Abstract
Background:
Following the adoption of new nomenclature for steatotic liver disease, we aimed to build consensus on the use of International Classification of Diseases codes and recommendations for future research and advocacy.
Methods:
Through a two-stage Delphi process, a core group (n = 20) reviewed draft statements and recommendations (n = 6), indicating levels of agreement. Following revisions, this process was repeated with a large expert panel (n = 243) from 73 countries.
Results:
Consensus ranged from 88.8% to 96.9% (mean = 92.3%).
Conclusions:
This global consensus statement provides guidance on harmonizing the International Classification of Diseases coding for steatotic liver disease and future directions to advance the field.
INTRODUCTION
Nomenclature changes in the field of steatotic liver disease (SLD) were recently proposed and are currently being adopted by a wide range of stakeholders.1 Among the suggested modifications, the change from NAFLD to metabolic dysfunction–associated steatotic liver disease (MASLD) reflects a drop of the “nonalcoholic” label, enabling the inclusion of positive diagnostic criteria while removing potentially stigmatizing classification. The intake of alcohol as a disease contributor is also acknowledged in the new nomenclature, with the introduction of the term “MASLD and alcohol-associated liver disease (ALD)”, abbreviated as MASLD and ALD (MetALD).1 Moreover, the nomenclature process introduced new defining criteria for MASLD and MetALD. Whereas studies have demonstrated almost complete overlap between populations defined by NAFLD and MASLD criteria, the cutoffs for alcohol use in the MetALD definition remain to be clarified by future studies.2–4
As a consequence of these nomenclature changes and to aid in their implementation, administrative coding will need to be adjusted. Globally, the International Classification of Diseases (ICD) coding system is the most used. We thus aimed to build consensus on the appropriateness of using current ICD NAFLD and NASH codes to code MASLD and metabolic dysfunction–associated steatohepatitis (MASH), respectively. We also sought to develop recommendations to guide research and advocacy on amending future ICD codes for SLD. While ICD systems vary at the local level (eg, which version is in use), ICD-10 is currently the dominant system. Nonetheless, following its release in 2022, ICD-11 use will be gradually introduced over the coming years.
METHODS
We performed a two-stage Delphi process whereby, first, a core group of people (n = 20) indicated their agreement or disagreement with statements and recommendations (n = 6) (Supplemental Table 1, http://links.lww.com/HC9/A809) using “yes” to agree and “no” to disagree, through Microsoft Forms, from July 23 to August 6, 2023. Respondents were also invited to provide qualitative feedback on each item and overall, which was considered during item revisions. This group included individuals who had previously contributed to a consensus statement on the use of NAFLD ICD codes in research5 and key opinion leaders involved in the nomenclature change.
The second stage involved inviting a panel of individuals with SLD experience to indicate their level of agreement (“agree,” “somewhat agree,” “somewhat disagree,” or “disagree”) with the modified items (n=6) (Table 1), using the described methodology,6 through Qualtrics XM, from October 6–23, 2023. Respondents were also invited to provide qualitative feedback on each item and overall, which was considered during manuscript writing. Invitees who were not familiar with ICD codes and their use could opt out. Respondents who did not feel qualified to indicate their level of agreement with a survey item could choose the option “not qualified to respond.” For the purposes of this study, we defined reaching consensus as having > 80% agreement on each item, with overall agreement being the sum of the “agree” and “somewhat agree” categories in stage 2.
TABLE 1.
