Relationship Between Psoriasis and Non-Alcoholic Fatty Liver Disease
Relationship Between Psoriasis and Non-Alcoholic Fatty Liver Disease
Relationship Between Psoriasis and Non-Alcoholic Fatty Liver Disease
Key words: non-alcoholic fatty liver disease (NAFLD), psoriasis, metabolic syndrome.
Address for correspondence: Prof. Krishnasamy Narayanasamy, Department of Hepatology, Madras Medical College, Rajiv Gandhi
Government General Hospital, 600003 Chennai, India, phone: 91-9841170145, e-mail: drkns_1963@yahoo.com
Abstract
Introduction: Various components of metabolic syndrome have an important role in the pathogenesis of both non-alcoholic
fatty liver disease (NAFLD) and psoriasis, suggesting an association between these diseases. However, at present very few studies
have reported on the systematic evaluations of the prevalence of NAFLD in patients with psoriasis disorder.
Aim: To investigate the prevalence of NAFLD in patients with psoriasis vulgaris. The study also evaluated the parallel rela-
tionship between both of the diseases.
Material and methods: Patients over18 years old and with a diagnosis of psoriasis vulgaris at the outpatient unit of Depart-
ment of Dermatology were considered for enrolment and were followed up by the Department of Hepatology, Madras Medical
College. Each and every patient completed a questionnaire, underwent a thorough skin evaluation, and had a right upper quad-
rant ultrasound and fasting blood workup.
Results: Two hundred and fifty patients were enrolled in the study. The participants were predominantly middle aged (mean:
44.74 ±11.989 years), overweight (average body mass index (BMI): 24.772 ±3.611 kg/m2), and male (68%, n = 170). The overall
prevalence of NAFLD among psoriasis was 45.2%.
Conclusions: Non-alcoholic fatty liver disease is highly prevalent among our cohort of patients with psoriasis, occurring in
45.2% of patients. Comorbidity of NAFLD is highly associated with psoriasis, which emphasises that both diseases may develop
simultaneously. Health care providers should be mindful of this association since early evaluation and diagnosis of NAFLD in
patients with psoriasis may play a vital role in alleviating the progression of liver disease.
mean ± standard deviation for continuous variables and Table I. Characteristics of psoriasis subjects (n = 250)
as numbers and percentages for categorical variables.
Characteristics Value
Statistical analyses included the analysis of variance –
ANOVA (for continuous variables) and Pearson’s c2 test Age 44.74 ±11.989
(for categorical variables). The association of NAFLD Gender (male) 170 (68%)
with the psoriasis was assessed by logistic regression Weight 62.54 ±9.608
analysis. Values at p < 0.05 were considered statistically
Height 158.84 ±7.833
significant.
BMI 24.772 ±3.611
Results Waist circumference 91.53 ±13.910
Baseline characteristics of the psoriasis Systolic 120.26 ±15.222
cohort
Diastolic 81.43 ±11.335
To evaluate the prevalence of NAFLD in people with
FBS 114.23 ±25.328
psoriasis, we conducted 9-month hospital-based study.
During the enrolment period, 340 adults with psoria- TGL 202.87 ±109.762
sis were eligible for the study and 250 (73.52%) agreed Cholesterol 214.04 ±40.969
to participate in our study. Their characteristics are
HDL 44.28 ±8.572
summarised in Table I. All participants were diagnosed
with psoriasis vulgaris, in which some of the specific Obese 46 (18.4%)
types were as follows: 49 had chronic plaque psoriasis, Metabolic syndrome 177 (70.8%)
45 had palmoplantar psoriasis, 38 had scalp psoriasis,
Fatty liver 134 (53.6%)
28 patients had psoriasis arthritis, 21 had pustular type,
and 7 had nail type. NAFLD 113 (45.2%)
The participants were largely middle aged (44.74 Alcoholic 22 (8.8%)
±11.989) and the majority were overweight (24.772 Abdominal obesity 120 (48%)
±3.611 kg/m2) and male (68%, n = 170). More than two
Hypercholesterolaemia 160 (64%)
thirds of the participants (70.8%) met the criteria for di-
agnosis of metabolic syndrome based on NCEP – ATP III. Hypertriglyceridaemia 166 (66.4%)
Abdominal obesity was detected in 48% of psoriasis Low HDL 117 (46.8%)
patients. Dyslipidaemia was more commonly observed
Hyperglycaemia 132 (52.8%)
in 96% of patients (abnormal value at least anyone of
lipid profile), and 52.8% of patients were hyperglycae- Hypertension 134 (53.6%)
mic. 53.6% of psoriatic patients had hypertension, and Diabetes 133 (53.2%)
44% of the patients presented with elevated ALT levels.
