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Cited by 155Liver Diseases and ImmunityPediatric Hepatobiliary Diseases and TreatmentsDrug Transport and Resistance Mechanisms

The DOI matches its Crossref record; 26 of the 26 references it cites were found in a registry or an index.

Pretreatment prediction of response to ursodeoxycholic acid in primary biliary cholangitis: development and validation of the UDCA Response Score

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Carbone, Marco, Nardi, Alessandra, Flack, Steve, Carpino, Guido, Varvaropoulou, Nikoletta, Gavrila, Caius, Spicer, Ann, Badrock, Jonathan, Bernuzzi, Francesca, Cardinale, Vincenzo, Ainsworth, Holly F, Heneghan, Michael A, Thorburn, Douglas, Bathgate, Andrew, Jones, Rebecca, Neuberger, James M, Battezzati, Pier Maria, Zuin, Massimo, Taylor-Robinson, Simon, Donato, Maria F, Kirby, John, Mitchell-Thain, Robert, Floreani, Annarosa, Sampaziotis, Fotios, Muratori, Luigi, Alvaro, Domenico, Marzioni, Marco, Miele, Luca, Marra, Fabio, Giannini, Edoardo, Gaudio, Eugenio, Ronca, Vincenzo, Bonato, Giulia, Cristoferi, Laura, Malinverno, Federica, Gerussi, Alessio, Stocken, Deborah D, Cordell, Heather J, Hirschfield, Gideon M, Alexander, Graeme J, Sandford, Richard N, Jones, David E, Invernizzi, Pietro, Mells, George F, Thomas, Caradog, Rahman, Meshbah, Yapp, Tom, Lye Ch'ng, Chin, Harrison, Melanie, Sturgess, Richard, Galaska, Roman, Healey, Chris, Whiteman, Jessica, Czaijkowski, Marek, Gray, Catherine, Gunasekera, Anton, Gyawli, Pranab, Premchand, Purushothaman, Mann, Steven, Elliott, Keith, Kapur, Kapil, Watson, Alan, Foster, Graham, Trembling, Paul, Subhani, Javaid, Harvey, Rory, McCorry, Roger, Adgey, Carolyn, Hobson, Lucie, Mulvaney-Jones, Caroline, Evans, Richard, Mathialahan, Thiriloganathan, Ramanaden, David, Gasem, Jaber, Van Duyvenvoorde, Greta, Shorrock, Christopher, Seward, Katie, Southern, Paul, Tibble, Jeremy, Penn, Ruth, Gorard, David, Maiden, Jane, Damant, Rose, Palegwala, Altaf, Jones, Susan, Alexander, Graeme, Mells, George, Sandford, Richard, Whiteman, Jessica, Dolwani, Sunil, Prince, Martin, Silvestre, Valeria, Foxton, Matthew, Dungca, Eleanor, Mitchison, Harriet, Wheatley, Natalie, Gooding, Ian, Doyle, Helen, Karmo, Mazn, Kent, Melanie, Saksena, Sushma, Braim, Delyth, Patel, Minesh, Lord, Susan, Ede, Roland, Paton, Alison, Austin, Andrew, Lancaster, Nicola, Sayer, Joanna, Gibbins, Andrew, Hogben, Karen, Hovell, Chris, Fisher, Neil, Carter, Martyn, Koss, Konrad, Musselwhite, Janine, Muscariu, Florin, Piotreowicz, Andrzej, McKay, Alexandra, Grimley, Charles, Neal, David, Ting