comments and controversies
Author afﬁliations
and support
information (ifapplicable) appear
at the end of thisarticle.
Accepted on February
14, 2022 andpublished at
ascopubs.org/journal/
jco on March 28,
2022: DOI https://doi.
org/10.1200/JCO.21.
02373© 2022 by American
Society of ClinicalOncology

Breaking the Child-Pugh Dogma in
Hepatocellular Carcinoma
Philip James Johnson, MD1; David J. Pinato, MD, PhD2,3; Anton Kalyuzhnyy, BSc4; and Hidenori Toyoda, MD5

The Child or Child-Turcotte score (1964) was proposed to assess prognosis in patients with cirrhosis
and portal hypertension as a predictor of postoperative(portocaval shunt surgery) mortality.1 The scoring
system included ﬁve components, three subjective
categorized variables: ascites, encephalopathy, andnutritional status and two objective continuous variables: serum albumin and bilirubin levels. The ChildTurcotte score was modiﬁed by Pugh in 1973, thenutritional status component being replaced by prothrombin time.2 This modiﬁcation has, henceforth,been referred to as the Child-Pugh score (C-P score)and has subsequently been applied as a prognostic
tool for patients with chronic liver disease in othercircumstances, including patients with hepatocellular
carcinoma (HCC). The components of the C-P score
were identiﬁed empirically as the principal factors
perceived to reﬂect the severity and hence prognosis of
cirrhosis. Each of the components was scored individually (0, 1, 2 or 3 points—3 being the most severe)on the basis of empirically assigned cutoff ranges anddescriptive terms, contributing to a total score from 5 to
15 points. The total scores were then divided into threegrades of increasing severity and poorer prognosis (A,B, and C, with C having the worst prognosis).
The outcome of patients with HCC is determined by
two parameters: the tumor-related aspects (size,
metastases, and vascular invasion, etc) and the degree of liver dysfunction.3,4 In the most widely usedstaging classiﬁcation, the Barcelona Clinic Liver
Cancer stage system, which offers both a guide to themost appropriate treatment and the expected prognosis, liver dysfunction is accounted for by the C-P
score.5 In general clinical/hepatological practice, theC-P score informs many aspects of treatment allocation. The conﬁnement of patients with the lowest risk
category of C-P grade (CP-A) in clinical trials (thereby
isolating the effect of the anticancer treatment from theadverse impact of liver dysfunction), has been one of
the reasons suggested for the successful identiﬁcationof sorafenib as an effective systemic agent for advanced HCC.6,7
Recently, the ALBI (albumin-bilirubin) score has beendeveloped as an HCC-speciﬁc reﬁnement of the C-P
score.8 It is a simple, statistical model derived from alarge HCC data set that has been extensively validated. ALBI takes just two of the Child-Pugh variables, albumin and bilirubin, and to this extent
implies that the clinical features are redundant in the
prognostic impact of the C-P score. Again, it ispresented as grades 1-3, with 3 having the worst
prognosis. It is important to recognize that ALBI is
not proposed as a prognostic system in its own right,
but rather a better approach to assessing that
portion of HCC prognosis that is affected by underlying liver function. Herein, we summarize thelimitations of the C-P score as applied to patientswith HCC and propose that the ALBI score may offer
practical and practice-changing advantages.
Limitations of the C-P Score—Subjectivity andInconsistency of Versions
The limitations of the C-P scoring system include thesubjectivity of assessment of ascites and encephalopathy, the interdependence of the ﬁve parameters,
the absence of some important prognostic parameterssuch as renal function, and the lack of speciﬁcity for
different disease etiologies.9,10 A review of the literature(This statement is based on a search for Child-Pughscore on the online Google search engine, Google
Scholar, and PubMed. Values relating to the various
C-P scoring systems were collated focusing on theapplication of these systems to prognosis of liver cirrhosis in general, rather than cirrhosis that is attributable to speciﬁc disease etiologies. References citedby the sources were also manually searched. Eachsource was required to meet the following criteria: [1]source must be complete, ie, [i] fully published in theliterature [research papers, review articles, and textbooks] and [ii] complete website or database, and [2]source must provide a value for every component of
the C-P score.) reveals that there are more than 30
different versions of the C-P score. There are no formal
descriptors or values for ascites or encephalopathy
status, and this results in profound inconsistencies inassessing each component of the score, with fundamental implications for the prognostic ability of thismodel. For example, if an investigator/clinician grades
ascites as moderate, this scores 2 points according tosome sources and 3 points according to others. Even
with an ascites score of 1 (ascites absent), there can1

