254   Acta Med Indones - Indones J Intern Med • Vol 53 • Number 3 • July 2021

ORIGINAL ARTICLE

ABSTRAK
Latar belakang: Sklerosis sistemik (SSc) merupakan penyakit autoimun sistemik yang mengenai 

jaringan ikat multisistem dan salah satu penyebab terjadinya interstitial lung disease (ILD). Modified 
Rodnan’s Skin Score (MRSS) merupakan pemeriksaan standar baku emas yang bersifat semikuantitatif, 
non-invasif untuk mengukur fibrosis kulit pada SSc. Kelainan fibrosis paru pada SSc terutama berbentuk 
ILD merupakan penyebab mortalitas terbanyak dan seringkali terlambat dalam diagnosis. Pemeriksaan 
baku emas untuk menilai morfologi ILD adalah dengan High Resolution Computed Tomogaphy (HRCT) 
scan thoraks, namun ketersediaannya masih sangat terbatas. Derajat fibrosis kulit berdasarkan MRSS 
pada SSc dapat memprediksi adanya ILD pada beberapa penelitian, namun belum banyak diteliti di 
Indonesia. Tujuan penelitian ini untuk mengetahui hubungan morfologi ILD berdasarkan HRCT scan 
thoraks dengan derajat fibrosis kulit berdasarkan MRSS pada sklerosis sistemik. Metode: Penelitian 
ini merupakan penelitian observasional analitik retrospektif dengan desain cross sectional. Subjek 
penelitian ini adalah pasien sklerosis sistemik yang memiliki data hasil pemeriksaan MRSS dan HRCT 
scan thoraks sejak Juli 2019 hingga Maret 2020. Analisis statistik yang menggunakan uji korelasi 
Spearman’s. Hasil: Terdapat 42 subjek penelitian, terdiri dari 41 perempuan (97.6%) dan satu laki-laki 
(2.4%) dengan rerata usia 41.29±12.045 tahun dengan rentang usia dari 19 tahun hingga 60 tahun. 
Hasil uji korelasi berdasarkan Spearman’s terdapat korelasi sedang dengan R= 0,429 yang bermakna 
(p = 0.005) antara skor morfologi ILD dengan nilai MRSS. Kesimpulan: Terdapat korelasi sedang 
yang bermakna antara skor morfologi Interstitial Lung Disease berdasarkan HRCT thoraks dengan 
derajat fibrosis kulit berdasarkan Modified Rodnan’s Skin Score pada sklerosis sistemik.

Kata kunci: high-resolution computed tomography chest, interstitial lung disease, modified 
Rodnan’s skin score, sklerosis sistemik.

ABSTRACT
Background: Systemic sclerosis (SSc) is a systemic autoimmune disease multiorgan/multisystem 

involvement. Modified Rodnan’s Skin Score (MRSS) is a gold standard for measuring skin fibrosis in 

C o r r e l a t i o n  b e t w e e n  I n t e r s t i t i a l  L u n g  D i s e a s e 
Morphology Scores Based on High-resolution Computed 
Tomography Chest and Skin Fibrosis Degree Based on  
Modified Rodnan’s Skin Score on Systemic Sclerosis

Irma Hassan Hikmat1, Suci S. Ramdhini1, Hari Soekersi1, Sumartini Dewi2,3

1 Department of Radiology, Faculty of Medicine, Universitas Padjadjaran, Hasan Sadikin Hospital, Bandung, 
Indonesia.

2 Division of Rheumatology, Department of Internal Medicine, Hasan Sadikin Hospital, Bandung, Indonesia.
3 Immunology Study Center, Faculty of Medicine, Universitas Padjadjaran, Bandung, Indonesia.

Corresponding Author:
Sumartini Dewi, MD. Division of Rheumatology, Department of Internal Medicine, Immunology Study Center, 
Faculty of Medicine, Universitas Padjadjaran. Jl. Eijkman No. 38, Bandung 40161, Indonesia. 
Email: sumartini.dewi@unpad.ac.id