Tan, Lai, Lim, Guan, Brighton, Jacqueline, Foale, Carole, Ala, Aftab, Saeed, Athar, Flahive, Kerry, Wood, Gordon, Townshend, Paula, Ford, Chris, Brown, Jonathan, Kordula, Jean, Bowles, Jane, Wilkinson, Mark, Palmer, Caroline, Ramage, John, Gordon, Harriet, Featherstone, James, Ridpath, Jo, Ngatchu, Theodore, Levi, Sass, Shaukat, Syed, Sadeghian, Joy, Shidrawi, Ray, Williams, Bronwen, Abouda, George, Jones, Sarah, Duggan, Claire, Hynes, Abigail, Narain, Mark, Rees, Ian, Salam, Imroz, Crossey, Mary, Taylor-Robinson, Simon, Brown, Ashley, MacNicol, Carolyn, Williams, Simon, Wilhelmsen, Elva, Banim, Paul, Raymode, Parizade, Chilton, Andrew, Das, Debasish, Lee, Hye-Jeong, Curtis, Howard, Heneghan, Michael, Gess, Markus, Durant, Emma, Drake, IM, Bishop, Rebecca, Davies, Mervyn, Jones, Rebecca, Aldersley, Mark, Ncube, Noma, McNair, Alistair, Srirajaskanthan, Raj, Sen, Sambit, Casey, Rebecca, Bird, George, Mendall, Mike, Cowley, Caroline, Barnardo, Adrian, Kitchen, Paul, Yoong, Kevin, Amore, Kelly, Sirdefield, Dawn, Orpe, Jacky, Mathew, Ray, MacFaul, George, Wrigth, Aruna, Shah, Amir, Evans, Chris, Keggans, Janie, Bird, Bridget, Baxter, Gwen, Saha, Subrata, Pollock, Katharine, Hughes, Maggie, Bramley, Peter, Grieve, Emma, Young, Karin, Fraser, Andrew, Mukhopadhya, Ashis, Ocker, Kate, Mills, Peter, Hines, Francis, Shallcross, Chris, Wilkins, Joy, Grellier, Leonie, Campbell, Stewart, Martin, Kirsty, Bathgate, Andrew, Innes, Caron, Shepherd, Alan, Rushbrook, Simon, Valliani, Talal, Przemioslo, Robert, Fairlamb, Helen, Macdonald, Chris, Eastick, Anne, Metcalf, Jane, Tanqueray, Elizabeth, Shmueli, Udi, Holbrook, Becky, Davis, Andrew, Browning, Julie, Naqvi, Asifabbas, Walker, Kirsten, Lee, Tom, Verheyden, Juliette, Slininger, Susan, Ryder, Stephen D, Chapman, Roger, Collier, Jane, O'Donnell, Denise, Stafford, Lizzie, Williamson, Kate, Kent, Linda, Klass, Howard, Ninkovic, Mary, March, Linda, Cramp, Matthew, Simpson, Diane, Dickson, Christine, Sharer, Nicholas, Hayes, Maria, Goggin, Patrick, Quinne, Mary, Pearson, Sallyanne, Hoeroldt, Barbara, Jones, Linda, Wright, Alice, Booth, Jonathan, Loftus, Alison, Lipscomb, George, Dewhurst, Hannah, Gunter, Emma, Williams, Earl, Fouracres, Anna, Farrington, Liz, Graves, Lyn, Hussaini, Hyder, Stableforth, Bill, Marriott, Suzie, Ayres, Reuben, Leoni, Marina, Burroughs, Andrew, Marshall, Eileen, Thorburn, Douglas, Tyrer, David, Martin, Kate, Lombard, Martin, Patanwala, Imran, Dali-Kemmery, Lola, Lambourne, Victoria, Maltby, Julia, Vyas, Samir, Colley, Julie, Shinder, Bal, Singhal, Saket, Jones, Jayne, Mills, Marisa, Gleeson, Dermot, Carnahan, Mandy, Butterworth, Jeff, Boulton, Kerenza, Taylor, Natalie, George, Keith, Harding, Tim, Tregonning, Julie, Douglass, Andrew, Brown, Carly, Clifford, Gayle, Panter, Simon, Gocher, Denise, Shearman, Jeremy, Bray, Gary, Hamilton, Maria, Butcher, Graham, Forton, Daniel, Mclindon, John, Curtis, Janette, Das, Debashis, Shewan, Tracey, Cowan, Matthew, Whatley, Gregory, Nasseri, Mariam, Grover, Bob, Sivaramakrishnan, Nurani, Ducker, Samantha, Houghton, Kathryn, Jones, David, Griffiths, Laura, Tripoli, Sherill, Pitcher, Maxton, Shpuza, Ervin, White, Nikki, Ghosh, Deb, Douds, Andrew, Green, Marie, Brookes, Matthew, Cumlat, Lourdes, Wong, Voi Shim, Warner, Karen, Netherton, Kimberley, Mandal, Adtya, Jain, Snjiv, Gupta, Hemant, Sanghi, Pradeep, Pereira, Steve, Neuberger, James, Gunson, Bridget, Hirschfield, Gideon, Lim, Reina