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Johnson et al

be controversy when, for example, ascites is clearly
detected on imaging but not on clinical examination. Thissituation is further complicated by the ﬂuctuant nature ofencephalopathy. The issue of subjectivity of encephalopathy scoring in randomized clinical trials has beenformally criticized and tackled by the amended West
Haven Score, which scores lower grades of encephalopathy more speciﬁcally.11,12 Moreover, the varying
terminology is very rarely supported by subsequent explanations. For example, certain literature deems
chronicity a valid factor when grading encephalopathy
while other sources reference the subjective comatose
state as a factor. The version of the C-P score used isseldom, if ever, reported in research publications.

variations, especially for cirrhosis at an early stage, andwhere, as is the case in most primary care situations,objective measurements such as the liver stiffness
measurement are not readily accessible.17 Indeed,current European Association for the Study of the Liverguidelines note that discrimination between severe ﬁbrosis and compensated cirrhosis is often unclear.18
ALBI was developed in an HCC population without any
regard to the presence or absence of cirrhosis. Certainly
10%-20% of patients with HCC do not havecirrhosis.19,20 Being a continuous and much moregranular score the option remains to vary the cutoff point
and add additional factors for further discrimination at
different disease stages as several groups have done.21

Limitations of the C-P Score—Lack of Sensitivity inPatients With Mild Liver Dysfunction

ALBI offers prognostic discrimination in patients with early
compensated liver disease in whom the C-P score often
does not distinguish from the heathy population (ie, CP-A5
score). Thus, in a study involving more than 3,000 patients,
the median survival for ALBI 1, 2, and 3 were 100, 65, and20 months, respectively, compared with 68 months for CPA5.22 Similarly, in a cohort of more than 1,000 patients
receiving sorafenib within clinical trials, who were classiﬁed(per protocol) as CP-A, ALBI still offered clear prognostic
discrimination.16

Over the recent years, there has been a marked improvement in the liver function among those patients
presenting with HCC. This may reﬂect recommended
lifestyle changes (alcohol and obesity control), effective
antiviral therapies, and likely improved HCC outcomes. The
lowest grade is A, and the lowest score is 5. At the latter
point, patients are, effectively, classiﬁed as having no liver
dysfunction since this is the status at which the healthy
population would be classiﬁed/graded. There is increasing
evidence that the percentage of patients with CP-A and CPA5 has risen recently.13 In Japan, the percentage of HCC
cases in the C-P score A grade has risen from 30% (19811982) to 70% (2006-2008).14 Figure 1 shows the experience of one institution over a 30-year observation period
where the percentage of CP-A5 cases has risen from ,25% to 67%.15
The initial ALBI analysis showed that most of the impact ofserum bilirubin levels on prognosis was contained within
the conventional normal/reference range, whereas within
all C-P systems adverse points are only scored whenvalues exceed twice the reference range. Hence, at leastin the situation of HCC, the C-P score does not use therange of serum bilirubin levels that have prognostic impact. Thus, for the purposes of clinical practice andclinical trials when we classify a patient as Child-Pugh CPA5, we are saying that, in effect, we do not recognize any
degree of liver dysfunction when arriving at clinicaldecisions.
Advantages of the ALBI Score
A key advantage of the ALBI score is that it is entirely
objective, obviating any need for subjective assessmentof clinical signs, that it is derived from an entirely HCC
population16 and is a continuous score that readily lends
itself for assessment of changes in liver reserve overtime. By comparison, the C-P score, strictly speaking,should only be applied to patients with cirrhosis. It is
well-recognized that the clinical diagnosis of cirrhosis isopen to substantial interobserver and intraobserver

