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Report

High burden of the metabolic syndrome and its component


disorders in South Africans with psoriasis
Nasrin Goolam Mahyoodeen1, MBChB, FCP (SA), Cert. Endo. & Metab. (SA) ,
Nigel J. Crowther2, PhD, Tracy Snyman2, BSc (Hons),
Lushen Pillay3, MBChB, FCDerm, MMed (Derm), and Mohammed Tikly1, FRCP, PhD

1
Department of Internal Medicine, Chris Abstract
Hani Baragwanath Academic Hospital, Background Psoriasis is associated with cardiometabolic diseases (CMDs) in Caucasians,
Faculty of Health Sciences, University of
but no data is available from sub-Saharan populations on either CMD prevalence or
the Witwatersrand, Johannesburg, South
Africa, 2Department of Chemical Pathology,
psoriasis risk factors. Our aim was to investigate the prevalence of CMDs in a
National Health Laboratory Service, predominantly non-Caucasian cohort of South Africans with psoriasis and to determine the
University of the Witwatersrand, principal risk factors associated with psoriasis.
Johannesburg, South Africa, and Methods This was a cross-sectional case-control study of adult psoriasis patients
3
Department of Dermatology, Faculty of
(n = 103) and controls (n = 98), comparing sociodemographic, anthropometric, clinical, and
Health Sciences, University of the
biochemical characteristics. The groups were matched for gender, ethnicity, and body
Witwatersrand, Johannesburg, South Africa
mass index (BMI).
Correspondence Results The prevalence of metabolic syndrome (MetS) (52.4% vs. 33.7%; P = 0.007), type
Nasrin Goolam Mahyoodeen, MBChB, FCP 2 diabetes (T2D) (25.2% vs. 4.1%; P < 0.0001), and hypertension (70.9% vs. 46.6%;
(SA), Cert. Endo. & Metab. (SA)
P = 0.001) were all higher in the psoriasis group. High-sensitivity CRP was higher in
Department of Internal Medicine
Chris Hani Baragwanath Academic Hospital
psoriasis patients than controls (4.70 (2.00, 10.9) vs. 2.00 (1.10, 4.80) ng/ml; P < 0.0005).
PO Box Bertsham 2013 Multivariable logistic regression analysis showed that severe psoriasis was independently
South Africa associated with MetS (odds ratio [95% CIs]: 4.42 [1.72, 11.4]; P = 0.002), T2D (11.3 [3.07,
E-mail: mahyoodeen@yahoo.com 41.3]; P = 0.0002), and hypertension (2.48 [0.97, 6.32]; P = 0.05), whilst for psoriasis the
principal risk factors were smoking (3.87 [1.97, 7.63]; P < 0.0001) and hsCRP (1.05 [1.00,
This study was conducted at the
1.10]; P = 0.029), with completion of high school (0.23 [0.11, 0.48]; P < 0.0001) being
following institutions: Chris Hani
Baragwanath Academic Hospital, Charlotte
protective.
Maxeke Johannesburg Academic Hospital, Conclusions In this population, psoriasis is characterized by a high burden of CMDs,
Helen Joseph Hospital. particularly in those subjects with severe psoriasis. Inflammation plays a role in the etiology
Conflicts of interest: None. of psoriasis, whilst smoking and poor education further increase disease risk.
Funding: This work was supported by
grants from the Carnegie Corporation of
New York, NY, USA. Grant Number: B
8749.RO1 to NGM, the National Research
Foundation (Thuthuka to NGM), the Astra
Zeneca Research Trust (to NGM), and the
Medical Research Council of South Africa
(Self-initiated Research Grant to MT).

doi: 10.1111/ijd.14348

prevalence of metabolic syndrome (MetS)4 and its component dis-


Introduction
orders, i.e., obesity,5 hypertension,6 type 2 diabetes mellitus
Psoriasis is a complex, chronic immune-mediated inflammatory (T2D),7 and dyslipidemia,8 in psoriasis. These cardiometabolic
skin disorder that has a global prevalence ranging between 0.91% diseases (CMDs) are particularly more prevalent in patients with
and 8.5%.1 A wide range of comorbidities associated with psoria- severe psoriasis.4–8 Previous studies have also shown lower vita-
sis have been identified, including inflammatory arthritis (referred min D levels in psoriasis patients compared to controls.9
2 2 2
to as psoriatic arthritis [PsA]), Crohn’s disease, malignancies, There is increasing evidence that there is a link between
and chronic kidney disease.3 Furthermore, several studies in chronic inflammation and CMDs, including atherosclerosis.10
mainly Caucasian populations have shown an increased Chronic subclinical systemic inflammation accelerates
1