Teegan, Gallagher, Susan, Clement, Darren, Brind, Alison, Watts, Gill, Mupudzi, Mcdonald, Wright, Mark, Gitahi, Jane, Gordon, Fiona, Gocher, Denis, Unitt, Esther, Pateman, Hilary, Batham, Sally, Delahooke, Toby, Grant, Allister, Conder, Jill, Higham, Andrew, Cox, Mark, O'Donohoe, Lynn, Currie, Lynn, King, Alistair, Oblak, Metod, Collins, Carole, Whalley, Simon, Quinn, Marie, Baird, Yolanda, Amey, Isobel, Fraser, Jocelyn, Li, Andy, Cotterill, Donna, Bell, Andrew, Watson, Alan, Singhal, Amit, Gee, Ian, Greer, Sandra, Ang, Yeng, Ransford, Rupert, Allison, Joanna, Gotto, James, Dyer, Simon, Sweeting, Helen, Millson, Charles, Invernizzi, Pietro, Carbone, Marco, Cristoferi, Laura, Bonato, Giulia, Malinverno, Federica, Bernuzzi, Francesca, Alvaro, Domenico, Labbadia, Giancarlo, Bragazzi, Maria Consiglia, Andreone, Pietro, Muratori, Luigi, Azzaroli, Francesco, Floreani, Annarosa, Galli, Andrea, Tarocchi, Mirko, Giannini, Edoardo, Miele, Luca, Gasbarrini, Antonio, Grieco, Antonio, Marrone, Giuseppe, Donato, Maria Francesca, Valenti, Luca, Marra, Fabio, Marzioni, Marco, Maroni, Luca, Rigamonti, Cristina, Zuin, Massimo, Battezzati, Pier Maria, Picciotto, Antonino·2018·The Lancet Gastroenterology & Hepatology
DOI 10.1016/s2468-1253(18)30163-8PMC PMC6962055
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Abstract

Background Current guidelines advocate a step-wise approach to disease-modifying treatment of primary biliary cholangitis (PBC): all patients begin treatment with ursodeoxycholic acid (UDCA) monotherapy – and those with inadequate biochemical response to UDCA are subsequently considered for second-line therapies, the conventional period to demonstrate inadequate UDCA response being 12 months. A potential limitation with this approach, however, is that patients at highest risk end up waiting longest for effective treatment. In this study, we sought to determine whether UDCA response can be accurately predicted using pre-treatment clinical parameters, so that alternative approaches to treatment stratification might be explored. Methods We undertook logistic regression analysis of pre-treatment variables in 2,703 UDCA-treated patients to derive the best-fitting model of UDCA response, defined as ALPT12 < 1.67×ULN. We validated the model in an external PBC cohort from Italy (n=460). Finally, we explored the biological plausibility of the model by looking for correlation between model predictions and key histological features on PBC liver biopsies (n = 20), such as biliary injury and fibrosis. Findings The following pre-treatment parameters were associated with lower probability of UDCA response: higher ALP (p<0.0001), higher bilirubin (p=0.0003), lower transaminases (TA, p=0.0012), younger age (p<0.0001), longer interval from diagnosis to the start of UDCA (treatment time lag, p<0.0001), and worsening of ALP from diagnosis (ΔALP, p<0.0001). Based on these variables, we