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INTRODUCTION
Systemic sclerosis (SSc) is a systemic 

autoimmune disease affecting multisystem 
connective tissue and one of the causes of 
interstitial lung disease (ILD).1,2 The number 
of patients with systemic sclerosis continues 
to increase and has the potential for increased 
morbidity and mortality due to visceral organ 
fibrosis.3,4 Data on the  incidence and prevalence 
of systemic sclerosis in Indonesia are not yet 
available. However, the number continues to 
increase and has the potential to become a severe 
and life-threatening disease. Systemic sclerosis is 
the third most common disease in Rheumatology 
Polyclinic of RSUP Dr. Hasan Sadikin Bandung, 
after systemic lupus erythematosus (SLE) and 
rheumatoid arthritis (RA). In 2019, there were 
100 systemic sclerosis patients (7%) of the total 
patients visiting the rheumatology polyclinic. 
The survey was conducted in 2015 - 2016 by the 
rheumatology division, Department of Internal 
Medicine, Faculty of Medicine, Padjadjaran 
University (UNPAD) Bandung at Dr. Hasan 
Sadikin Bandung, and there were 24 (42.1%) 
patients who had involvement of pulmonary 
fibrosis.1,3

In SSc, lung involvement may include 
pulmonary fibrosis or a ground- glass opacity 
image on a high-resolution computed tomography 
(HRCT) chest scan with a forced vital capacity 

(FVC) value of less than 80% and a forced 
expiratory volume/FVC ratio of more than 
80%.5,6 ILD is the leading cause of morbidity and 
mortality in systemic sclerosis patients up to 40% 
within ten years after disease onset.7

Matsuda et al.5 in 2019 stated that there 
is an association between MRSS and organ 
involvement; higher MRSS significantly 
increased the prevalence of SSc-related ILD. A 
study by Deepa et al.6 in India in 2016 revealed 
that Rodnan’s score was significantly associated 
with severe lung involvement. Likewise, a study 
by Cottrell et al.7 in 2014 mentioned that the 
incidence of moderate to severe restrictive lung 
disease (RLD) was associated with an increase 
in skin sclerosis scores. These evidences refer 
that MRSS (Modified Rodnan’s skin score) 
can be used as an alternative marker of lung 
involvement in systemic sclerosis.

MRSS is a semi-quantitative, non-invasive 
gold standard examination to measure skin 
fibrosis in SSc. In SSc, pulmonary fibrosis 
disorder, especially ILD, is the most common 
cause of mortality and lattermost diagnosed. Chest 
X-ray is not specific for ILD. The gold standard 
examination for assessing ILD morphology is the 
High-resolution Computed Tomography (HRCT) 
chest scan, but its availability is still very limited. 
The degree of skin fibrosis based on MRSS on 
SSc can predict the presence of ILD shown in 

SSc. In SSc, lung fibrosis disorders, especially interstitial lung disease (ILD), are the leading cause 
of mortality and often late in diagnosis. High-Resolution Computed Tomography (HRCT) Chest scan 
is a gold standard for evaluating ILD morphology, but its availability is limited. The degree of skin 
fibrosis based on MRSS in SSc can predict the presence of ILD in several studies but has not been 
widely studied in Indonesia. This study aimed to determine the relationship of the ILD morphology 
based on thoracic HRCT scan with the degree of skin fibrosis based on MRSS in SSc. Methods: This 
study is a retrospective analytic observational study with a cross-sectional design. The subjects of this 
study are SSc patients who had data of MRSS and HRCT chest scan from July 2019 to March 2020. 
Statistical analysis uses Spearman’s correlation test. Results: There were 42 study subjects, consisting 
of 41 women (97.6%) and one man (2.4%) with an average age of 39.50 years old (age range of 19 
years to 60 years old). Correlation test results based on Spearman’s show a moderate correlation 
between the morphological score of ILD with MRSS with R = 0.429, which is significant (p = 0.005). 
Conclusion: There is a significant moderate correlation between the morphological scores of ILD 
based on HRCT chest and the degree of skin fibrosis based on MRSS in SSc.

Keywords: High-resolution computed tomography chest, interstitial lung disease, modified 
Rodnan’s skin score, systemic sclerosis.



Irma Hassan Hikmat                                                                                    Acta Med Indones-Indones J Intern Med

256

several studies, but it has not been widely studied 
in Indonesia. Research on the morphological 
relationship between ILD and MRSS has never 
been conducted in Indonesia. It is expected that 
this study would increase the evidence regarding 
MRSS scoring to predict the presence of ILD; 
hence the management of complications of 
systemic sclerosis will be more effective.

