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Original Articles 401

The Charlson Comorbidity Index in


Registry-based Research
Which Version to Use?
Nele Brusselaers1,2; Jesper Lagergren3,4
1Centre for Translational Microbiome Research (CTMR), Department of Microbiology, Tumor- and Cell Biology,
Karolinska Institutet, Stockholm, Sweden;
2Science for Life Laboratory (SciLifeLab), Stockholm, Sweden;

3Upper Gastrointestinal Surgery, Department of Molecular Medicine and Surgery, Karolinska Institutet, Karolinska

University Hospital, Stockholm, Sweden;


4Division of Cancer Studies, King’s College London, UK

Keywords to ICD version 8 and version 9 was con- 1. Introduction


Charlson Comorbidity Index, comorbidity, ducted by means of the ICD-code converter

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outcome, survival, ICD, International Classifi- of Statistics Sweden. The problem of confounding effects of co-
cation of Diseases Results: In total, 16 studies were identified morbidities on survival was recognised in
reporting ICD-adaptations of the Charlson the early 1970s, and is also referred to as
Summary Comorbidity Index. The Royal College of Sur- susceptibility bias [1]. If certain comorbid-
Background: Comorbidities may have an geons in the United Kingdom combined 5 ities, e.g. diabetes mellitus or obesity, are
important impact on survival, and comorbid- versions into an adapted and updated ver- known and important confounders, their
ity scores are often implemented in studies sion which appeared appropriate for re- effect should be analysed individually. Yet,
assessing prognosis. The Charlson Comorbid- search purposes. Their ICD-10 codes were often a more general assessment of comor-
ity index is most widely used, yet several back-translated into ICD-9 and ICD-8 accord- bidity status is required, preferably as a
adaptations have been published, all using ing to their proposed adaptations, and ver- single numeric score which could easily
slightly different conversions of the Inter- ified with previous versions of the Charlson and reliably be added to the statistical
national Classification of Diseases (ICD) Comorbidity Index. model [2]. There are several comorbidity
coding. Conclusion: Many versions of the Charlson scoring systems developed and in use, of
Objective: To evaluate which coding should Comorbidity Index are used in parallel, so which the Charlson Index is among the ol-
be used to assess and quantify comorbidity clear reporting of the version, exact ICD- dest and the most widely used [3, 4]. This
for the Charlson Comorbidity Index for regis- coding and weighting is necessary to obtain scoring system is based on a selected
try-based research, in particular if older ICD transparency and reproducibility in research. number of chronic, mainly non-communi-
versions will be used. Yet, the version of the Royal College of Sur- cable diseases an individual has. These
Methods: A systematic literature search geons is up-to-date and easy-to-use, and were selected based on a cohort of only 559
was used to identify adaptations and modi- therefore an acceptable co-morbidity score medical patients admitted in 1984 to a hos-
fications of the ICD-coding of the Charlson to be used in registry-based research es- pital in New York, the United States, aim-
Comorbidity Index for general purpose in pecially for surgical patients. ing to include “comorbid conditions which
adults, published in English. Back-translation singly or in combination might alter the
risk of short-term mortality” [3]. Since the
original Charlson scoring was based on the
Correspondence to: Methods Inf Med 2017; 56: 401–406 review of medical records, International
Dr. Nele Brusselaers https://doi.org/10.3414/ME17-01-0051 Classification of Diseases (ICD) coding
Centre for Translational Microbiome Research (CTMR) received: May 17, 2017
was not reported; nor was it in the age-
Department of Microbiology, Tumor- and Cell Biology accepted: August 28, 2017
Karolinska Institutet epub ahead of print: October 12, 2017 modified version (adding additional weight
Nobel väg 5 for age) [5]. Especially for research using
171 77 Stockholm registry data, exact coding information is
Sweden
E-mail: Nele.Brusselaers@ki.se
however needed to improve transparency
and reproducibility; and the first trans-
lations of these diseases into ICD-codes
(9th edition) were published in the early
1990s [6, 7]. Since administrative registries
may have used different ICD versions over
time, exact coding is necessary for different