derived a predictive score of UDCA response: UDCAresponsescore(URS)=0.77+0.60×(TBdiag)−1−2.73×ln(ALPdiag)+0.35×ln(TAdiag)+0.03×age−0.15×(treatmenttimelag)−0.56×ΔALP In external validation, the AUROC was 0.83 (0.79-0.87). In PBC liver biopsies, the URS was associated with ductular reaction (DR) and intermediate hepatocytes (IH). Interpretation We have derived and externally validated a model based on pre-treatment variables that accurately predicts UDCA response. Association with DR and IH provides face validity. Thus, this model provides a basis to explore alternative approaches to treatment stratification in PBC. Fundings Medical Research Council (MR/L001489/1); University of Milan-Bicocca. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors
Carbone, M., Nardi, A., Flack, S., Carpino, G., Varvaropoulou, N., Gavrila, C., Spicer, A., Badrock, J., Bernuzzi, F., Cardinale, V., Ainsworth, H. F., Heneghan, M. A., Thorburn, D., Bathgate, A., Jones, R., Neuberger, J. M., Battezzati, P. M., Zuin, M., Taylor-Robinson, S., Donato, M. F., Kirby, J., Mitchell-Thain, R., Floreani, A., Sampaziotis, F., Muratori, L., Alvaro, D., Marzioni, M., Miele, L., Marra, F., Giannini, E., Gaudio, E., Ronca, V., Bonato, G., Cristoferi, L., Malinverno, F., Gerussi, A., Stocken, D. D., Cordell, H. J., Hirschfield, G. M., Alexander, G. J., Sandford, R. N., Jones, D. E., Invernizzi, P., Mells, G. F., Thomas, C., Rahman, M., Yapp, T., Lye Ch'ng, C., Harrison, M., Sturgess, R., Galaska, R., Healey, C., Whiteman, J., Czaijkowski, M., Gray, C., Gunasekera, A., Gyawli, P., Premchand, P., Mann, S., Elliott, K., Kapur, K., Watson, A., Foster, G., Trembling, P., Subhani, J., Harvey, R., McCorry, R., Adgey, C., Hobson, L., Mulvaney-Jones, C., Evans, R., Mathialahan, T., Ramanaden, D., Gasem, J., Van Duyvenvoorde, G., Shorrock, C., Seward, K., Southern, P., Tibble, J., Penn, R., Gorard, D., Maiden, J., Damant, R., Palegwala, A., Jones, S., Alexander, G., Mells, G., Sandford, R., Whiteman, J., Dolwani, S., Prince, M., Silvestre, V., Foxton, M., Dungca, E., Mitchison, H., Wheatley, N., Gooding, I., Doyle, H., Karmo, M., Kent, M., Saksena, S., Braim, D., Patel, M., Lord, S., Ede, R., Paton, A., Austin, A., Lancaster, N., Sayer, J., Gibbins, A., Hogben, K., Hovell, C., Fisher, N., Carter, M., Koss, K., Musselwhite, J., Muscariu, F., Piotreowicz, A., McKay, A., Grimley, C., Neal, D., Ting Tan, L., Lim, G., Brighton, J., Foale, C., Ala, A., Saeed, A., Flahive, K., Wood, G., Townshend, P., Ford, C., Brown, J., Kordula, J., Bowles, J., Wilkinson, M., Palmer, C., Ramage, J., Gordon, H., Featherstone, J., Ridpath, J., Ngatchu, T., Levi, S., Shaukat, S., Sadeghian, J., Shidrawi, R., Williams, B., Abouda, G., Jones, S., Duggan, C., Hynes, A., Narain, M., Rees, I., Salam, I., Crossey, M., Taylor-Robinson, S., Brown, A., MacNicol, C., Williams, S., Wilhelmsen, E., Banim, P., Raymode, P., Chilton, A., Das, D., Lee, H.