Furthermore, since initial publication in 2015, the ALBIscore has been validated in all clinical HCC stages andtreatments. The initial large international validation study
concluded “… the ALBI grade satisﬁed the criteria for
accuracy and reproducibility…in Eastern and Western
HCC patients…consideration should be given to the ALBI
grade as a stratifying biomarker of liver reserve in routine
clinical practice.”23(p338) More recently (2020), a systematic review of the entire literature on HCC and ALBI
concluded that “ALBI showed better discriminative
ability than Child-Pugh for predicting the prognosis in
HCC patients.”24(p383) The performance of the Barcelona
Clinic Liver Cancer classiﬁcation is not decreased when
ALBI is substituted for the C-P score,25 and the additionof platelet count (P) to ALBI (PALBI) seems to further
enhance its performance but has not yet been as excessively studied as ALBI.22
We anticipate that ALBI will ﬁnd an important role withinclinical trials involving novel therapeutics.26 There is increasing evidence that not only can ALBI predict survival
after therapy16,27,28 but it may also be associated withimproved outcomes in modern systemic therapies for advanced HCC, including lenvatinib,29,30 immunotherapy,31
and selective internal radiation therapy/transarterial chemoembolization where it may aid identiﬁcation of toxicity
posttreatment.32,33 Indeed, classiﬁcation of hepatotoxicity
in patients with HCC is unsatisfactory, and criteria such as
ALT/AST elevation seem to be poor measures of safety in
HCC.34 CP-A versus B classiﬁcation is prognostic but does
not identify patients who suffer from increased toxicity tosorafenib.35,36 In the light of these perceived advantages,

2 © 2022 by American Society of Clinical Oncology

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Breaking the Child-Pugh Dogma in HCC

100
90

85.1
76.5

80

73.4
69.0

66.7

Patients (%)

70
59.4

56.4

60
52.1

50.8

50

44.5

40
30

33.6

24.7

20
CP-A

10

CP-A5

0
1990-1994(n = 376)

1995-1999(n = 434)

2000-2004(n = 436)

2005-2009(n = 447)

2010-2014(n = 392)

2015-2019(n = 255)

Time Period
FIG 1. Changes in CP-A and CP-A5 over a 30-year period. Data collected prospectively from all patients with
HCC seen at Ogaki Municipal Hospital, Japan (Data redrawn from Kumada et al15). CP-A, Child-Pugh Class
A; CP-A5, Child-Pugh Class A5; HCC, hepatocellular carcinoma.

the ALBI score is already used in routine clinical practice inJapan and endorsed by the Japanese National Liver Cancer
Study Group.37
Finally, ALBI is ﬁnding a signiﬁcant role in prognostic models
where it is important to consider liver function. Examples are
the age–male–ALBI–platelets score17 for prediction of HCC
development in patients with chronic liver disease (where it iscombined with sex and platelet count) and several other,extensively validated, prognostic models.38
Limitations of ALBI
Since ALBI is simply a statistically based reﬁnement of the C-P
score, it inevitably suffers from some of the inherent limitationsof the C-P score. The investigation for both has been on theirdiscriminatory performance rather than calibration. The variables used in the C-P score were chosen intuitively on thebasis of clinical features that were known to associate with liver
dysfunction and biochemical parameters that were plausible
and linked to liver function because they become abnormal as
the liver fails.39 To this extent, the development of ALBI offers
no mechanistic insights that throw light on its performance
unlike ICG-15 (indocyanine green retention 15 minutes afteradministration) clearance, which is the standard measurement of hepatic excretion used extensively in Japan, as part of
the Makuuchi criteria for safe hepatic resection.40 Nonetheless, the correlation between ICG-15 and ALBI is good,16,21
and ALBI is a much simpler parameter to assess and othermethods of assessing liver function have not been widelyadopted. Interestingly, experience in HIV-associated HCC
revealed the ALBI score to reﬂect the quality of the underlying

immune function, a parameter linked to faster progression ofﬁbrosis in people living with HIV and hepatitis.31
The model for end-stage liver disease score, which like the
C-P score was originally applied in the management of portal
hypertension (transjugular intrahepatic portosystemic shunt)
and again like the C-P score, has had its role extrapolated
this time to liver transplantation, and hepatic resection41 is analternative approach to liver function assessment in HCC.
However, it is by design aimed at end-stage liver disease
where it plays an important role in informing graft allocation
priority policy for liver transplantation and to the selection ofpatients for hepatic resection.18,42 Nonetheless, in the settingof cirrhosis and HCC, head-to-head comparisons suggestthat in most HCC cases ALBI offers better prognostic discrimination,22,43 although focusing on ALBI for early cirrhosis
and considering model for end-stage liver disease score in
end-stage liver disease remains an option.
The fact that the original C-P score that was based on a total of
38 patients, unrelated to HCC, with no statistical analysis, has
held the stage for nearly 50 years is surely a testament toclinical acumen. Although the C-P score will undoubtedly
continue to guide treatment decisions in patients with cirrhosis, clinical care of patients with HCC, now counting on anumber of local and systemic treatment options, demands
solid and evidence-based instruments to deliver the promiseof individualized patient management.
In an increasingly complex clinical landscape seeing patients with advanced HCC achieving previously unthinkablelandmark survival end points at 2 years from diagnosis,44

