since the 1970s as a major predictor of poor outcome in PBC.
“Serum bilirubin has been recognised since the 1970s as a major predictor of poor outcome in PBC [72,7].”
From EASL Clinical Practice Guidelines: The diagnosis and management of patients with primary biliary cholangitis. (2017) · cites this paper as [7]
The introduction (p. 2) calls serum bilirubin a well-established independent predictor of prognosis in PBC, and the Discussion (p. 9) links higher levels to reduced transplant-free survival. Neither passage establishes that it has been recognised as such since the 1970s. (LLM, conf=0.86)
Experimental — accuracy not yet measuredParis 2 criteria have been recognized as relevant predictors of clinical outcomes in several independent populations of patients with primary biliary cholangitis.
“Patients were selected on the basis of Paris 2 criteria, 15 which have been recognized as relevant predictors of clinical outcomes in several independent populations of patients with primary biliary cholangitis.24,25”
From A Placebo-Controlled Trial of Bezafibrate in Primary Biliary Cholangitis (2018) · cites this paper as [25]
The Results (p. 4) show that alkaline phosphatase and bilirubin thresholds predicted transplant-free survival in a pooled international PBC cohort. However, the paper does not establish that the Paris 2 criteria as a set predicted clinical outcomes in several independent populations; its reported analyses concern individual biochemical thresholds. (LLM, conf=0.83)
Experimental — accuracy not yet measuredIn a large international cohort of patients with primary biliary cholangitis, elevations in alkaline phosphatase were independently associated with a risk of liver transplantation or death 2.0 to 2.5 times as high as the risk associated with normal levels.
“In a large, international cohort analysis involving patients with primary biliary cholangitis, elevations in the alkaline phosphatase level were independently associated with a risk of liver transplantation or death that was 2.0 to 2.5 times as high as the risk associated with normal levels. 10”
From A Placebo-Controlled Trial of Obeticholic Acid in Primary Biliary Cholangitis (2016) · cites this paper as [10]
The Statistical Analysis section (p. 3) says the analyses adjusted for age, sex, year of diagnosis, and UDCA therapy. The Results (p. 4) find higher alkaline phosphatase associated with greater risk of transplantation or death, but compare patients above 2.0 times the upper limit of normal with those at or below that threshold—not specifically with patients whose alkaline phosphatase was normal. The cited passages do not establish the claimed 2.0-to-2.5-fold risk relative to normal levels. (LLM, conf=0.86)
Experimental — accuracy not yet measuredAn abnormally elevated bilirubin level was a stronger predictor of outcomes, with a risk of liver transplantation or death 5.1 to 10.7 times the risk associated with normal levels; even increased values within the normal range were associated with a risk of disease progression.
“An abnormally elevated bilirubin level, which occurs later in disease progression, was a stronger predictor of outcomes, with a risk of liver transplantation or death that was 5.1 to 10.7 times the risk associated with normal levels; however, even increased values within the normal range were associated with a risk of disease progression. 10”
From A Placebo-Controlled Trial of Obeticholic Acid in Primary Biliary Cholangitis (2016) · cites this paper as [10]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
PBC is chronic and often progressive, leading to end-stage liver disease and related complications.
“The disease is chronic and often progressive, resulting in end-stage liver disease and its associated complications [6][7][8].”
From EASL Clinical Practice Guidelines: The diagnosis and management of patients with primary biliary cholangitis. (2017) · cites this paper as [7]
Response to UDCA is variable, and incomplete response is associated with increased risk of death from PBC or need for liver transplantation.
“Response to UDCA is variable, and incomplete response is associated with increased risk of death from PBC or need for liver transplantation.11–18”
From The British Society of Gastroenterology/UK-PBC primary biliary cholangitis treatment and management guidelines (2018) · cites this paper as [11]
Serum bilirubin has been recognized since the 1970s as a major predictor of poor PBC outcome.
“Serum bilirubin has been recognised since the 1970s as a major predictor of poor outcome in PBC [72,7].”
From EASL Clinical Practice Guidelines: The diagnosis and management of patients with primary biliary cholangitis. (2017) · cites this paper as [7]
PBC is chronic and often progressive, leading to end-stage liver disease and its complications.