METHODS
This research is an observational analytic 

correlation study with a cross-sectional model, 
using retrospective data. This study measures 
the relationship between risk factors and their 
outcome. The risk factors and outcomes were 
observed once and at the same time. The subjects 
of this study were systemic sclerosis patients who 
met the 2013 ACR/EULAR criteria and visited the 
Rheumatology Department of Internal Medicine 
at Dr. Hasan Sadikin Bandung from July 2019 to 
March 2020.

This study has received ethical approval from 
the Research Ethics Committee of the Faculty of 
Medicine, Padjadjaran University, and Dr. Hasan 
Sadikin Bandung with a letter of ethics number 
LB.02.01/X.65/73/2020.

Subjects
The inclusion criteria for the subjects of 

this study were subjects aged 18-60 years old 
diagnosed with systemic sclerosis, who have 
completed data on the degree of skin fibrosis based 
on MRSS and spirometry results of restrictive 
lung abnormalities. Subjects with restrictive lung 
disease due to autoimmune diseases other than 
systemic sclerosis and subject with tuberculosis 
and malignancy were excluded from our study.

MRSS and ILD Evaluation
The range of MRSS values is 0 - 51. The 

standard value is achieved by transforming 
MRSS values into an interval scale with the 
following formula: Transformation value 100 
= (Actual value - lowest actual value)/Value 
range x 100.

The HRCT chest examinations utilize 
t h e  M u l t i d e t e c t o r  C T / M D C T 1 2 8 - S l i c e 
(Hitachi SCENARIA SE-128 –slice, Hitachi 
Healthcare), which produce digital Imaging and 
Communication in Medicine (DICOM) data.

The ILD morphological score was obtained 
from the analysis of HRCT imaging based on 
the Warrick semi-quantitative method. The total 
score based on the parenchymal lesion pathology 
and the extent of the lesion ranged from 0 to 
30.45.54. Degree of severity include Mild (<8), 
Moderate (8-15), and Severe (> 15).

Statistical Analysis
Statistical analysis was conducted to assess 

the correlation between the ILD morphological 
score based on chest HRCT and the pulmonary 
fibrosis score based on MRSS on systemic 
sclerosis patients. Spearmen correlation was used 
to determine the correlation between numerical 
and ordinal data. Interpretation of hypothesis 
test results was based on correlation strength, 
correlation direction, and p-value: Correlation 
strength (r) based on Guillford’s criterion (1956): 
0.0 - <0.2 = very weak; 0.2 - <0.4 = weak; 0.4 - 
<0.7 = moderate; 0.7 - <0.9 = strong; 0.9 -1.0 = 
very strong.

RESULTS
The study subjects were 42 patients who met 

the inclusion and exclusion criteria as described 
in Figure 1.

Subject diagnosed with systemic sclerosis and have 
completed data on MRSS and restrictive lung 

abnormalities (n=43)

One subject was older than 60 year old (n=1)

Subject met inclusion and exclusion criteria (n=42)

Assesment of skin fibrosis (MRSS) and
ILD score based on HRCT Thorax

Data analysis

Figure 1. Patient flow chart.

Table 1 shows a total of 42 study subjects 
consisting of 41 women (97.6%) and one 
male (2.4%) with an average age of 39.5 years 
old and age range of 19 to 60 years old. The 
median duration of disease was three years 
with the range from 1 to 13 years. Most initial 
symptoms were presented as skin fibrosis in 



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38 (90.5%) subjects. Previous chest X-ray 
results were normal in 23 (55%) subjects, 
bronchopneumonia in 9 (21.4%) subjects, and 
bronchitis in 3 (7.1%) subjects, respectively. 
Only one (2.4%) patient was described as ILD.

After HRCT chest was performed, the 
ground glass opacities were found in all 
study subjects, septal or subpleural lines in 
40 (95.2%) subjects, irregular pleural margins 
in 32 (76.2%) subjects, honeycombing in 23 
(54.8%) subjects, and subpleural cysts in 19 
(45.2%) subjects.

Table 2 shows an overview of the ILD 
m o r p h o l o g i c a l  s c o r e ,  I L D ,  a n d  M R S S 
morphological categories. The ILD morphological 
score has a median of 18.00 with a range of 6.00-
27.00, consisting of 4 (9.5%) mild subjects, 11 
(26.2%) moderate) subjects and 27 (64.3%) severe 
subjects. MRSS has a mean of 18.93 (SD 8.247).