Elevated ALT 110 (44%)
according to PASI score (mean ± SD: 32.88 ±13.542 vs. showed fibrosis in F1 stage. Cirrhosis of the liver did
23.19 ±12.052; p < 0.0001) (Table II). not occur in any of the NAFLD patients with psoriasis.
Fibrosis scores of NAFLD patients with psoriasis were
higher than non-NAFLD patients with psoriasis. Among Correlation between psoriasis with
the NAFLD patients with psoriasis, 36.2% showed NAFLD and psoriasis without NAFLD
portal and periportal fibrosis with septum (F2–F3). Univariate logistic regression analysis was per-
Most of the NAFLD patients with psoriasis (63.8%) formed to explore the mechanisms underlying the cor-
relation between psoriasis and NAFLD in the 218 pa- Another important finding of our study is multivar-
tients. The significant were observed between NAFLD iate analysis, which has not been carried out in pre-
and non-NAFLD subjects in age, sex, weight, waist cir- vious reports. The variables that were independently
cumference, fasting blood sugar, PASI, metabolic syn- associated with NAFLD among patients with psoriasis
drome, ALT, duration of psoriasis, fibroscan, direct se- were hypertriglyceridaemia (OR = 3.174, 95% CI: 1.565–
rum bilirbin, serum protein and statistical significant 6.438, p < 0.001), hyperglycaemia (OR = 2.495, 95%
was not observed in other variables in univariate anal- CI: 1.191–5.227, p < 0.015), fibro scan (OR = 0.692,
ysis (Table III). 95% CI: 0.553–0.867, p < 0.001), PASI (OR = 0.950,
95% CI: 0.922–0.979, p < 0.001), and duration
Table III. Univariate analysis (OR = 0.865, 95% CI: 0.756–0.990, p < 0.035) and gender
(OR = 2.681, 95% CI: 1.244–5.778, p < 0.012) (Table IV).
Characteristics P-value OR (95% CI)
Age 0.020 1.028 (1.004–1.052)
Discussion
Gender (male) 0.035 1.856 (1.043–3.301)
The hallmark of NAFLD refers to the accumulation
Weight 0.048 0.972 (0.945–1.0) of fat in the liver. Non-alcoholic fatty liver disease is
Height 0.212 0.978 (0.945–1.013) regarded as the hepatic manifestation of metabolic
BMI 0.264 0.960 (0.893–1.032) syndrome and the most common form of chronic liv-
Systolic 0.149 0.987 (0.970–1.005)
er disease throughout world [11–13]. The previously
well-described risk factors for NAFLD include meta-
Diastolic 0.595 1.006 (0.983–1.030)
bolic syndrome and lifestyle habits, such as fructose
FBS 0.006 0.984 (0.973–0.996) consumption and physical activity level, which impact
TGL 0.0001 0.993 (0.990–0.997) disease severity [14]. Recent reports have shown that
Cholesterol 0.237 0.996 (0.990–1.003) people with psoriasis may be at greater risk for devel-
HDL 0.341 0.985 (0.955–1.016) oping of NAFLD [15, 16].