“The disease is chronic and often progressive, resulting in end-stage liver disease and its associated complications [6][7][8].”
From EASL Clinical Practice Guidelines: The diagnosis and management of patients with primary biliary cholangitis. (2017) · cites this paper as [7]
Experimental — accuracy not yet measuredIn a large international meta-analysis including 4,845 patients, UDCA-treated individuals had significantly improved transplant-free survival at 5, 10, and 15 years compared with nontreated individuals (90%, 78%, and 66% versus 79%, 59%, and 32%, respectively).
“In a large, international meta-analysis including 4,845 patients, UDCAtreated individuals had significantly improved transplant-free survival at 5, 10, and 15 years compared with nontreated individuals (90%, 78%, and 66% versus 79%, 59%, and 32%, respectively).(77)”
From Primary Biliary Cholangitis: 2018 Practice Guidance from the American Association for the Study of Liver Diseases (2019) · cites this paper as [77]
Serum ALP and total bilirubin predict outcomes in PBC patients treated with UDCA.
“Specifically, serum ALP and total bilirubin predict outcomes in this context.(77)”
From Primary Biliary Cholangitis: 2018 Practice Guidance from the American Association for the Study of Liver Diseases (2019) · cites this paper as [77]
Higher levels of alkaline phosphatase and bilirubin correlate with disease progression, and lower levels are predictive of survival without the need for liver transplantation.
“Higher levels of alkaline phosphatase and bilirubin levels correlate with disease progression, and lower levels are predictive of survival without the need for liver transplantation. 9,10”
From A Placebo-Controlled Trial of Obeticholic Acid in Primary Biliary Cholangitis (2016) · cites this paper as [10]
The majority of patients diagnosed today are asymptomatic at diagnosis and nearly 90% do not have fibrosis when first identified.
“The majority of patients diagnosed today are asymptomatic at diagnosis and one contemporary series showed that nearly 90% do not have fibrosis when first identified (although others have shown higher rates potentially reflecting case mix).11 12 26 27”
From The British Society of Gastroenterology/UK-PBC primary biliary cholangitis treatment and management guidelines (2018) · cites this paper as [11]
The Baseline Data (pp. 3–4) report diagnosis years and histological stages, but not whether most patients were asymptomatic at diagnosis or whether nearly 90% lacked fibrosis when first identified. A search for asymptomatic presentation and fibrosis at diagnosis found no passage establishing either figure in this paper. (LLM, conf=0.73)
Experimental — accuracy not yet measuredALP and bilirubin are two main prognostic factors for long-term survival in PBC.
“two of the main prognostic factors that predict long-term survival in PBC.20”
From Combination of fibrates with obeticholic acid is able to normalise biochemical liver tests in patients with difficult‐to‐treat primary biliary cholangitis (2021) · cites this paper as [20]
Higher alkaline phosphatase levels correlate with disease progression and are associated with higher risk of liver transplantation or death in patients with primary biliary cholangitis.
“Higher levels of ALP correlate with disease progression, and are associated with higher risk of liver transplantation or death.4”
From NGM282 for Treatment of Patients With Primary Biliary Cholangitis: A Multicenter, Randomized, Double‐Blind, Placebo‐Controlled Trial (2018) · cites this paper as [4]
Reduction in alkaline phosphatase levels has been validated as a surrogate marker of slower disease progression and improved transplant-free overall survival in patients with primary biliary cholangitis.
“Reduction in ALP levels has been validated as a surrogate marker of slower disease progression as well as improved transplant‐free overall survival.4”
From NGM282 for Treatment of Patients With Primary Biliary Cholangitis: A Multicenter, Randomized, Double‐Blind, Placebo‐Controlled Trial (2018) · cites this paper as [4]
Recent data have revealed the importance of ALP as a surrogate of clinical outcomes in patients with PBC.
“Recent data have revealed the importance of ALP as a surrogate of clinical outcomes in patients with PBC.4”
From NGM282 for Treatment of Patients With Primary Biliary Cholangitis: A Multicenter, Randomized, Double‐Blind, Placebo‐Controlled Trial (2018) · cites this paper as [4]
Elevated levels of ALP are prognostic of worse clinical outcomes in PBC, with lower levels of ALP associated with longer transplant-free survival and improved overall survival.