Journal of Clinical Oncology

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3

Johnson et al

the ALBI grade offers consistent prognostic discrimination
within that increasing percentage of patients with HCC withvery early liver disease, whereas the C-P score does not.
The accumulating body of evidence in support of the ALBI
grade as an optimal predictor of outcome in patients who

are diagnosed with HCC today calls for its broader use inclinical practice and drug development. This is particularly
so in a ﬁeld where high attrition rates and incomplete
disease phenotyping continue to delay the delivery of
precision medicine.

AFFILIATIONSAUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF
INTEREST1

Department of Molecular and Clinical Cancer Medicine, University ofLiverpool, Liverpool, United Kingdom
2
Department of Surgery & Cancer, Imperial College London,
Hammersmith Hospital, London, United Kingdom
3
Division of Oncology, Department of Translational Medicine, Universityof Piemonte Orientale, Novara, Italy
4
Computational Biology Facility, University of Liverpool, Liverpool,
United Kingdom
5Department of Gastroenterology and Hepatology, Ogaki Municipal
Hospital, Ogaki, Japan

Disclosures provided by the authors are available with this article at DOI
https://doi.org/10.1200/JCO.21.02373.

AUTHOR CONTRIBUTIONSProvision of study materials or patients: Hidenori Toyoda
Manuscript writing: All authors
Final approval of manuscript: All authors
Accountable for all aspects of the work: All authors

CORRESPONDING AUTHORACKNOWLEDGMENT

Philip James Johnson, MD, Department of Molecular and Clinical Cancer
Medicine, Institute of Systems, Molecular and Integrative Biology,
University of Liverpool, Sherrington Building, Ashton St, Liverpool L69
3GE, United Kingdom; e-mail: Philip.Johnson@liverpool.ac.uk.

Although we are grateful to several colleagues (Neil Guha, Hamish Innes,
Theresa Hydes, Alessandro Cucchetti, Atsushi Hiraoka, and Makoto
Chuma) who offered advice during the preparation of this manuscript, theauthors take sole responsibility for the content. We are particularly
grateful to Dr Harun Khan for the literature search concerning versions of
the C-P score. D.J.P. acknowledges infrastructural support by the NIHR
Imperial Biomedical Research Center.

SUPPORT
Supported by grant funding from the Wellcome Trust Strategic Fund
(PS3416), the AIRC MFAG Grant Number 25697 (Associazione Italiana
per la Ricerca sul Cancro Foundation, Milan, Italy) (D.J.P.).

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5

Johnson et al
AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST
Breaking the Child-Pugh Dogma in Hepatocellular Carcinoma
The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated unless otherwise noted.
Relationships are self-held unless noted. I 5 Immediate Family Member, Inst 5 My Institution. Relationships may not relate to the subject matter of this manuscript.
For more information about ASCO’s conﬂict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/jco/authors/author-center.
Open Payments is a public database containing information reported by companies about payments made to US-licensed physicians (Open Payments).
David J. Pinato
Honoraria: Roche/Genentech, Bristol Myers Squibb, Da Volterra, Avamune,
MurslaConsulting or Advisory Role: EISAI, Mina Therapeutics, Roche, H3
Biomedicine, Da Volterra, AstraZeneca, Ipsen
Speakers’ Bureau: Bayer, ViiV Healthcare, Falk Pharma, Roche
Research Funding: MSD Oncology (Inst), Bristol Myers Squibb (Inst),
GlaxoSmithKline (Inst)
Travel, Accommodations, Expenses: Bristol Myers Squibb, Bayer, MSD
Oncology
Other Relationship: Wiley

Hidenori Toyoda
Honoraria: AbbVie, Bayer Yakuhin, Gilead Sciences, MSD K.K, Janssen, Eisai,
Chugai Pharma, Otsuka, Terumo
Speakers’ Bureau: AbbVie, Gilead Sciences, MSD, Bayer, Eisai
No other potential conﬂicts of interest were reported.

© 2022 by American Society of Clinical Oncology

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