|Year : 2018 | Volume
| Issue : 1 | Page : 29-36
The relationship between platelet volume and risk of atherosclerosis in patients with psoriasis
Enas A.M. Mahrous
Department of Dermatology and Andrology, Shibin El-Kom Teaching Hospital, Menoufia Governorate, Egypt
|Date of Submission||07-Sep-2017|
|Date of Acceptance||12-Nov-2017|
|Date of Web Publication||12-Mar-2018|
Enas A.M. Mahrous
Shibin El-Kom, Menoufia Governorate, 4327
Source of Support: None, Conflict of Interest: None
Objective The aim of this research was to evaluate the relation between the mean platelet volume (MPV) and clinical aspects (onset, duration, and severity) in patients with psoriasis. In addition, the purpose was to evaluate the possible risk of atherosclerosis in these patients.
Background Psoriasis is an inflammatory skin disease affecting 2–4% of the world population. However, studies in developing countries have reported higher prevalence rates of ∼4.6% on an average. MPV is an indicator of platelet activation, and it is a newly emerging risk factor for patients with atherothrombotic psoriasis.
Patients and methods A case–control study was conducted on 40 patients with variable degrees of psoriasis severity (cases) and they were compared with 20 matched healthy participants (controls). All participants were selected from dermatology inpatients and outpatient clinics of the Menoufia University Hospital in the period from September 2015 to March 2016. Full detailed history, routine laboratory investigations, clinical features, Psoriasis Area and the Severity Index (PASI) scores, and carotid intima-media thickness (CIMT) and nonalcoholic fatty liver disease (NAFLD) values were taken for each participant (cases and controls).
Results There were statistically no significant differences between patients with psoriasis and control groups regarding age, sex, BMI, total cholesterol, and triglycerides (P>0.05%, for all), whereas patients with psoriasis had significantly higher systolic and diastolic blood pressure, fasting plasma glucose, mean MPV and CIMT values, and frequency of ultrasound-diagnosed NAFLD than the control group. In addition, BMI, duration of illness, PASI, and mean values of MPV were significantly (P=0.5) elevated in patients with psoriasis with atherosclerosis than patients with psoriasis without atherosclerosis. Moreover, MPV level was correlated positively with age, BMI, duration of psoriasis, PASI score, and CIMT in the atherosclerotic psoriatic case group. Moreover, CIMT and PASI score were correlated positively with BMI, duration of illness, MPV, systolic blood pressure, diastolic blood pressure, glycated hemoglobin, and NAFLD in the psoriasis patient group, whereas CIMT was significantly correlated positively with PASI score.
Conclusion Psoriasis is associated with high MPV. So, MPV is a good indicator of psoriasis severity. Thus, MPV is a good positive test for early detection of premature atherosclerosis in patients with psoriasis. This study may confirm previous observation indicating increased platelet activation in psoriasis. Increased platelet activity could contribute toward increasing the atherosclerotic risk in patients with psoriasis.
Keywords: atherosclerosis, patients with psoriasis, platelet volume, Psoriasis Area and the Severity Index score
|How to cite this article:|
Mahrous EA. The relationship between platelet volume and risk of atherosclerosis in patients with psoriasis. Egypt J Dermatol Venerol 2018;38:29-36
|How to cite this URL:|
Mahrous EA. The relationship between platelet volume and risk of atherosclerosis in patients with psoriasis. Egypt J Dermatol Venerol [serial online] 2018 [cited 2019 Sep 16];38:29-36. Available from: http://www.ejdv.eg.net/text.asp?2018/38/1/29/227097
| Introduction|| |
Psoriasis (PS) is a common chronic, relapsing, immune-mediated disease involving the skin and joints of genetically predisposed individuals . It is a chronic inflammatory skin disease characterized by relapsing thick scaling plaques. PS affects 2–3% of the worldwide population, with prevalence varying according to race and geographic location .
The prevalence of PS ranged from 0.91 to 8.5% in the adult population. Among patients with PS, ∼6–42% are Caucasians. Psoriatic arthritis is defined as inflammatory arthritis associated with PS . PS not only negatively affects the quality of life but also increases the risk of cardiovascular events and cardiovascular mortality . Therefore, early detection of subclinical atherosclerosis in patients with PS would help to reduce cardiovascular morbidity and mortality .
Disease-specific risk factors are a direct consequence of PS inflammation and include hyperhomocysteinemia, elevated C-reactive protein, elevated blood inflammatory cytokines, and platelet hyperactivity. Platelet activation has been suggested to take part in the pathophysiology of PS . However, the exact mechanisms of these associations remain unclear. The mean platelet volume (MPV) is an indicator of platelet function and activation, which is a determinant of atherosclerosis. Elevation of MPV values has been shown to be an independent risk factor for acute myocardial infarction and other vascular conditions, such as renal artery stenosis, hyperlipidemia, and diabetes mellitus .