Final consensus statements and recommendations
Statements | Grade | A (%) | SA (%) | A+SA (%) | SD (%) | D (%) | NQ (%) | N | |
---|---|---|---|---|---|---|---|---|---|
1 | MASLD is currently best coded using the ICD-10 code for NAFLD (K76.0). | B | 67.4 | 21.5 | 88.8 | 5.6 | 5.6 | 4.1 | 233 |
2 | MASH is currently best coded using the ICD-10 coding for NASH (K75.8 or K75.81, depending on the setting). | A | 70.8 | 21.0 | 91.8 | 4.3 | 3.9 | 4.1 | 233 |
3 | ALD is best coded using the “alcohol-associated liver disease” spectrum of ICD-10 codes (K70). | A | 84.6 | 12.3 | 96.9 | 2.2 | 0.9 | 6.6 | 227 |
4 | As no appropriate MetALD ICD-10 code exists, clinical research and health care professionals should use ICD coding for the more relevant part of MASLD/ALD on an individual basis while awaiting ICD-10/11 definition changes by the World Health Organization. | B | 62.3 | 26.8 | 89.2 | 6.9 | 3.9 | 4.9 | 231 |
Recommendations | |||||||||
5 | Research should focus on identifying how to best distinguish between MASLD, MetALD, and ALD when using historical data sources (eg, register-based data). | A | 68.5 | 22.7 | 91.2 | 5.9 | 2.9 | 2.1 | 238 |
6 | International societies should advocate for a global update of ICD terminology by the World Health Organization to better reflect the nomenclature change, including separate diagnostic codes for MASLD, MASH, MetALD, ALD, and cryptogenic steatotic liver disease. | A | 86.4 | 9.5 | 95.9 | 2.9 | 1.2 | 0.4 | 242 |
Mean % agreement | 73.3 | 19.0 | 92.3 | — | — | — | — | — |
Notes: Percentages may add up to more than 100 due to rounding. Grades are based on the percentage of combined agreement (agree+somewhat agree): A, 90%–99% combined agreement; B, 78%–89% combined agreement. Responses to each statement and recommendation are presented as percentages of the total responses.
Abbreviations: A, agree; ALD, alcohol-associated liver disease; D, disagree; ICD, International Classification of Diseases; MASH, metabolic dysfunction-associated steatohepatitis; MASLD, metabolic dysfunction-associated steatotic liver disease; MetALD, MASLD and ALD; N, total number of responses; NQ, percentage of participants that indicated that they were not qualified to respond; SA, somewhat agree; SD, somewhat disagree.
Ethical considerations
This study received ethical review exemption from the Hospital Clínic of Barcelona, Spain, ethics committee on October 4, 2023. All research was conducted in accordance with the Declarations of Helsinki and Istanbul. Respondents consented to participating, and data were anonymized for all analyses.
RESULTS
A total of 479 individuals were invited to participate in stage 2, of whom 269 (56.2%) responded. Of these, 26 (9.7%) opted out as they were not familiar with ICD codes and their use. The 243 respondents (90.3%) who completed the survey worked in 73 countries and had a mean age of 53.9 (SD: 9.4). Most respondents were male (65.4%), worked in high-income countries (66.3%) and in the Europe and Central Asia World Bank region (41.2%), and primarily worked in academia (67.9%) and as clinicians/medical doctors (72.8%) (Supplemental Table 2, http://links.lww.com/HC9/A809, contains further panelist details).
In stage 2, consensus ranged from 88.8% to 96.9% (mean = 92.3%). Four items had < 80% “agree” responses and relied more heavily on the “somewhat agree” category to reach a consensus. A total of 351 qualitative comments were provided across items. There was ≥ 88.8% consensus that MASLD, MASH, and ALD are currently best coded with K76.0, K75.8, or K75.81, and the K70 spectrum of ICD-10 codes, respectively. As for MetALD, which has no ICD code as it was newly introduced, 89.2% agreed that using ICD coding for the perceived dominant disease driver (MASLD or ALD) on an individual basis was preferable while awaiting updates to the ICD system. In terms of recommendations, 91.2% of participants agreed that research should prioritize how best to distinguish between MASLD, MetALD, and ALD when using historical data. Furthermore, the consensus that international societies should advocate for a global update of ICD terminology to better reflect the SLD nomenclature changes was 86.4%.
DISCUSSION
This study found that, among a large panel of experts working across 73 counties, there was a high degree of consensus that NAFLD and NASH ICD codes can be updated to reflect the new MASLD and MASH names and definitions, respectively, without the need for new codes. Renaming the administrative terms across various systems and countries to reflect the nomenclature change should be a priority. This is important, as introducing coding changes may lead to considerable difficulties in comparing study results and interpreting disease epidemiology patterns across settings and over time. It should be noted that definition and ICD code modifications will not mitigate the challenge of correctly calculating the amount of alcohol consumed by patients, but we hope that the recommendation of focusing research on identifying how to best distinguish between MASLD, MetALD, and ALD will promote investigations around this topic. Further work to introduce novel ICD codes to specifically define MetALD is needed, which may be achieved through discussions with national and regional norm-setting bodies and the World Health Organization, which maintains and updates the ICD system.