-J., Curtis, H., Heneghan, M., Gess, M., Durant, E., Drake, I., Bishop, R., Davies, M., Jones, R., Aldersley, M., Ncube, N., McNair, A., Srirajaskanthan, R., Sen, S., Casey, R., Bird, G., Mendall, M., Cowley, C., Barnardo, A., Kitchen, P., Yoong, K., Amore, K., Sirdefield, D., Orpe, J., Mathew, R., MacFaul, G., Wrigth, A., Shah, A., Evans, C., Keggans, J., Bird, B., Baxter, G., Saha, S., Pollock, K., Hughes, M., Bramley, P., Grieve, E., Young, K., Fraser, A., Mukhopadhya, A., Ocker, K., Mills, P., Hines, F., Shallcross, C., Wilkins, J., Grellier, L., Campbell, S., Martin, K., Bathgate, A., Innes, C., Shepherd, A., Rushbrook, S., Valliani, T., Przemioslo, R., Fairlamb, H., Macdonald, C., Eastick, A., Metcalf, J., Tanqueray, E., Shmueli, U., Holbrook, B., Davis, A., Browning, J., Naqvi, A., Walker, K., Lee, T., Verheyden, J., Slininger, S., Ryder, S. D., Chapman, R., Collier, J., O'Donnell, D., Stafford, L., Williamson, K., Kent, L., Klass, H., Ninkovic, M., March, L., Cramp, M., Simpson, D., Dickson, C., Sharer, N., Hayes, M., Goggin, P., Quinne, M., Pearson, S., Hoeroldt, B., Jones, L., Wright, A., Booth, J., Loftus, A., Lipscomb, G., Dewhurst, H., Gunter, E., Williams, E., Fouracres, A., Farrington, L., Graves, L., Hussaini, H., Stableforth, B., Marriott, S., Ayres, R., Leoni, M., Burroughs, A., Marshall, E., Thorburn, D., Tyrer, D., Martin, K., Lombard, M., Patanwala, I., Dali-Kemmery, L., Lambourne, V., Maltby, J., Vyas, S., Colley, J., Shinder, B., Singhal, S., Jones, J., Mills, M., Gleeson, D., Carnahan, M., Butterworth, J., Boulton, K., Taylor, N., George, K., Harding, T., Tregonning, J., Douglass, A., Brown, C., Clifford, G., Panter, S., Gocher, D., Shearman, J., Bray, G., Hamilton, M., Butcher, G., Forton, D., Mclindon, J., Curtis, J., Das, D., Shewan, T., Cowan, M., Whatley, G., Nasseri, M., Grover, B., Sivaramakrishnan, N., Ducker, S., Houghton, K., Jones, D., Griffiths, L., Tripoli, S., Pitcher, M., Shpuza, E., White, N., Ghosh, D., Douds, A., Green, M., Brookes, M., Cumlat, L., Wong, V. S., Warner, K., Netherton, K., Mandal, A., Jain, S., Gupta, H., Sanghi, P., Pereira, S., Neuberger, J., Gunson, B., Hirschfield, G., Lim, R. T., Gallagher, S., Clement, D., Brind, A., Watts, G., Mupudzi, M., Wright, M., Gitahi, J., Gordon, F., Gocher, D., Unitt, E., Pateman, H., Batham, S., Delahooke, T., Grant, A., Conder, J., Higham, A., Cox, M., O'Donohoe, L., Currie, L., King, A., Oblak, M., Collins, C., Whalley, S., Quinn, M., Baird, Y., Amey, I., Fraser, J., Li, A., Cotterill, D., Bell, A., Watson, A., Singhal, A., Gee, I., Greer, S., Ang, Y., Ransford, R., Allison, J., Gotto, J., Dyer, S., Sweeting, H., Millson, C., Invernizzi, P., Carbone, M., Cristoferi, L., Bonato, G., Malinverno, F., Bernuzzi, F., Alvaro, D., Labbadia, G., Bragazzi, M. C., Andreone, P., Muratori, L., Azzaroli, F., Floreani, A., Galli, A., Tarocchi, M., Giannini, E., Miele, L., Gasbarrini, A., Grieco, A., Marrone, G., Donato, M. F., Valenti, L., Marra, F., Marzioni, M., Maroni, L., Rigamonti, C., Zuin, M., Battezzati, P. M., & Picciotto, A.