“Elevated levels of ALP are prognostic of worse clinical outcomes in PBC, with lower levels of ALP associated with longer transplant‐free survival and improved overall survival.”
From NGM282 for Treatment of Patients With Primary Biliary Cholangitis: A Multicenter, Randomized, Double‐Blind, Placebo‐Controlled Trial (2018) · cites this paper as [4]
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- Authors
- Lammers, W. J., van Buuren, H. R., Hirschfield, G. M., Janssen, H. L. A., Invernizzi, P., Mason, A. L., Ponsioen, C. Y., Floreani, A., Corpechot, C., Mayo, M. J., Battezzati, P. M., Parés, A., Nevens, F., Burroughs, A. K., Kowdley, K. V., Trivedi, P. J., Kumagi, T., Cheung, A., Lleo, A., Imam, M. H., Boonstra, K., Cazzagon, N., Franceschet, I., Poupon, R., Caballeria, L., Pieri, G., Kanwar, P. S., Lindor, K. D., & Hansen, B. E.
- Affiliations
- Erasmus MC (NL)
- University of Birmingham (GB)
- University Health Network (CA)
- Fondazione Humanitas per la Ricerca (IT)
- University of Alberta (CA)
- Amsterdam UMC Location University of Amsterdam (NL)
- University of Padua (IT)
- Assistance Publique – Hôpitaux de Paris (FR)
- The University of Texas Southwestern Medical Center (US)
- University of Milan (IT)
- Hospital Clínic de Barcelona (ES)
- Universitair Ziekenhuis Leuven (BE)
- The Royal Free Hospital (GB)
- Virginia Mason Medical Center (US)
- Mayo Clinic (US)
- Corresponding author
- Hansen, Bettina E.
- ORCID
- Lammers, Willem J.
- Hirschfield, Gideon M.
- Janssen, Harry L.A.
- Invernizzi, Pietro
- Mason, Andrew L.
- Ponsioen, Cyriel Y.
- Floreani, Annarosa
- Corpechot, Christophe
- Mayo, Marlyn J.
- Battezzati, Pier M.
- Parés, Albert
- Nevens, Frederik
- Burroughs, Andrew K.
- Kowdley, Kris V.
- Trivedi, Palak J.
- Kumagi, Teru
- Cheung, Angela
- Imam, Mohamad H.
- Boonstra, Kirsten
- Cazzagon, Nora
- Poupon, Raoul
- Pieri, Giulia
- Lindor, Keith D.
- Hansen, Bettina E.
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2014-12
- Volume
- 147
- Issue
- 6
- Pages
- 1338-1349.e5
- ISSN
- 0016-5085 (ISSN-L)
- OpenAlex
- W1987523828
- Semantic Scholar
- 0d4f9630f12910194b9fbfed618c9a235f64faaf
- Cited by
- 498
- References
- 39
- Citations by year
- 2026: 47 · 2025: 41 · 2024: 40 · 2023: 43 · 2022: 47 · 2021: 53 · 2020: 40 · 2019: 46 · 2018: 49 · 2017: 30 · 2016: 28 · 2015: 30 · 2014: 3
- FWCI
- 3.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- Padua Research Archive (University of Padova) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
- Funders
- Stichting voor Lever- en Maag-Darm Onderzoek
- Intercept Pharmaceuticals
- Topics
- Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
- Health Sciences › Medicine › Surgery › Pediatric Hepatobiliary Diseases and Treatments
- Health Sciences › Medicine › Hepatology › Liver Disease and Transplantation
- Keywords
- primary biliary cirrhosis, alkaline phosphatase, bilirubin, surrogate endpoints, transplant-free survival, liver transplantation, disease progression, prognostic factors, individual patient data meta-analysis, survival prediction, cholestatic liver disease, mortality risk stratification, treatment response monitoring, liver fibrosis markers
- MeSH terms
- Adult, Aged, Alkaline Phosphatase, Bilirubin, Cholagogues and Choleretics, Education, Medical, Continuing, Female, Follow-Up Studies, Humans, Liver Cirrhosis, Biliary, Male, Middle Aged, Predictive Value of Tests, Prognosis, Risk Factors, Ursodeoxycholic Acid, Biomarkers, Survival Analysis, Liver Transplantation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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