CONCLUSIONS
This global expert consensus statement recommends that the currently available ICD codes for NAFLD and NASH can be used to define MASLD and MASH, respectively, although advocacy is needed to update ICD terminology to better reflect the nomenclature change and introduce new codes for MetALD specifically.
Supplementary Material
ACKNOWLEDGMENTS
Assistance with the study: The authors thank all the additional panel members: Abdelmounem E. Abdo, Fredrik Åberg, Leon A. Adams, Reda M. Albadawy, Zinaida Alexa, Maryam S. Alkhatry, Naim Alkhouri, Alina M. Allen, Michael Allison, Khalid M. AlNaamani, Faisal A. Alnaser, Saleh A. Alqahtani, Khalid A. Alswat, Mario R. Alvares-da-Silva, Domenico Alvaro, Quentin M. Anstee, Juan Pablo Arab, Matthew J. Armstrong, Marco Arrese, Diego Arufe, Oidov Baatarkhuu, Gyorgy Baffy, Shokhista R. Bakieva, Louise A. Baur, Cynthia Behling, Renata Belfort-DeAguiar, Carlos E. Benítez, Thomas Berg, Annalisa Berzigotti, Ulrich Beuers, Cristiana Bianco, Emanuele Bosi, Paul N. Brennan, Elisabetta Bugianesi, Patrizia Burra, Christopher D. Byrne, Maria C. Cabrera, Rotonya M. Carr, Patrizia Carrieri, Marlen I. Castellanos Fernandez, Laurent Castera, Maria G. Castillo-Lopez, Graciela E. Castro-Narro, Eira Cerda-Reyes, Wah Kheong Chan, Yoosoo Chang, Phunchai Charatcharoenwitthaya, Norberto Chavez-Tapia, Raymond T. Chung, Andreea Ciudin, Kirsten J. Coppell, Helena Cortez-Pinto, Helma P. Cotrim, Javier Crespo, Anuradha S. Dassanayake, Nicholas O. Davidson, Robert J. de Knegt, Victor de Ledinghen, Münevver Demir, Moises Diago, Javier O. Díaz, Gabriel S. Diaz, John F. Dillon, Bruce D. Dimmig, Melisa Dirchwolf, Ajay Duseja, Karel Dvorak, Mattias Ekstedt, Mohamed El-Kassas, Osama M. Elsanousi, Ahmed M. Elsharkawy, Gamal E. Esmat, Jian-Gao Fan, Maria Lucia Ferraz, Davide Fortin, Yasser M. Fouad, Sven M. Francque, Scott L. Friedman, Michael Fuchs, Amalia Gastaldelli, Anja Geerts, Andreas Geier, Hasmik L. Ghazinyan, George B. B. Goh, Nicolas Goossens, Martin M. Grajower, Henning Grønbæk, Hannes Hagström, Nelia Hernandez, Samantha L. Hocking, Terry T.-K. Huang, Ramazan Idilman, Scott D. Isaacs, Vasily Isakov, Mona H. Ismail, Helen Jarvis, Peter Jepsen, François R. Jornayvaz, Sudhamshu K.C., Satoru Kakizaki, Fasiha Kanwal, Jia-Horng Kao, Saul J. Karpen, Takumi Kawaguchi, Seung Up Kim, David E. Kleiner, Ger H. Koek, Rohit Kohli, Loreta A. Kondili, Marko Korenjak, Aleksander Krag, Carina P. Kugelmas, Marcelo Kugelmas, Carlo La Vecchia, Brian P. Lam, Naomi F. Lange, Mariana Lazo, Nathalie C. Leite, Chun-Jen Liu, Undram Lkhagvaa, Patricio Lopez-Jaramillo, Adelina Lozano, Panu K. Luukkonen, Maria Paula Macedo, Mamun A. Mahtab, Giulio Marchesini, Sebastián Marciano, Sophia E. Martinez-Vazquez, Lyudmila Mateva Vladimirova, Charles N. Mbendi, Jeff J. McIntyre, Hailemichael D. Mekonnen, Juan M. Mendive, Luca Miele, Tamara Milovanovic, Tahiri Mohammed, Rosalba