Non-alcoholic fatty liver disease prevalence has
LDL 0.111 1.006 (0.999–1.014)
been estimated to be in the 20–30% range in the gen-
Obese 0.699 1.167 (0.532–2.560) eral population in various countries and is rapidly in-
Metabolic syndrome 0.004 2.581 (1.366–4.879) creasing. The prevalence of NAFLD has become a ma-
Waist circumference 0.001 0.966 (0.947–0.987) jor public health concern in developed and developing
Abdominal obesity 0.006 2.132 (1.239–3.669) countries [17, 18]. Non-alcoholic fatty liver disease is
one such disease that now has potentially enormous
Hypercholesterolaemia 0.785 0.927 (0.536–1.602)
public health consequences due to its progression to
Hypertriglyceridaemia 0.0001 3.510 (1.939–6.327) more severe forms of the disease ranging from ste-
Low HDL 0.227 0.720 (0.422–1.227) atosis to steatohepatitis (NASH), which, in turn, can
Hyperglycaemia 0.0001 2.962 (1.704–5.148) progress into cirrhosis and end stage liver disease and
Hypertension 0.843 1.056 (0.617–1.805) finally the need for liver transplantation. The increasing
incidence of NAFLD throughout world has contributed
Diabetes 0.0001 2.852 (1.640–4.959)
to rising numbers of HCC incidents [19]. There is also
Elevated ALT 0.0001 2.809 (1.617–4.877)
ALT 0.0001 0.951 (0.929–0.973) Table IV. Multivariate analysis
AST 0.087 0.980 (0.957–1.003) Characteristics P-value AOR (95% CI)
AST/ALT 0.0001 4.889 (2.202–10.852) Age 0.136 1.022 (0.993–1.052)
Duration 0.013 0.877 (0.792–0.972) Gender (male) 0.012 2.681 (1.244–5.778)
Fibro Scan 0.0001 0.642 (0.533–0.774) Weight 0.069 0.967 (0.933–1.003)
PASI 0.0001 0.941 (0.918–0.965) Abdominal obesity 0.474 1.291 (0.642–2.593)
S. Bilirubin – total 0.425 0.805 (0.472–1.373) Hypertriglyceridemia 0.001 3.174 (1.565–6.438)
S. Bilirubin – direct 0.702 0.723 (0.137–3.805) Hyperglycaemia 0.015 2.495 (1.191–5.227)
SAP 0.124 1.009 (0.998–1.020) Elevated ALT 0.224 1.563 (0.761–3.209)
Serum protein 0.147 0.816 (0.620–1.074) Duration 0.035 0.865 (0.756–0.990)
Albumin 0.168 1.576 (0.825–3.012) Fibro Scan 0.001 0.692 (0.553–0.867)
Platelet 0.198 1.248 (0.891–1.749) PASI 0.001 0.950 (0.922–0.979)
evidence suggesting that NAFLD individuals are at risk It is reported that metabolic syndrome is more com-
of developing cardiovascular events independently of mon in psoriasis patients [26]. We found higher rates of
conventional risk factors and metabolic syndrome com- metabolic syndrome among NAFLD than non-NAFLD pa-
ponents [20]. tients with psoriasis. However, our major finding in this
Psoriasis is a chronic, inflammatory, immune-medi- study was that psoriasis with NAFLD was positively cor-
ated skin disease. Both innate and adaptive immunity related with three components of metabolic syndrome:
are crucial in the initiation and maintenance of psoriatic hyperglycaemia, hypertriglyceridemia, and abdominal
plaques. Non-alcoholic fatty liver disease began to be obesity, but significant correlation was not observed
considered a part of the metabolic syndrome spectrum, with hypertension and low level of HDL in univariate
and the relationship between NAFLD and psoriasis be- logistic regression analysis, although the levels of HDL
came grounded in their association with metabolic syn- and blood pressure were reported to be higher in psori-
drome and secretion of proinflammatory cytokines. The asis patients with NAFLD than in those with non-NAFLD.
first report of patients with psoriasis and concomitant Although obesity is reported to be highly prevalent
among psoriasis patients, we did not find significant
hepatic steatosis was unexpectedly found during a sur-
correlation between BMI and NAFLD in psoriasis pa-
vey conducted in 2002, which aimed to evaluate pa-
tients. However, we observed a higher number of obese
tients with NAFLD. These patients presented with liver
among psoriasis with NAFLD patients than non-NAFLD
abnormalities seen on ultrasonography and underwent
psoriasis patients. This may be explained by which con-
a liver biopsy, which revealed hepatic fibrosis. Since
cluded that the predominant of our psoriasis patients
then, different population-based surveys have shown
were overweight.