ª 2018 The International Society of Dermatology International Journal of Dermatology 2018


2 Report Metabolic syndrome and psoriasis in South Africa Goolam Mahyoodeen et al.

atherosclerosis, and histological studies demonstrate the pres- and the lower border of the last rib. Hip circumference (HC)
ence of inflammation in atherosclerotic lesions.11 Further evi- was taken around the widest portion of the buttocks. Blood
dence linking inflammation to atherosclerosis is C-reactive pressure (BP) was measured with the subject seated, and the
protein (CRP), a well-recognized biomarker of inflammation is mean of two readings, 10 minutes apart, was documented.
also associated with atherothrombotic disease.12 Inflammation Metabolic syndrome was defined according to 2009
has also been linked to the development of rheumatoid arthri- Harmonized Guidelines.21 In patients without a history of T2D
tis,13 T2D,10 and MetS and its component disorders.10 It has and hypertension, newly diagnosed T2D was based on fasting
therefore been hypothesised that the high prevalence of CMDs plasma glucose >7 mmol/l,22 and impaired fasting glucose and
in psoriasis may arise from the high inflammatory milieu.14,15 hypertension were defined as per the Harmonized Guidelines.21
In the absence of any published data on CMD comorbidities in Estimated glomerular filtration rate (eGFR) was calculated using
sub-Saharan Africa, the primary aim of this study was to determine the abbreviated Modified Diet in Renal Disease equation.23 The
the burden of MetS, and its component diseases, in a predomi- Framingham 10-year risk of general cardiovascular disease
nantly non-Caucasian cohort of South African psoriasis patients. (CVD) score24 was used to calculate CVD risk in all patients.
The secondary aims were to determine the relation of MetS with Overnight fasting venous blood samples were tested for
disease severity and the association of hsCRP, as a marker of plasma glucose, serum lipids (total cholesterol, triglycerides and
inflammation, serum vitamin D levels, estimated glomerular filtra- high density lipoprotein cholesterol [HDL-C]), urea, and
tion rate (eGFR), and sociodemographic factors with psoriasis. creatinine, using enzymatic methods on the ADVIA 1800
Chemistry Systems Analyzer (Siemens Healthcare Diagnostics,
Tarrytown, NY, USA). The LDL-C was calculated using the
Patients and methods
Friedewald formula.25 High-sensitivity C-reactive protein
This is a cross-sectional case-control study of patients with (hsCRP) and lipoprotein (a) (Lp[a]) were measured using an
psoriasis attending the dermatology and rheumatology clinics at immunoturbidimetric method and 25-hydroxyvitamin D levels
three academic hospitals in Johannesburg, South Africa. (25[OH]D) using a chemiluminescence assay on the
Consenting adult psoriasis and PsA patients, 18 years and ARCHITECT c8000 System (Abbott, Lake Forest, Illinois, USA).
older, were recruited. The diagnosis of psoriasis and/or PsA
was made by a consultant dermatologist or rheumatologist. Statistical methods
Exclusion criteria were human immunodeficiency virus infection, Descriptive statistics for continuous variables are presented as
inflammatory arthritis due to another cause, and pregnancy. mean  standard deviation (SD) or median and interquartile
Control subjects were individuals without any known chronic ranges (IQR) for normal or skewed data, respectively. Skewed non-
immune-mediated inflammatory disorder and were matched for normal continuous variables were log transformed before applying
geographical area of residence, gender, ethnicity, and body parametric statistical tests. Categorical variables were compared
mass index (BMI). They were recruited by requesting patients across groups using the v2 test. Continuous variables were
to bring in an unrelated individual from their area of residence. compared between groups using Student’s unpaired t-test and
The study was approved by the University of the Witwatersrand where appropriate ANCOVA was used with adjustment for age and
Human Research Ethics Committee (M1403100). WC. Logistic regression analysis was used to assess whether the
A combination of clinical records review, clinical examination, relationships of mild and severe psoriasis with MetS, T2D,
and blood investigations, done at the time of the clinical hypertension, high triglycerides, and low HDL-C were affected after
examination, were documented. Socioeconomic status was adjusting for possible confounders. Risk factors for psoriasis were
assessed using a validated questionnaire based on access to 12 isolated by performing univariate regression analyses of study
common personal assets such as a motor vehicle, refrigerator, variables. All variables with P < 0.20 in the univariate models were
and television set.16 A score of >10 was categorized as high included into a single multivariable logistic regression model.
SES. Level of education status was categorized as either Backward, stepwise removal of non-significant variables was
completion of high school or not. Smoking status was categorized performed until all variables in the model were significantly
as either current/ex-smoker or never smoked. Severity of (P < 0.05) related to psoriasis. All analyses were performed using
cutaneous involvement was assessed by the Psoriasis Area and Statistica version 13.2 (StatSoft, Tulsa, OK, USA).
Severity Index (PASI) score.17 Severe psoriasis was defined as
the presence of one or more of the following: (1) PASI score
Results
>10,18 (2) systemic therapy for psoriasis,19,20 and (3) PsA.20
Anthropometric data included weight in kilograms (kg), Demographic and clinical and cardiometabolic
measured with light clothing and no shoes, and height characteristics
measured to the nearest centimeters (cm) to calculate the BMI. The demographic, clinical, and cardiometabolic characteristics of
Waist circumference (WC) was measured using a soft tape the 103 patients and 98 control subjects are shown in Table 1.
measure at the mid-point of the upper border of the iliac crest Most of the patients were of either Indian (42.1%) or mixed