© Schattauer 2017 Methods Inf Med 5/2017


402 N. Brusselaers, J. Lagergren: The Charlson Index in Registry-based Research

2.2 ICD-Coding in Administrative


Records identified through Additional records identified Databases
database (PubMed) searching through other sources
(n=1270) (n=2)
The ICD-codes are the global health infor-
mation standard for mortality and morbid-
ity statistics, and are presently translated
Records after duplicates removed Records excluded on title (n=983): into 43 languages and used in all member
(n=1272) Not English (n=76), not adults (n=61),
specific groups (elderly, n=68; states of the World Health Organisation.
intensive care/trauma, n=38; The ICD-coding has existed since 1893,
maternal health, n=36, palliative,
n=1, surgical, n=15, psychiatry,
and has been regularly updated since to re-
Records screened n=188; other, n=15), clearly flect advances in healthcare and medical
(n=1272) irrelevant (n=485) science over time [10], introducing new
disease categories, and more specific dis-
Records excluded on abstract ease information. Yet, there are several ver-
Records screened (n=289)
(n= 77): sions adapted for different countries and
On other comorbidity scoring (n=41);
now new ICD coding (n=29); on updates occurring between two official
comorbidity yet not relevant (n=7) ICD versions, also showing important dif-

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ferences concerning comorbidities [11]. In
Full‐text articles excluded, with Sweden, the 7th, 8th, 9th and 10th editions
Full‐text articles assessed reasons (n=196):
for eligibility (n= 212) were introduced in 1955, 1968, 1987 and
No new ICD‐codes for Charlson score
(n=170), not for general purpose 1997, respectively. Since the Swedish Pa-
(n=5), not on Charlson scoring (n=7), tient Registry was established in 1964 and
other weighting yet no new ICD‐
codes (n=5), comparison of different
has gradually expanded, with nationwide
Studies included in ICD‐versions yet no new coding coverage since 1987, the ICD 8th, 9th and
qualitative synthesis
(n = 16)
(n=4), coding algorithms for Charlson 10th versions of the ICD-coding in particu-
(n=4), modified Charlson based on
survey so not on ICD‐coding lar have been used, depending on the year
of hospitalisation [12]. Since comorbidities
are not always recorded as part of the dis-
Figure 1 Flow chart describing the systematic literature search. ICD = International Classification of
Diseases. charge diagnosis for each hospitalisation,
exact coding for the 3 last versions is
needed to optimise the coverage of chronic
versions of the ICD coding (8–10th edition) 2. Methods comorbidities to catch comorbidities listed
to improve the ascertainment of the burden for previous hospitalisations.
of chronic diseases over a longer period of 2.1 Systematic Literature Search
time [8]. What complicates the use of the and Translations
2.3 The Original Charlson
Charlson Comorbidity Index, are the dif- A systematic literature search was per- Comorbidity Index
ferent updates and adaptations used in formed to identify all articles published in
research, in particular the different ICD- English describing adaptations or modifi- The original Charlson Index was developed
codes used to define the included diseases. cations of the ICD-codes of the Charlson based on a cohort of 559 medical patients,
Currently, many versions are used, and sev- Comorbidity Index for general purpose in and validated in a cohort of women with pri-
eral studies using the Charlson Index do adults. Studies which merely modified the mary breast cancer [3]. This weighted index
not specify which version, ICD-codes or weights of the included comorbidities were grouped 19 clinically relevant comorbidities,
weighting have been used. Therefore, re- excluded. The search was conducted in i.e. those resulting in a ≥20% increase in
producibility is often problematic, and the PubMed (▶ Figure 1), using the following 1-year mortality, in 4 categories according to
validity of the comorbidity variable insuffi- search string (last updated 25th March their assigned weight: 1 point was given to
ciently clear. Especially if comorbidity is 2016): (“International Classification of Dis- patients with an ICD-code for myocardial
assessed as a main exposure, the results eases”[Mesh] OR “ICD”[Tiab] OR infarction, congestive heart failure, periph-
may even be unreliable. The aim of this re- “coding”[Tiab] OR “codes”[Tiab] OR eral vascular disease, cerebrovascular dis-
port was to evaluate which version of the “Charlson”[Title] OR “scores”[Title] OR ease, dementia, chronic pulmonary disease,
Charlson Comorbidity Index ICD-coding “scoring”[Title]) AND (“Charlson”[Tiab] connective tissue disease, peptic ulcer dis-
should be used for general purpose in reg- OR “morbidity”[Title] OR “comorbid- ease, mild liver disease, or diabetes; 2 points
istry-based prognostic research in adults, ity”[Title]). The ICD-code converter of were given for hemiplegia, moderate or se-
in particular when comorbidity is ascer- Statistics Sweden was used to back-trans- vere renal disease, diabetes with end organ
tained based on different (older) ICD-ver- late codes from ICD-version 10 to earlier damage, any malignant tumour, leukaemia
sions. ICD-versions [9]. or lymphoma; 3 points were given for mod-