Table 2. ILD Morphological Score, ILD and MRSS 
Morphological Categories.

Variables N=42

ILD Morphological Score

Median 18.00

Range (min-max) 6.00-27.00

ILD Morphological Category, n (%)

Mild 4 (9.5)

Moderate 11 (26.2)

Severe 27 (64.3)

MRSS

Mean (SD) 18.93 (8.247)
Note: Categorical data are presented with number/
frequency and percentage, while numeric data are 
presented with mean, median, standard deviation, and 
range.

Table 3. Analysis of the correlation between ILD 
Morphological Score and MRSS

Variables Correlation R p-value

Correlation between 
Skor Morphological 
ILD score and MRSS 
value

Spearman 0.429 0.005**

Note: p-value significance <0.05. Sign ** indicates statistically 
significant or significant a. r: correlation coefficient.

Table 3 shows the Spearman’s correlation test 
between the ILD morphological score and MRSS 
obtaining a p-value of 0.005 (p-value <0.05) and 
an R-value of 0.429 (Guilford’s criteria). R-value 
> 0.40 (<0.70) indicates a moderate correlation 
between the ILD morphological score and the 
MRSS score.

MRSS value towards ILD morphological 
score shows a positive trend (Figure  2), which 
is explained by an increase in the MRSS value yet 
followed by an increase of ILD morphological 
score.

DISCUSSION
The results of this study show that the 

female distribution was more than male, i.e. 41 
(97.6%) women and one (2.4%) man, with the 
median age of 39.5 years old. This is consistent 
with research by Vinent et al, Denton et al. and 
Budiman et al. stating that systemic sclerosis 
patients are dominated by women compared to 
male  patients, with the most frequent range in 
patients at age 25-55 years.1-3

Table 1. Subject Characteristic.

Variables N=42
Sex, n (%)

Male 1(2.4)
Female 41(97.6)

Age
Median 39.50
Range (min-max) 19.00-60.00

Duration of disease (years)
Median 3.00
Range (min-max) 1.00-13.00

Initial symptoms, n (%)
Skin Fibrosis 38 (90.5)
Raynaud’s Phenomenon 4 (9.5)

Chest X-ray, n (%)
Normal 23 (54.8)
Bronchopneumonia 9 (21.4)
Bronchitis 3 (7.1)
Pneumonia 2 (4.8)
Inactive pulmonary TB 2 (4.8)
Pleura thickening 1 (2.4)
Active pulmonary TB 1 (2.4)
Interstitial lung disease 1 (2.4)

Morphology of ILD, n (%)
Ground glass opacities 42 (100)
Irregular pleural margin 32 (76.2)
Septal or subpleural lines 40 (95.2)
Honeycombing 23 (54.8)
Subpleural cyst 19 (45.2)

Note: Categorical data are presented with number/
frequency and percentage, while numeric data are 
presented with mean, median, standard deviation, and 
range.



Irma Hassan Hikmat                                                                                    Acta Med Indones-Indones J Intern Med

258

Chest x-ray examination obtained normal 
results in 23 (55%) study subjects, whereas the 
others (45%) suggested bronchopneumonia 
disorders, bronchitis features, pneumonia, old 
pulmonary tuberculosis, pleural thickening, 
active pulmonary tuberculosis, and ILD. In SSc, 
patients with early symptoms of pulmonary 
involvement may have normal chest x-rays, 
but this does not eliminate the possibility of 
ILD. The ground-glass image is predominantly 
found in the basal lung area and can only be 
assessed in 25-44% of SSc patients.8,9 This chest 
x-rays imaging was described previously as 
bronchopneumonia, bronchitis, pneumonia, and 
pulmonary tuberculosis.

In this study, all subjects with the mild to 
severe category had ground-glass opacities 
m o r p h o l o g y  b e c a u s e  o f  i n c r e a s e d  l u n g 
attenuation. This is consistent with research by 
Deepa et al. in 2016 in the Italian population, 
explaining that the initial changes of the 
ILD process were alveolitis which featured 
ground-glass opacity, septal/subpleural lines, 
and irregular pleural margins as a result of the 
thickening of the interstitial intralobular tissue. 
The subsequent process is fibrosis which gives a 
honeycombing and subpleural cyst morphology. 
Histologically, ILD in SSc includes non-specific 
interstitial pneumonia (NSIP) with more 
inflammatory features and less fibrosis, usual 
interstitial pneumonia (UIP) characterized by 
fibrosis and scarring, as well as a combination 
of both.6,10,11,12 In addition, Table 4 explains 
the value of the MRSS with a mean of 18.93 

(SD 8.247), where is different from the research 
by  by Matsuda et al.5 with a mean of 9.9 (SD 
8.9) and Deepa et al.6 with a mean of 29.9 (SD 
7.13). Correlation between ILD morphological 
score and MRSS value.