International Journal of Dermatology 2018 ª 2018 The International Society of Dermatology


Goolam Mahyoodeen et al. Metabolic syndrome and psoriasis in South Africa Report 3

ancestry (31.8%), and only 11.7% were Caucasian and 14.6% HbA1c levels remained statistically significant (P = 0.015 and
black African patients. The mean  SD disease duration for psori- P = 0.013, respectively) after adjusting for age and WC.
asis was 18.9  13.3 years and median (IQR) PASI score was The median hsCRP in the psoriasis group was more than
4.80 (2.40, 11.7). Sixty-one (59.2%) patients were deemed to have twice that in the control group (P < 0.0005), the difference per-
severe psoriasis, and 28 (27.2%) had PsA. There were no differ- sisting after adjusting for age and WC (P = 0.002). The Fram-
ences in age and gender between patients with severe and mild ingham CVD risk score was significantly higher in psoriasis
psoriasis (P = 0.85 and P = 0.81, respectively). The prevalence of patients than in controls (P < 0.0001). No significant differences
smoking was significantly higher in psoriasis patients compared to in cholesterol-related lipid levels, glucose and vitamin D levels,
the control group (P < 0.0005). The psoriasis group was of lower urea, creatinine, and eGFR were observed.
SES than the control group, with respect to both ownership of
household items and education (both comparisons, P < 0.0005). Prevalence of metabolic syndrome and its components
There was a high prevalence of obesity in both patients and con- The prevalence of MetS was significantly higher in the psoriasis
trols (50.5% and 38.8% respectively). The psoriasis group had a sig- group than the control group (52.4% vs. 33.7%; P = 0.007), as
nificantly greater WC (P = 0.004), higher systolic and diastolic BP were T2D (25.2% vs. 4.1%; P < 0.0005) and hypertension
(P = 0.0002 and P = 0.005, respectively), triglyceride (P = 0.047), (70.9% vs. 46.6%; P = 0.001). There were no significant differ-
and HbA1c levels (P < 0.0005); and a trend towards lower HDL-C ences in the prevalence of low HDL-C levels (28.2 vs. 21.4%;
levels (P = 0.054). The difference in WC remained significant after P = 0.27) or hypertriglyceridemia (26.2 vs. 19.4%; P = 0.25)
adjustment for age (P = 0.023) and differences in systolic BP and between the two groups.