a higher prevalence of NAFLD in patients with psoriasis
In our study we observed that ALT was increased
compared with the general population. It was also ob- in psoriasis patients with NAFLD and highly associated
served that the PASI was higher in patients with both with psoriasis. We did not detect any significant as-
psoriasis and NAFLD than in those with psoriasis only. sociation of NAFLD in other liver function tests in our
We have conducted a study to determine the prev- psoriasis patients. Our study found that DM was com-
alence of NAFLD among patients with psoriasis in our mon in psoriasis patients. We also found that hypercho-
region. The present study reports a notable increase in lesterolaemia was not associated with NAFLD patients
the prevalence of NAFLD when compared with a pre- with psoriasis even though TGL was highly significantly
vious study in 2012 carried out in our region, in which associated with NAFLD patients with psoriasis.
17% prevalence was reported [21]. Our study is the first In multivariate analysis, NAFLD was associated with
to confirm that patients with psoriasis are at increased both the severity and duration of psoriasis. We also ob-
risk for NAFLD, as suggested by previous studies that served that psoriasis is associated with hyperglycaemia
used the same evaluating measures for fatty liver; how- and hypertriglyceridemia. Therefore, it was concluded
ever, our study showed that the prevalence of NAFLD that NAFLD is related to the duration of the disease,
was 45.2%, i.e. the prevalence rate of NAFLD is more components of metabolic syndrome such hyperglycae-
than 2.5-fold higher. It should be noted that we do not mia and hypertriglyceridemia, and closely associated
feel the results of our study discredit the possibility of with the development of psoriasis and NAFLD.
NAFLD prevalence among psoriasis as determined in
other studies conducted in Italy, Netherland, and the Conclusions
USA, which demonstrated that the prevalence was Our findings suggest that NAFLD is frequent in pa-
46%, 47%, and 47%, respectively [22–24]. tients with psoriasis and is also associated with the
Many studies showed that elderly patients are at duration and severity of the disease. Physicians must
increased risk of NAFLD with psoriasis even if the skin be careful of this association and evaluation of NAFLD
disease is mild or moderate and not requiring system- in patients with psoriasis, but future investigation is re-
ic therapy [24, 25]. But an important finding of our quired to determine the most appropriate diagnostic
study showed that a high prevalence is observed even and treatment strategies for these patients.
in middle-aged psoriatic populations; the mean age of
patients was 44.02 years. Conflict of interest
We observed a significant relationship between The authors declare no conflict of interest.
NAFLD and gender. NAFLD was more prevalent in male
gender than in female gender. High BMI levels were fre- References
quent in our NAFLD patients with psoriasis, and this 1. Davidovici BB, Sattar N, Prinz JC, et al. Psoriasis and systemic
finding confirmed the previous findings [21]. inflammatory diseases: potential mechanistic links between
skin disease and co-morbid conditions. J Invest Dermatol 20. Ballestri S, Lonardo A, Bonapace S, et al. Risk of cardiovas-
2010; 130: 1785-96. cular, cardiac and arrhythmic complications in patients with
2. Azfar RS, Gelfand JM. Psoriasis and metabolic disease: epide- non-alcoholic fatty liver disease World J Gastroenterol 2014;
miology and pathophysiology. Curr Opin Rheumatol 2008; 20: 20: 1724-45.
416-22. 21. Madanagobalane S, Anandan S. The increased prevalence of
3. Boehncke WH, Boehncke S, Schon MP. Managing comorbid non-alcoholic fatty liver disease in psoriatic patients: a study
disease in patients with psoriasis. BMJ 2010; 340: b5666. from South India. Australas J Dermatol 2012; 53: 190-7.