Moreno-Alcántar, Timothy R. Morgan, Ayesha A. Motala, Cynthia A. Moylan, Carla Musso, Edna J. Nava-González, Francesco Negro, Alexander V. Nersesov, Brent A. Neuschwander-Tetri, Philip N. Newsome, Dafina Nikolova, Mazen Noureddin, Katja Novak, Jude A. Oben, Claudia P. Oliveira, Janus P. Ong, Arlinking K. Ong-Go, Charles Asabamaka Onyekwere, P. Martin Padilla-Machaca, Raluca Pais, Calvin Q. Pan, Manas K. Panigrahi, George Papatheodoridis, Juan Paredes Méndez, Brian L. Pearlman, Juanita Pérez-Escobar, Juan M. Pericàs, Gianluca Perseghin, Mario G. Pessoa, Salvatore Petta, Massimo Pinzani, Nikolaos Pyrsopoulos, Marek Rác, Alnoor Ramji, Marcus S. Ranney, Natarajan Ravendhran, Mary E. Rinella, Stuart K. Roberts, Stefano Romeo, Manuel Romero-Gomez, Ian A. Rowe, Shakhlo S. Sadirova, Riina Salupere, Nurgul Toktogulova, Sanjaya K. Satapathy, Raymond B. Sayegh, Jörn M. Schattenberg, Giada Sebastiani, Lawrence Serfaty, Marina Serper, Lali Sharvadze, Jonathan Shaw, Kotacherry T. Shenoy, Nick Sheron, Oren Shibolet, Jay H. Shubrook, Shivaram P. Singh, Edford Sinkala, Igor Skrypnyk, Silvia Sookoian, C. Wendy Spearman, Kannan Sridharan, Norbert Stefan, Jonathan G. Stine, Nikos Stratakis, Juan J. Suárez, Dhastagir Sultan Sheriff, Shikha S. Sundaram, Gianluca Svegliati-Baroni, Mark G. Swain, Frank Tacke, Shahrad Taheri, Soek-Siam Tan, Tawesak Tanwandee, Elliot B. Tapper, Giovanni Targher, Eugen Tcaciuc, Norah A. Terrault, Maja Thiele, Dina Tiniakos, Aldo Torre, Esther A. Torres, Sombat Treeprasertsuk, Emmanuel A. Tsochatzis, Svetlana Turcan, Adela Turcanu, Jonas Valantinas, Luca V. C. Valenti, Laurens A. van Kleef, Lisa B. VanWagner, Jose A. Velarde-Ruiz Velasco, Mette Vesterhus, Eduardo Vilar-Gomez, Kymberly D. Watt, Julia J. Wattacheril, Sarah H. Wild, Fonda Wilkins, Robert J. Wong, Vincent Wai-Sun Wong, Stavra A. Xanthakos, Yusuf Yilmaz, Dan Yock Young, Ming-Lung Yu, Volkan D. Yumuk, Shira Zelber-Sagi, Kenneth I. Zheng, and Ming-Hua Zheng.
Footnotes
Abbreviations: ALD, alcohol-associated liver disease; ICD, International Classification of Diseases; MASH, metabolic dysfunction–associated steatohepatitis; MASLD, metabolic dysfunction–associated steatotic liver disease; MetALD, MASLD and ALD; SLD, steatotic liver disease.
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Contributor Information
Hannes Hagström, Email: hannes.hagstrom@ki.se.
Leon A. Adams, Email: leon.adams@uwa.edu.au.
Alina M. Allen, Email: allen.alina@mayo.edu.
Christopher D. Byrne, Email: c.d.byrne@soton.ac.uk.
Yoosoo Chang, Email: yoosoo.chang@gmail.com.
Ajay Duseja, Email: ajayduseja@yahoo.co.in.
Henning Grønbæk, Email: henngroe@rm.dk.
Mona H. Ismail, Email: mismail.md@gmail.com.
Peter Jepsen, Email: pj@clin.au.dk.
Fasiha Kanwal, Email: kanwal@bcm.edu.
Jennifer Kramer, Email: jkramer@bcm.edu.
Rohit Loomba, Email: roloomba@ucsd.edu.
Henry E. Mark, Email: henryemark@gmail.com.
Philip N. Newsome, Email: p.n.newsome@bham.ac.uk.