Methods Inf Med 5/2017 © Schattauer 2017


N. Brusselaers, J. Lagergren: The Charlson Index in Registry-based Research 403

Charlson et al 2008 [14] Halfon et al 2002 [19]


Bottle et al 2011 [18]
• 4 disease categories ‐ Translation into ICD10
‐ Extra codes added ‐ ICD10
Charlson et al added (to predict costs in ‐ 17 categories
‐ 17 categories
1987 [3] primary care) ‐ Switzerland
‐ United Kingdom
‐ 19 categories • ICD9
‐ No ICD codes • 23 categories
Sundararajan et al 2004 [25] Quan et al 2011 [22]
‐ United States • United States
‐ Translation into ICD10‐AM ‐ Updated and validated
‐ 17 categories version, ICD10
Deyo et al 1992 [6] ‐ Australia ‐ 12 categories
‐ Translation into ICD9‐CM ‐ Canada
‐ 17 categories
‐ United States Quan et al 2005 [23] Thygesen et al 2011 [26]
‐ Translation into ICD10 ‐ Combined version ICD10
‐ 17 categories ‐ 19 categories
Romano et al 1993 [7]
‐ Canada ‐ Denmark
‐ Also called ”Dartmouth‐
Manitoba” version
Ramiarina et al 2008 [24]
‐ Translation into ICD9‐CM
‐ Combined version ICD10
‐ 17 categories
‐ 18 categories
‐ ICD9‐CM
Nuttall et al 2006 [21] ‐ Brazil
‐ United States
‐ Two translations into ICD10
Charlson et al 1994
‐ 17 categories Armitage et al 2010 [17]
[5] D’Hoore et al 1993 [15] ‐ United Kingdom ‐ Also called Royal College of
• Modification ‐ Translation into ICD9 ‐ (Exact coding not mentioned) Surgeons adaptation
• 19 categories ‐ 17 categories ‐ Combined version ICD 10
• Age‐modified ‐ Canada ‐ 14 categories
Charlson score

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‐ United Kingdom
• No ICD codes
• United States Christensen et al 2011 [13]
Martins et al 2006 [16] ‐ Translation into ICD8
‐ Translation into ICD9 and ‐ Translation into ICD10 Present study
ICD10 ‐ 19 categories ‐ Back‐translation into ICD8
‐ 19 categories ‐ Denmark and ICD9
‐ Brazil ‐ 14 categories
‐ Sweden
Lix et al 2016 [20]
‐ Translation into ICD10‐CA
‐ 17 categories
‐ United States

Figure 2 Schematic overview of the different adaptations and translations of the Charlson Comorbidity Index identified with the systematic literature
search, and their relation, based on the International Classification of Diseases (ICD) 8th, 9th and 10th versions. ICD-CM = clinical modification; ICD-AM =
Australian modification; ICD-CA = Canadian modification.