Table 1 Demographic, clinical, and Psoriasis Controls


cardiometabolic characteristics of Variable n = 103 n = 98 P value
South Africans with psoriasis and
control subjects Female gender (n [%]) 55 (53.4) 61 (62.2) 0.204
Age (years) 53.3  14.5 47.9  14.5 0.009
Disease duration (years) 18.9  13.3 – –
PASI score 4.80 (2.40, 11.7) – –
Psoriatic arthritis (n [%]) 28 (27.1) – –
Smokers (n [%]) 61 (59.2) 26 (26.5) <0.0001
Systemic therapy (n [%]) 43 (41.7) – –
High SES (n [%]) 50 (48.5) 74 (75.5) <0.0001
Completed high school (n [%]) 52 (50.5) 81 (82.7) <0.0001
BMI (kg/m²) 31.6  8.42 29.3  6.67 0.058
Obesity (n [%]) 52 (50.5) 38 (38.8) 0.095
Waist circumference (cm) 101  16.4 94.5  15.2 0.004
Hip circumference (cm) 107  14.7 103  12.1 0.073
Waist : hip ratio 0.946  0.09 0.916  0.11 0.035
Systolic BP (mmHg) 141  24.6 129  17.2 0.0004
Diastolic BP (mmHg) 86.4  12.8 81.5  11.6 0.005
HbA1c (%)a 6.20 (5.90, 6.90) 5.95 (5.55, 6.30) <0.0001
Glucose (mmol/l)a 5.71 (4.70, 6.00) 5.20 (4.20, 5.60) 0.744
Total cholesterol (mmol/l)a 5.31 (4.45, 6.20) 5.31 (4.62, 6.29) 0.176
HDL cholesterol (mmol/l)a 1.21 (1.05, 1.56) 1.37 (1.10, 1.73) 0.054
LDL cholesterol (mmol/l)a 3.24 (2.55, 4.04) 3.38 (2.64, 4.13) 0.180
Triglycerides (mmol/l)a 1.60 (1.05, 2.01) 1.11 (0.83, 1.76) 0.047
Lipoprotein (a) (mg/dL)a 25.3 (9.40, 38.8) 21.4 (10.0, 38.8) 0.971
hsCRP (ng/ml)a 4.70 (2.00, 10.9) 2.00 (1.10, 4.80) <0.0001
Framingham risk scoreb 19.1 (8.47, 32.5) 7.25 (3.65, 13.8) <0.0001
Vitamin D (ng/ml)a 19.0 (12.6, 24.1) 18.1 (13.1, 24.3) 0.582
Urea (mmol/l)a 5.40 (4.20, 6.85) 5.40 (4.40, 6.00) 0.421
Creatinine (lmol/l)a 87.0 (71.0, 102) 79.0 (71.0, 94.0) 0.130
Estimated GFR (ml/min/m2)a 70.8 (63.8, 83.4) 74.9 (66.0, 91.8) 0.140

PASI, Psoriasis Area and Severity Index; SES, socioeconomic status; BMI, body mass
index; BP, blood pressure; HbA1c, hemoglobin A1c; HDL, high-density lipoprotein; LDL,
low-density lipoprotein; hsCRP, highly sensitive quantification of C-reactive protein; GFR,
glomerular filtration rate.
Data given as mean  SD, median (interquartile range) or n (%).
a
N = 91 and N = 97, for cases and controls, respectively.
b
N = 80 and N = 79, for cases and controls, respectively.

ª 2018 The International Society of Dermatology International Journal of Dermatology 2018