Our study revealed that there was a 
moderately significant correlation between ILD 
morphological scores based on chest HRCT and 
the degree of skin fibrosis based on MRSS. Our 
results are in line with Matsuda et al.5 in 2019 
in the Japanese population that stated higher 
MRSS was associated with the presence of ILD 
in SSc (p <0.05). Deepa et al.6 in 2016 in the 
Indian population stated that Rodnan’s score 
was significantly associated with severe lung 
involvement (p = 0.031). Cottrell et al.7 in 2014 
showed that in the United States population 
patients with higher skin fibrosis scores may 
develop to moderate to severe restrictive 
pulmonary involvement (p <0.001).

The strong correlation between skin fibrosis 
and pulmonary fibrosis as ILD in SSc patients may 
be affected by similarities in the pathophysiology 
of skin and lung involvement in SSc, namely the 
presence of inflammatory cell invasion in the 
early stages and proliferation accompanied by 
degeneration of collagen fibers in the late stages 
of the disease.8

A similar study by Wu et al.13 in 2018 
used a large European Scleroderma Trial and 
Research (EUSTAR) database, multicenter and 
prospective study to assess the association of 
increased skin fibrosis with organ involvement 
and increased mortality in diffuse SSc patients. 

Figure 2. Correlation between ILD Morphological Score and MRSS Value.

0

10

20

30

40

50

0 5 10 15 20 25 30

M
R

SS

Score of Morfologi ILD



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259

Out of 1021 subjects, 78 subjects had increased 
skin fibrosis within one year of observation. The 
study found that the increase in skin fibrosis in 
one year was associated with decreased lung 
function (p = 0.004) and a worse survival rate (p 
= 0.063); hence it can be confirmed that MRSS 
is an alternative marker for diffuse SSc.13

A study by Wangkaew et al.14 in 2016 in the 
Thai population showed a correlation between 
changes in HRCT and changes in clinical 
variables such as FVC, MRSS, erythrocyte 
sedimentation rate (ESR), and changes & SpO2 
in the early phase of SSc patients. On the other 
hand, a study by Yani et al.15 in 2019 concluded 
there is no correlation between serum Krebs 
von den Lungen (KL-6) levels with FVC and 
MRSS value of subjects with both restrictive 
lung disease and diffuse type systemic sclerosis. 
The KL-6 is a serum biomarker that IS produced 
by alveolar pneumocytes WHENEVER there is 
a fibrogenesis activity in the lungs. This study 
used the cohort method involving 31 subjects 
who underwent HRCT chest examination at 
the beginning and observation for the next 12 
months, then calculated the HRCT score based 
on ILD morphology. The HRCT score was found 
to be a useful and sensitive method for assessing 
disease progression in SSc-related ILDs (r = 
−0.38, P <0.05).

However, our study did not reflect the initial 
incidence of ILD in SSc patients. SSc patients 
who were sent for HRCT scan with suspected 
ILD were already undergoing modification 
therapy for Anti Rheumatic Drugs (DMARD)/
conventional immunosuppressants with different 
doses and duration of therapy. There was no 
initial data on the chest HRCT examination when 
the patient was diagnosed with SSc; therefore, 
the chest HRCT examination during the study 
did not reflect the changes that occurred. Further 
cohort research with the completed HRCT dan 
MRSS baseline data is required in SSc patients 
for early detection of ILD and evaluating changes 
over a period of time.

CONCLUSION
T h e r e  w a s  a  m o d e r a t e l y  s i g n i f i c a n t 

correlation between the ILD morphological 
score based on HRCT chest and the degree of 

skin fibrosis based on modified Rodnan’s skin 
score on systemic sclerosis.

ACKNOWLEDGMENTS
IH, SS, HS, and SD conceived and designed 

the study. SS acquired the data. All authors 
contributed to the writing of the manuscript. This 
study was funded by Universitas Padjadjaran 
Internal Grant.

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