erate or severe liver disease; and 6 points homa, leukaemia and any malignant tu- ent ICD-10 Charlson Comorbidity scoring
were given following a diagnosis of meta- mour together as “any malignancy” [6, 7]. versions in use, using different ICD coding
static solid malignant tumours or acquired In general, the first version interpreted the for each comorbidity [13, 17–26].
immunodeficiency syndrome (AIDS). The Charlson categories more strictly [6], while Recently, the Royal College of Surgeons
sum of these 19 comorbidities equals the the “Dartmouth-Manitoba” codes (i.e. de- summarised, re-evaluated and updated 5
total Charlson Comorbidity Index. veloped in 2 universities in the United different versions [19, 21, 23, 25] into a
States and Canada) also included entities modified Charlson Index [17]. This version
which were conceptually comparable – al- reduced the number of comorbidity cat-
3. Results though not all codes of the first version egories from 17 into 14, removing the cat-
were included [7]. One problem with the egory of peptic ulcer disease (since it is not
The search identified 16 studies presenting original index was that some included considered a chronic disease anymore), and
modified or adapted ICD-coding for the diagnoses that could be complications dur- grouping diseases together despite the se-
Charlson Comorbidity Index; 1 using ing the particular hospitalisation episode verity level (which may be difficult to assess
ICD-8 coding [13], 5 using ICD-9 coding (e.g. myocardial infarction, acute stroke) based on registry-based data). For example,
[6, 7, 14–16], and 12 using ICD-10 coding instead of pre-existing comorbidities [17, diabetes mellitus codes with or without
[13, 17–26]. The complex relation between 27]. Without medical records it cannot be complications were grouped into one cat-
the different versions is presented in ▶ Fig- discerned if these are complications or co- egory. This version also eliminated pro-
ures 2–3, with the 5 different versions of morbid conditions; and these codes should cedure codes (because of variation between
ICD-9 coding based directly on the orig- therefore be excluded if the outcome of the countries and coding systems), paediatric
inal Charlson’s index; and the ICD-10 ver- current hospital episode is being evaluated diagnostic codes (since the Charlson Index
sions based on 1–4 of these ICD-9 versions. [3, 7]. At least three other ICD-9 conver- is designed for adults), and very rare en-
Both of the two best-known adaptations sions have been published [14–16]. Yet, in tities. The codes were also simplified to re-
of the Charlson Comorbidity Index into particular the 2 above mentioned versions duce coding errors and improve generalis-
ICD-9 codes reduced the number of co- have been used and converted into ICD-10. ability; aiming towards an internationally-
morbidities from 19 to 17, grouping lymp- Consequently, there are also several differ- applicable and user-friendly tool to assess

© Schattauer 2017 Methods Inf Med 5/2017


404 N. Brusselaers, J. Lagergren: The Charlson Index in Registry-based Research

1987 1992‐1993 1994 2002‐2008 2010‐2016


Two more versions in ICD‐ First back translation into
Original Charlson Index First 3 versions in ICD‐9 Age modified Charlson 9 (19‐23 disease ICD‐8 (19 disease
[3] [6, 7, 15] index [5] categories) [14, 16] categories) [13]
(no ICD coding; 19 (17‐23 disease (no ICD coding; 19
disease categories) categories) disease categories) First 6 versions in ICD‐10 Another 6 versions in
(17‐19 disease ICD‐10 (14‐19 disease
categories) [16, 19, 21, categories) [13, 17, 18,
23‐25] 20, 22, 26]

Figure 3 Time-line of time of publication of the different adaptations and translations of the Charlson Comorbidity Index identified with the systematic lit-

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erature search, based on the different versions of the International Classification of Diseases (ICD).

comorbidity. This version also recom- lated into ICD-9 and ICD-8 versions, fol- 4. Discussion
mended to drop the weighting of comor- lowing the above mentioned rules of eligi-
bidities, and instead categorised the bility [17], and double checked with three Transparency and generalisability are cru-
number of comorbidities into 0, 1, 2 or ≥3. ICD-9 versions [6, 15, 27], and one pre- cial in epidemiological research, especially
The final ICD-10 codes suggested by the viously published ICD-8 version [13]. This when administrative databases are used for
Royal College of Surgeons were back-trans- resulted in the codes presented in ▶Table 1. research purposes. Even if comorbidities

Table 1 International Classification of Diseases (ICD) coding based on the Royal College of Surgeons’ adaptation of the Charlson Comorbidity Index, back-
translated from ICD-10 into ICD-9 and ICD-8.