Mary E. Rinella, Email: mrinella@bsd.uchicago.edu.
Ian A. Rowe, Email: i.a.c.rowe@leeds.ac.uk.
Seungho Ryu, Email: sh703.yoo@gmail.com.
Arun Sanyal, Email: arun.sanyal@vcuhealth.org.
Jörn M. Schattenberg, Email: schatten@uni-mainz.de.
Marina Serper, Email: Marinas2@pennmedicine.upenn.edu.
Nick Sheron, Email: nicksheronwork@outlook.com.
Tracey G. Simon, Email: tgsimon@mgh.harvard.edu.
C. Wendy Spearman, Email: Wendy.Spearman@uct.ac.za.
Elliot B. Tapper, Email: etapper@med.umich.edu.
Marcela Villota-Rivas, Email: marcela.villota@isglobal.org.
Sarah H. Wild, Email: sarah.wild@ed.ac.uk.
Vincent Wai-Sun Wong, Email: wongv@cuhk.edu.hk.
Yusuf Yilmaz, Email: dryusufyilmaz@gmail.com.
Shira Zelber-Sagi, Email: shira.zelber@gmail.com.
Fredrik Åberg, Email: Fredrik.aberg@helsinki.fi.
Jeffrey V. Lazarus, Email: jeffrey.lazarus@isglobal.org.
AUTHOR CONTRIBUTIONS
Hannes Hagström and Jeffrey V. Lazarus: Study conception and design; MVR: Statistical analysis; Hannes Hagström, Marcela Villota-Rivas, HEM, and Jeffrey V. Lazarus: Drafting of the manuscript; All: Acquisition of data; analysis and interpretation of data; and critical revision
CONFLICTS OF INTEREST
Hannes Hagström acknowledges research funding to his institutions from AstraZeneca, Echosens, Gilead, Intercept, MSD, Novo Nordisk, and Pfizer; has served as consultant or on advisory boards for AstraZeneca, Bristol Myers-Squibb, MSD, and Novo Nordisk; and has been part of hepatic event adjudication committees for Boehringer Ingelheim, KOWA, and GW Pharma, outside of the submitted work. Leon A. Adams has received speaker or advisory board fees from Novartis, Pfizer, Roche Diagnostics, and Gilead outside the submitted work. Alina M. Allen acknowledges grant support to her institution from the National Institutes of Health (NIH) (DK128127), Novo Nordisk, Pfizer, and Target Pharma and advisory board participation for Novo Nordisk and Boehringer Ingelheim, outside of the submitted work. Christopher D. Byrne acknowledges independent grant support from Echosens, France, outside of the submitted work. Ajay Duseja acknowledges an unpaid role as Secretary-General of the Indian National Association for the Study of the Liver (INASL), outside of the submitted work. Henning Grønbæk acknowledges research grants from ARLA, AbbVie, Intercept, and the Novo Nordisk Foundation, has served on the advisory board at Ipsen, and has been a speaker for Norgine, outside of the submitted work. Rohit Loomba has served as a consultant or advisory board member for Alnylam/Regeneron, Amgen, Arrowhead Pharmaceuticals, AstraZeneca, Bristol-Myers Squibb, CohBar, Eli Lilly, Galmed Pharmaceuticals, Gilead, Glympse bio, Inipharm, Intercept, Ionis, Janssen Inc., Merck, Metacrine, Inc., NGM Biopharmaceuticals, Novartis, Novo Nordisk, Pfizer, Sagimet, 89 bio, and Viking Therapeutics, acknowledges grant support to his institution from Allergan, Boehringer-Ingelheim, Bristol-Myers Squibb, Eli Lilly, Galectin Therapeutics, Galmed Pharmaceuticals, Genfit, Gilead, Intercept, Inventiva, Janssen Inc., Madrigal Pharmaceuticals, Merck, NGM Biopharmaceuticals, Pfizer, and Siemens, receives funding support from NIEHS (5P42ES010337), NCATS (5UL1TR001442), NIDDK (U01DK061734, R01DK106419, P30DK120515, R01DK121378, R01DK124318), NHLBI (P01HL147835), and DOD PRCRP (W81XWH-18-2-0026), and is a co-founder of Liponexus, Inc, outside of the submitted work. Philip N. Newsome acknowledges grants or contracts from Novo Nordisk, consulting fees from BMS, Boehringer Ingelheim, Gilead, Intercept, Novo Nordisk, Pfizer, Sun Pharma, Madrigal, GSK, and Poxel