4. Menter A, Griffiths CE, Tebbey PW, et al. Exploring the associ- 22. Van der Voort EA, Koehler EM, Dowlatshahi EA, et al. Psoria-
ation between cardiovascular and other disease-related risk sis is independently associated with nonalcoholic fatty liver
factors in the psoriasis population: the need for increased disease in patients 55 years old or older: results from a pop-
understanding across the medical community. J Eur Acad Der- ulation-based study. J Am Acad Dermatol 2014; 70: 517-24.
matol Venereol 2010; 24: 1371-7. 23. Gisondi P, Targher G, Zoppini G, Girolomoni G. Non-alcoholic
5. Paschos P, Paletas K. Non alcoholic fatty liver disease and met- fatty liver disease in patients with chronic plaque psoriasis.
abolic syndrome. Hippokratia 2009; 13: 9-19. J Hepatol 2009; 51: 758-64.
6. Adams LA, Lymp JF, Sauver J, et al. The natural history of non- 24. Roberts KK, Cochet AE, Lamb PB, et al. The prevalence of
alcoholic fatty liver disease: a population-based cohort study. NAFLD and NASH among patients with psoriasis in a tertiary
Gastroenterology 2005; 129: 113-21. care dermatology and rheumatology clinic. Aliment Pharmacol
7. Vilarrasa E, Puig L. Psoriasis: biologic treatment and liver dis- Ther 2015; 41: 293-300.
ease. World J Dermatol 2014; 3: 76-85. 25. Tseng HW, Lin HS, Lam HC. Co-morbidities in psoriasis: a hos-
8. Waist Circumference and Waist-Hip Ratio, Report of a WHO pital-based case-control study. J Eur Acad Dermatol Venereol
Expert Consultation, Geneva, 8–11 December 2008. 2013; 27: 1417-25.
9. Expert Panel on Detection, Evaluation, and Treatment of High 26. Gisondi P, Tessari G, Conti A, et al. Prevalence of metabolic syn-
Blood Cholesterol in Adults. Executive summary of the third drome in patients with psoriasis: a hospital-based case-control
report of The National Cholesterol Education Program (NCEP) study. Br J Dermatol 2007; 157: 68-73.
expert panel on detection, evaluation, and treatment of high
blood cholesterol in adults (Adult Treatment Panel III). JAMA Received: 17.04.2015
2001; 285: 2486-97. Accepted: 10.07.2015
10. Smith CH, Anstey AV, Barker JN, et al. British Association of
Dermatologists guidelines for use of biological interventions
in psoriasis 2005. Br J Dermatol 2005; 153: 486-97.
11. Paschos P, Paletas K. Non alcoholic fatty liver disease and met-
abolic syndrome. Hippokratia 2009; 13: 9-19.
12. Anand SS, Yusuf S, Vuksan V, S, et al. Differences in risk factors,
atherosclerosis, and cardiovascular disease between ethnic
groups in Canada: the Study of Health Assessment and Risk
in Ethnic Groups (SHARE). Lancet 2000; 356: 279-84.
13. Younossi ZM, Stepanova M, Negro F, et al. Nonalcoholic fatty
liver disease in lean individuals in the United States. Medicine
(Baltimore) 2012; 91: 319-27.
14. Abdelmalek MF, Suzuki A, Guy C, et al. Increased fructose con-
sumption is associated with fibrosis severity in patients with
nonalcoholic fatty liver disease. Hepatology 2010; 51: 1961-71.
15. Miele L, Vallone S, Cefalo C, et al. Prevalence, characteristics
and severity of non-alcoholic fatty liver disease in patients
with chronic plaque psoriasis. J Hepatol 2009; 51: 778-86.
16. Gisondi P, Targher G, Zoppini G, et al. Non-alcoholic fatty liver
disease in patients with chronic plaque psoriasis. J Hepatol
2009; 51: 758-64.
17. Hossain P, Kawar B, El Nahas M. Obesity and diabetes in the
developing world – a growing challenge. N Engl J Med 2007;
356: 213-5.
18. Das K, Mukherjee PS, Ghosh A, et al. Non obese population in
a developing country has a high prevalence of non-alcoholic
fatty liver and significant liver disease. Hepatology 2010; 51:
1593-602.
19. Kikuchi L, Oliveira CP, Carrilho FJ. Nonalcoholic fatty liver dis-
ease and hepatocellular carcinoma. Biomed Res Intern 2014;
2014: 106247.