Affiliations
  • University of Rome Tor Vergata (IT)
  • University of Cambridge (GB)
  • Foro Italico University of Rome (IT)
  • Sapienza University of Rome (IT)
  • Newcastle University (GB)
  • PBC Foundation (GB)
  • Wellcome/MRC Cambridge Stem Cell Institute (GB)
  • Ospedale San Paolo (IT)
  • University of Milano-Bicocca (IT)
  • Edinburgh Royal Infirmary (GB)
  • Queen Elizabeth Hospital Birmingham (GB)
  • Imperial College London (GB)
  • St James's University Hospital (GB)
  • University of Milan (IT)
  • University of Padua (IT)
  • Agostino Gemelli University Polyclinic (IT)
ORCID
Venue
The Lancet Gastroenterology & Hepatology
Publisher
Elsevier BV
Published
2018-09
Volume
3
Issue
9
Pages
626-634
ISSN
  • 2468-1156 (ISSN-L)
  • 2468-1253
DOI
10.1016/s2468-1253(18)30163-8
PMC
PMC6962055
OpenAlex
W2883784290
Semantic Scholar
cd10e32484b0f06ad9d9e15fe1b21304b3b08b07
Cited by
155
References
26
Citations by year
2026: 9 · 2025: 18 · 2024: 20 · 2023: 23 · 2022: 19 · 2021: 23 · 2020: 23 · 2019: 15 · 2018: 4
FWCI
10.18
Type
journal article
Language
en
Open access
Licence
Locations
  • The Lancet. Gastroenterology & hepatology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • BOA (University of Milano-Bicocca) (submittedVersion, other-oa)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion, other-oa)
  • Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
  • Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, other-oa)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
  • Florence Research (University of Florence) (submittedVersion)
  • CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
  • IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
  • Università Politecnica delle Marche (Università Politecnica delle Marche) (submittedVersion)
  • Research Explorer (The University of Manchester) (submittedVersion, other-oa)
  • Spiral (Imperial College London) (submittedVersion, cc-by-nc-nd)
  • UEA Digital Repository (University of East Anglia) (submittedVersion)
  • Apollo (University of Cambridge) (submittedVersion)
  • Padua Research Archive (University of Padova) (submittedVersion)
  • Apollo
Funders
  • Wellcome Trust (085925)
  • NIHR Imperial Biomedical Research Centre
  • Intercept Pharmaceuticals
  • Birmingham Biomedical Research Centre
  • Medical Research Council (MR/L001489/1)
  • NIHR Nottingham Biomedical Research Centre
  • National Institute for Health and Care Research
  • Isaac Newton Trust
  • Università degli Studi di Milano-Bicocca
Topics
  • Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
  • Health Sciences › Medicine › Surgery › Pediatric Hepatobiliary Diseases and Treatments
  • Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
Keywords
primary biliary cirrhosis, ursodeoxycholic acid, alkaline phosphatase, total bilirubin, transaminases, liver biopsy histology, ductular reaction, liver fibrosis, biliary injury, second-line therapy, external validation
MeSH terms
Alkaline Phosphatase, Transaminases, Bilirubin, Cholagogues and Choleretics, Decision Support Techniques, Female, Humans, Liver Cirrhosis, Biliary, Male, Middle Aged, Risk Factors, ROC Curve, Ursodeoxycholic Acid, Linear Models, Treatment Outcome, Age of Onset, Area Under Curve, Time-to-Treatment

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