4 Report Metabolic syndrome and psoriasis in South Africa Goolam Mahyoodeen et al.

Subgroup analysis showed the prevalence of MetS was sig- Risk factors associated with psoriasis
nificantly higher in the severe psoriasis subgroup (65.6%) com- Logistic regression analysis demonstrated that the principal risk
pared to both the mild psoriasis subgroup and control group factors associated with psoriasis were smoking (3.87 [1.97,
(33.3% and 33.7%, respectively, P < 0.0005 for both) (Fig. 1). 7.63]; P < 0.0001) and hsCRP (1.05 [1.00, 1.10]; P = 0.029),
In the case of T2D, compared to a prevalence of 4.1% in the with completion of high school (0.23 [0.11, 0.48]; P < 0.0001)
control group, the prevalence was increased in both the severe being protective (Table 3).
and mild psoriasis subgroups (31.1%, P < 0.0005 and 16.7%,
P = 0.01, respectively). Hypertension was more prevalent only
Discussion
in the severe psoriasis subgroup (73.8% vs. 49.0% in control
group, P = 0.002). The prevalence of a low HDL-C was higher In this case-control study of mainly indigent urban South Afri-
in the severe psoriasis subgroup (36.1%) when compared to cans, we found a higher prevalence of MetS, hypertension, and
both the control group (21.4%, P = 0.043) and the mild psoria- T2D in patients with psoriasis, even after adjusting for possible
sis subgroup (16.7%, P = 0.025). There was no difference in confounders. Moreover, we observed a risk-gradient for CMD,
the Framingham CVD risk score between patients with severe sometimes referred to as the ‘psoriatic march’,14 where the risk
and mild disease (21.4 [8.05, 34.2] vs. 18.0 [8.66, 30.9], respec- is greatest in severe psoriasis and less so in mild disease. The
tively, P = 0.61). However, both groups had a significantly Framingham CVD risk score was also found to be higher in the
higher score compared to controls (7.25 [3.65, 13.8], psoriasis group compared with the control group.
P < 0.0001 for both groups). A third of the control group fulfilled the criteria for MetS, com-
When we compared patients with PsA (n = 28) to those with pared to more than 50% in the psoriasis group of whom 70%
cutaneous psoriasis only (n = 75), the former group had a had hypertension and 25% had T2D. The prevalence rates of
higher prevalence of MetS (71.4% vs. 45.3%, P = 0.018) and MetS in both the general population and in patients with psoria-
low HDL-C levels (53.6% vs. 18.7%, P = 0.0004). However, no sis are substantially higher than reported in Western industri-
significant differences were noted in the prevalence of T2D alized countries but similar to those in developing countries.
(32.1% vs. 22.7%, P = 0.33), hypertension (78.6% vs. 68.0%, The prevalence of MetS varies from 13.5–25.9% for the general
P = 0.28), or high TG levels (32.1% vs. 24%, P = 0.52) or in population to 20.8–34.2% in psoriasis patients in the United
the Framingham CVD risk score (22.1 [8.05, 42.7] vs. 18.0 States,26 United Kingdom,27 and Italy.28 In developing countries
[8.66, 30.7], P = 0.52) between those with PsA and those with like India29 and Tunisia,30 the prevalences are in the order of
cutaneous psoriasis, respectively. 30% for the general population and 40–44% in psoriasis
Logistic regression analysis showed that, after adjusting for patients.
potential confounders (age, BMI, hsCRP, smoking, education, That more than 50% of the patients and 38% of controls in
and SES), severe but not mild psoriasis, compared with no pso- the present study were obese is a reflection of the growing
riasis, was associated with a higher risk of MetS (P = 0.002), problem of obesity in South Africa. In the South African National
T2D (P < 0.0005), and a trend towards an association with Health and Nutrition Examination Survey (of 7,267 subjects),
hypertension (P = 0.05) (Table 2). Neither mild (P = 0.48) nor the overall prevalence of obesity was 28.9%.31
severe psoriasis (P = 0.32) were associated with an increased The risk gradient where the highest risk for CMD is associ-
risk of low HDL-C or an increased risk for high TG levels (data ated with severe psoriasis is a phenomenon that has been ele-
not shown). gantly demonstrated in several previous studies. The seminal

Controls
80%
Mild PsO
70%
Severe PsO
60%

50% ***
Percent

40%
*** *** Figure 1 Prevalence of cardiometabolic
30%
* diseases in South Africans with psoriasis.
20% * * PsO, psoriasis; MetS, metabolic syndrome;
T2D, type 2 diabetes; HT, hypertension;
10% +
*** HyperTG, hypertriglyceridemia; HDL, high
0% density lipoprotein cholesterol. *P < 0.05,
**P < 0.005, ***P < 0.0005 vs. severe PsO;
MetS T2D HT HyperTG Low HDL +
P < 0.05 vs. mild PsO.
Cardiometabolic diseases

International Journal of Dermatology 2018 ª 2018 The International Society of Dermatology


Goolam Mahyoodeen et al. Metabolic syndrome and psoriasis in South Africa Report 5

Table 2 Logistic regression models showing relationship of mild and severe psoriasis with cardiometabolic diseases

Metabolic syndrome Type 2 diabetes Hypertension Low HDL


OR (95% CI), P value OR (95% CI), P value OR (95% CI), P value OR (95% CI), P value

Psoriasis severity (unadjusted)


Mild disease 0.98 (0.46, 2.11), 0.97 4.70 (1.29, 17.2), 0.02 2.08 (0.97, 4.45), 0.06 0.73 (0.28, 1.90), 0.52
Severe disease 3.75 (1.90, 7.39), 0.0001 10.6 (3.38, 33.4), <0.0001 2.93 (1.46, 5.89), 0.002 2.07 (1.01, 4.23) 0.04
Psoriasis severity (adjusted)a
Mild disease 0.49 (0.16, 1.49), 0.20 3.27 (0.72, 14.9), 0.12 1.39 (0.50, 3.85), 0.53 0.67 (0.22, 2.05), 0.48
Severe disease 4.42 (172, 11 4), 0.002 11.3 (3.07, 41.3), 0.0002 2.48 (0.97, 6.32), 0.05 1.57 (0.63, 3.90), 0.32

OR, odds ratio; HDL, high-density lipoprotein.


a
Adjusted for age, body mass index, hsCRP, smoking, education, and socioeconomic status; P values relative to the reference group (non-
psoriatic).