Chu et al.  found that increased platelet activity is associated with increased platelet volume. Large platelets characterized by a high MPV and containing more dense granules are metabolically and enzymatically more active than smaller ones . On the basis of this observation, elevated MPV is accepted as an indicator of platelet activation and indirectly as a marker of increased cardiovascular risk . MPV levels were significantly higher in patients with PS than controls and showed a positive correlation with Psoriasis Area and Severity Index (PASI) score . However, these results were denied by other investigators .
Endothelial function and carotid intima-media thickness (CIMT) have been suggested to be an important marker of subclinical atherosclerosis. Most studies have shown evidence of subclinical atherosclerosis in patients with PS as indicated by increased CIMT or impaired flow-mediated dilation than the matched controls. However, conflicting results regarding the relationship between PS and subclinical atherosclerosis risk still exists .
In addition, several studies indicate that MPV, the most simple parameter to estimate platelet activation, is higher in association with overall vascular mortality, including myocardial infarction . Larger and hyperactive platelets accelerate the formation of an intracoronary thrombus and therefore represent a major risk factor for atherothrombosis .
Therefore, the aim of this research was to evaluate the relation between the MPV and clinical aspects (onset, duration, and severity) in patients with PS, as well as the possible risk of atherosclerosis in these patients.
| Patients and methods|| |
A case–control study was conducted on 40 patients with variable degrees of PS severity (cases), and they were compared with 20 matched healthy (controls). All participants were selected from dermatology inpatients and outpatient clinics of the Menoufia University Hospital in the period from September 2015 to March 2016.
A signed written informed consent after explaining the aim of the study and before the beginning of the study was obtained from every participant. The consent form was developed according to the standard of Quality Improvement System in Ministry of Health in Egypt and modified according to the ethics committee in Faculty of Medicine, Menoufia University.
The inclusion criteria were patients with PS of both sexes, 19 years or older, and did not receive any topical or systemic treatment for PS before the study.
The exclusion criteria were any patients who had one or more of the immunoinflammatory diseases, uncontrolled systemic infection, and risk factors of atherosclerosis such as hypertension, history of cardiac disease, and diabetes.
All individuals were subjected to the following:
- Complete history taking, for example, name, age, sex, and family history of PS or any autoimmune disease.
- Clinical examination.
- Laboratory investigations.
- General examination including the following:
- BMI (Jin et al. ): underweight less than 18.5 kg/m2, normal (18.5–24.99 kg/m2), overweight (25–29.99 kg/m2), obese more than or equal to 30 kg/m2, and morbid obesity more than or equal to 35 kg/m2.
- Evaluation of vital signs, including blood pressure, pulse, and respiratory rate.
- Full dermatological examination: was done, including skin, hair, and nails. The severity of PS is assessed using PASI.
PASI score: The body is divided into four sections [head (H) (10% of a person’s skin, arms (A) (20%), trunk (T) (30%), legs (L) (40%)]. Each of these areas is scored by itself, and then the four scores are combined into the final PASI . For each section, the percent of the area of skin involved is estimated and then transformed into a grade from 0 to 6:
- 0% of involved area, grade 0.
- <10% of involved area, grade 1.
- 10–29% of involved area, grade 2.
- 30–49% of involved area, grade 3.
- 50–69% of involved area, grade 4.
- 70–89% of involved area, grade 5.
- 90–100% of involved area, grade 6.
Within each area, the severity is estimated by three clinical signs: erythema (redness), induration (thickness), and desquamation (scaling). Severity parameters are measured on a scale of 0–4, from none to maximum. The sum of all three severity parameters is then calculated for each section of the skin, multiplied by the area score for the area of the respective section (0.1 for the head, 0.2 for upper extremities, 0.3 for trunk, and 0.4 for lower extremities).
PASI = 0.1 (Rh + Th + Sh)Ah + 0.2(Ru + Tu + Su)Au + 0.3(Rt + Tt + St)At + 0.4(Rl + Tl + Sl) × Al, where R is redness score of the plaque; T is thickness score of the plaque; S is scaleness score of plaques; and A is area of PS involvement score.
A PASI score below 7 was defined as mild, between 7 and 12 as moderate, and above 12 as the severe disease .
Routine laboratory investigations
Routine laboratory investigations was to exclude dyslipidemia and/or diabetes mellitus, including glycosylated hemoglobin (HbA1c) and lipid profile.
Complete blood count assessment
From each participant in the study, 2 ml of venous blood was withdrawn under complete aseptic condition from the cubital vein in the test tube containing 20 μl of EDTA for complete blood count. The analysis was done as soon as possible using Sysmex XN 1000 cell counter (Sysmex Corporation, Kobe, Japan) to detect MPV as a part of complete blood count item.
Both abdominal ultrasonography for evaluating nonalcoholic fatty liver disease (NAFLD) and carotid ultrasonography for evaluating CIMT were performed using B-mode ultrasonography (Philips Xario 200, Sysmex Corporation, Kobe, Japan).