Pharmaceuticals, payment or honoraria from Novo Nordisk and AiCME, support for attending meetings and/or travel from Novo Nordisk, and advisory board participation for Novo Nordisk, Boehringer Ingelheim, Gilead, Intercept, Poxel Pharmaceuticals, BMS, Pfizer, Sun Pharma, Madrigal, and GSK, outside of the submitted work. Mary E. Rinella acknowledges consulting fees from Intercept, Madrigal, Novo Nordisk, GSK, NGM, CytoDyn, Sonic Incytes, Boehringer Ingelheim, Takeda, and HistoIndex, outside of the submitted work. Ian A. Rowe acknowledges personal fees from AbbVie and Roche, outside of the submitted work. Jörn M. Schattenberg acknowledges research funding from Gilead Sciences, Boehringer Ingelheim, and Siemens Healthcare GmbH, consulting fees from Apollo Endosurgery, Albireo Pharma Inc, Bayer, BMS, Boehringer Ingelheim, Gilead Sciences, Intercept Pharmaceuticals, Ipsen, Inventiva Pharma, Madrigal, MSD, NorthSea Therapeutics, Novartis, Novo Nordisk, Pfizer, Roche, Sanofi, and Siemens Healthcare GmbH, payment or honoraria from Boehringer Ingelheim, Echosens, med publico GmbH, Novo Nordisk, and Madrigal Pharmaceuticals, support for attending meetings and/or travel from Gilead Sciences, and stock from AGED diagnostics and Hepta bio, outside of the submitted work. Marina Serper acknowledges consulting fees from Gilead Sciences, outside of the submitted work. Tracey G. Simon has served as a consultant for Aetion, outside of the submitted work. C. Wendy Spearman acknowledges payment or honoraria from Gilead Sciences and Abbott, support for attending meetings and/or travel from Gilead Sciences, and roles as Vice-president of the Society on Liver Disease in Africa (SOLDA) and member of the International Advisory Board of The Lancet Gastroenterology and Hepatology journal, outside of the submitted work. Sarah H. Wild acknowledges attending conferences supported by Novo Nordisk, outside of the submitted work. Vincent Wai-Sun Wong acknowledges grants from Gilead Sciences to his institution, consulting fees from AbbVie, Boehringer Ingelheim, Echosens, Gilead Sciences, Intercept, Inventiva, Novo Nordisk, Pfizer, Sagimet Biosciences, and TARGET PharmaSolutions, payment and honoraria from Abbott, AbbVie, Gilead Sciences, Novo Nordisk, and Unilab, support for attending meetings and/or travel from AbbVie and Gilead Sciences, and unpaid stock as co-founder of Illuminatio Medical Technology Limited, outside of the submitted work. Yusuf Yilmaz acknowledges consultancy fees from Zydus and Cymabay, outside of the submitted work. Shira Zelber-Sagi has given presentations for and received support for attending meetings and/or travel from AbbVie, outside of the submitted work. Fredrik Åberg acknowledges speaker fees from Abbvie, Sandoz, Astellas, Siemens Healthineers, and Norgine and consultancy fees from Sandoz, Takeda, Guidepoint, Astra Zeneca, and Ipsen, outside of the submitted work. Jeffrey V. Lazarus acknowledges grants and speaker fees from AbbVie, Gilead Sciences, MSD, and Roche Diagnostics to his institution, speaker fees from Echosens, Janssen, Novo Nordisk, and ViiV, consulting fees from GSK and Novavax, and support to ISGlobal from grant CEX2018-000806-S, funded by MCIN/AEI/10.13039/501100011033, and the “Generalitat de Catalunya,” through the CERCA Program, outside of the submitted work. The remaining authors (Yoosoo Chang, Mona H. Ismail, Peter Jepsen, Fasiha Kanwal, Jennifer Kramer, Henry E. Mark, Seungho Ryu, Arun Sanyal, Nick Sheron, Elliot B. Tapper, and Marcela Villota-Rivas) have no conflicts to report.
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