Table 3 Logistic regression model showing risk factors for Previous studies have observed a higher prevalence of
psoriasis chronic kidney disease3 and lower vitamin D levels9 in psoriasis,
but this was not evident in the present study. However, as in
Dependent Independent Odds ratio (95% other studies, we found associations between lower education34
variable variables CI) P value and smoking with psoriasis.35
Although not the primary focus of the study, a disproportion-
Psoriasis Smoking 3.87 (1.97, 7.63) <0.0001
Level of education 0.23 (0.11, 0.48) <0.0001 ately high number of patients were of South Asian Indian or
hsCRP 1.05 (1.00, 1.10) 0.029 mixed ancestry and relatively few black African patients. This
is against a background of the majority of patients attending
hsCRP, highly sensitive quantification of C-reactive protein. state-run services being Black Africans. These findings mirror
Data shown is from a multivariable logistic regression model in those of an earlier study performed at the same dermatology
which backward, stepwise removal of nonsignificant variables (age,
clinics36 and may reflect ethnic differences in genetic risk for
waist circumference, hip circumference) was performed to yield the
final model shown above. psoriasis.
Some of the limitations of the study are the cross-sectional
design, the relatively small sample size, and that patients had
study on psoriasis and CMD concluded that psoriasis conferred already been initiated on systemic therapy at the time of recruit-
an independent risk for myocardial infarction with the risk being ment into the study. In addition, patients were recruited from
greatest in severe psoriasis.19 Subsequent studies have demon- public hospitals, and these findings may therefore not be gener-
strated similar relationships in terms of CVD,32 T2D,7 and alizable to all South African patients.
hypertension.6 Subgroup analysis in the present study showed In this study of mainly indigent non-Caucasian South Afri-
the increased risk of MetS and hypertension was exclusively in cans, the burden of MetS and its components was increased in
the severe psoriasis subgroup. Of note, we observed a very psoriasis as was the Framingham CVD risk score. Moreover,
strong association between T2D and severe psoriasis (OR the risk of these CMDs is greater in severe psoriasis, support-
[95% CIs]: 11.3 [3.07, 41.3]) which far exceeds the pooled risk ing the notion of a ‘psoriatic march’ and an etiological link
documented in a previous meta-analysis (1.97 [1.48–2.62]).7 between the severity of chronic inflammation of psoriasis and
The serum lipid levels for the psoriasis and control groups the burden of MetS. These findings therefore highlight the need
were similar for total cholesterol, LDL-C and Lp(a), HDL-C, and for all psoriatic patients, especially those with severe psoriasis,
triglycerides after adjusting for confounders. A previous study to be screened for CMDs. Our study also suggests that public
has shown higher total cholesterol levels in psoriasis but, similar health initiatives for reducing obesity and smoking could have a
to our findings, did not demonstrate any difference in LDL-C or positive effect on the severity of psoriasis.
Lp(a) between the psoriasis patients and controls.33
The pathophysiological mechanism linking psoriasis and
Acknowledgments
CMD is not entirely understood, but there is some evidence in
psoriasis, and in other chronic inflammatory disorders such as The authors would like to thank the study participants for taking
rheumatoid arthritis, that the cytokine-driven pro-inflammatory part in this investigation, and the routine section of the Depart-
systemic state contributes to increased risk of atherosclerosis ment of Chemical Pathology, NHLS, at the Charlotte Maxeke
and CMD.15 The significantly higher hsCRP levels in psoriasis Johannesburg Academic Hospital for performing the blood anal-
in the present study are noteworthy in this respect. yses.

ª 2018 The International Society of Dermatology International Journal of Dermatology 2018


6 Report Metabolic syndrome and psoriasis in South Africa Goolam Mahyoodeen et al.

Danish nationwide cohort study. J Intern Med 2011; 270: 147–


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