Comorbidity ICD-10 ICD-9 ICD-8


(Armitage et al 2010)[17] (back-translated) (back-translated)
1 Myocardial infarction I22-I23, I252 410, 412 410, 412
2 Congestive heart failure I11, I13, I255, I42–43, I50, I517 402, 425, 428, 429 4270, 428
3 Peripheral vascular disease I70–73, I770-I771, K551, K558–559, R02, 440–447, 785E, V43D 440–445
Z958–959
4 Cerebrovascular disease G45–46, I60–69 362C, 430–438 430–438
5 Dementia A810, F00–03, F051, G30–31 290, 294 2900–2901
6 Chronic pulmonary disease I26–27, J40-J47, J60–67, J684, J701, J703 416–416, 490–496, 500–505, 506D 490–493, 515–518
7 Rheumatic disease M05–06, M09, M120, M315, M32-M36 710–714, 725 710–712, 734
8 Liver disease B18, I85, I864, I982, K70–71, K721, K729, 070, 456A-456C, 571–573 070, 4560, 571, 573
K76, R162, Z944
9 Diabetes mellitus E10–14 250 250
10 Hemiplegia/paraplegia G114, G81–83 342–344 344
11 Renal disease I12–13, N01, N03, N05, N07, N08, N171, 403–404, 580–586, 588, V420, V451 403–404, 580–583, 792
N172, N18, N19, N25, Z49, Z940, Z992
12 Malignancy C00–26, C30–34, C37–41, C43, C45–58, 140–172, 174–195, 200–208, 140–172, 174–194, 200–207
C60–76, C80–85, C88, C90–97
13 Metastatic tumours C77–79 196–199 196–199
14 AIDS/HIV B20–24 279K -

AIDS, Acquired Immunodeficiency Syndrome; HIV, Human Immunodeficiency Virus.

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N. Brusselaers, J. Lagergren: The Charlson Index in Registry-based Research 405

are used as a confounder and not as main superior to the Charlson score [29, 30]. Yet, Royal College of Surgeons (categorising co-
exposure, a consistent, transparent and the Charlson score is still the most com- morbidities into 0, 1, 2 or ≥3 comorbid-
easy-to-use scoring system should be used, monly used. To have transparency in re- ities) makes the score easy-to-use since all
based on clear and generally accepted defi- search, stating that the Charlson score has comorbidities are considered equally im-
nitions. Yet, it is clear that different ver- been used is clearly insufficient because of portant. Yet, the effect of diseases such as
sions of the Charlson comorbidity index the many versions. Evidently, the treatment metastatic cancer, AIDS and moderate liver
are currently used in research, often with- and prognosis of several of the included co- disease will be underestimated – especially
out stating the exact coding or time-period morbidities has changed dramatically over if individuals will be categorised into the
used. Although disease specific versions of the last 30 years, not in the least consider- group with 1 comorbidity. Therefore, this
comorbidity scoring are gaining popularity, ing the treatment of the human immuno- version of the Charlson index may be not
a general comorbidity score remains of use deficiency virus (HIV), making the original ideal to investigate the impact of comor-
for example to compare different patient 1987 version inappropriate to score comor- bidity on the outcome in all populations,
groups and pathologies in health-economic bidity today. especially if comorbidity is the main expo-
evaluations [28]. Although especially developed for sur- sure of interest. Therefore, it remains im-
In (research) practice, we believe it is gical patients, the version of the Charlson portant to consider alternative scorings,
best to use as much information available Index of the Royal College of Surgeons depending on the study question, available
as possible if measuring chronic comorbid- combines 5 different ICD-10 versions into data and study population [4].

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ities based on hospitalisation or out-patient 1 version, updates the Charlson scoring for To conclude, many versions of the
records. Therefore, we recommend using contemporary use and simplifies the scor- Charlson Index are currently in use, defin-
older time-periods as well, even if the in- ing to enable international use and improve ing comorbidities based on different ICD
formation is coded in older ICD-versions user-friendliness. Therefore, this ICD-10 coding. When assessing comorbidity in
and therefore requires more work. This in- based version appears to be recommend- epidemiological studies based on adminis-
creases the validity of the comorbidity scor- able because of its’ simplicity and recency, trative data, it is essential to report which
ing, since if a patient had diabetes mellitus and has now been back-translated into version of a comorbidity scoring is used,
in 1965, the patient will still have it later in ICD-9 and ICD-8 coding for use in Swed- including a clear description of used ICD
live (even if not recorded for later hospitali- ish administrative databases to quantify version and comorbidity codes.
sation episodes). For power reasons, co- and assess comorbidity in earlier time-
morbidity is often scored in 2–3 categories periods (and consequently improve ascer-
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