Preparation: the following preparation was applied: dimly lit room, room temperature 22–25°C, and patient in the lying position. Examination was performed with the neck in the extended position, using ECG electrodes (control of heat cycles), standardized head-position to the right/left, minimum requirements of ultrasound transducer frequencies 5–15 MHz (better: 10-MHz linear ultrasound transducer), and appropriate depth of focus.
Refresh rate was more than or equal to 25 Hz (minimal compression). Gain was ∼60 dB.
Performance: sequential-based records after three to four heat cycles (longitudinal axis), Optimal image-adjustment: visualizing the double line pattern of the carotid artery (near and far wall of the common carotid artery).
Record of at least three fixed images (longitudinal axis) (optimal: vertical dipping ultrasound rays (the artery in horizontal focus). End-diastolic records of images/sequences were taken. The right and left CIMT was measured, the mean value of both was calculated, and then the result of estimated CIMT was interpreted as follows:
- The thickness of CIMT less than or equal to 8 mm was considered normal.
- The thickness of CIMT more than 8 mm was considered atherosclerotic.
Results were tabulated and statistically analyzed by using a personal computer using Microsoft Excel 2016 and SPSS, version 20 (SPSS Inc., Chicago, Illinois, USA). Statistical analysis was used as follows: descriptive statistic included percentage (%), mean, and SD, where analytical included χ2, t-test, Mann–Whitney test, and Pearson’s correlation coefficient (r). A value of P less than 0.05 was considered statistically significant.
| Results|| |
The current study was conducted on 40 patients with PS. Their mean age was 40.35±9.07 years, whereas the mean age of disease onset was 37.85±9.13 years. There were 30 (75.0%) males and 10 (25.0%) females. The mean value of their BMI was 29.11±6.17 kg/m2. In addition, 20 healthy volunteers were included in the study (control group), and their mean age of was 43.05±9.10 years. There were 13 (65.0%) males and seven (35.0%) females. The mean BMI was 28.76±6. 02 kg/m2 in the control group. There were statistically no significant differences between patients with PS and control groups regarding age, sex, and BMI (P>0.05%) ([Table 1]).
|Table 1 Demographic data and characteristic features of patients with psoriasis and control groups|
Click here to view
However, patients with PS had significantly higher systolic (127±7.13) and diastolic blood pressure (85±5.16), fasting plasma glucose (89±6.80), and HbA1c (5.9±0.50) as compared with controls (P<0.05). In contrast, no statistically significant difference (P≥0.05) was observed among the studied groups regarding total cholesterol (P=0.491) and triglycerides (P=0.673) ([Table 1]).
Results present in [Table 2] show that the mean value of MPV was significantly increased (P<0.001) in patients with PS as compared with controls (9.52±0.85 vs. 7.11±0.36 fl/ml). Moreover, high degrees of MPV predominated in patients with PS than control group (P=0.001) ([Table 2]).
|Table 2 Comparison between patients with psoriasis and control regarding mean and the degree of the mean platelet volume|
Click here to view
In addition, results present in [Table 3] show that patients with PS had significantly higher CIMT than the control group (0.82±0.15 vs. 0.61±0.1 mm; P<0.001). The frequency of ultrasound-diagnosed NAFLD in patients with PS was significantly higher than in the control group (57.5 vs. 35%, P<0.05). Moreover, the difference between the two groups in terms of moderate–severe NAFLD and the grade of NAFLD distribution was stronger (P<0.001) ([Table 3]).
According to estimated CIMT values, patients with PS (40 cases) were divided into patients with PS with atherosclerosis (27 patients with PS who have CIMT>0.08 mm) and those without atherosclerosis (13 patients with PS had CIMT≤0.08 mm). In addition, the current study revealed no significant differences (P>0.05, for all) among atherosclerotic and nonatherosclerotic groups of patients with PS regarding age and age of onset (years) ([Table 4]).
|Table 4 Comparison between atherosclerotic and nonatherosclerotic psoriatic cases regarding their personal and clinical data|
Click here to view
In contrast, BMI, duration of illness, PASI, and mean values of MPV were significant (P=0.5) elevated in PS atherosclerotic cases than nonatherosclerotic psoriatic cases (29.59±3.51, 8.20±3.00, 13.98±4.14, and 9.95±0.56, respectively, vs. 26.30±0.73, 6.17±1.44, 10.00±1.52, and 8.70±0.60, respectively), as well as severity of PS (elevated PASI score) (13.98±4.14 vs. 10.00±1.52) (P=0.025) and progressive disease (44.4 vs. 7.7%) (P=0.012) ([Table 4]).
In studying the association between an MPV and different variables in atherosclerotic and nonatherosclerotic PS cases, MPV levels were significant positively correlated with age (r=0.52, P=0.035), BMI (r=0.58, P=0.028), duration of PS (r=0.60, P=0.004), PASI score (r=0.83, P<0.001), and CIMT (r=0.79, P<0.001) in the atherosclerotic psoriatic case group. However, in the nonatherosclerotic psoriatic case group, MPV was significant positive correlated with the PASI score (r=0.68, P=0.003) only ([Table 5]).
|Table 5 The relation between an mean platelet volume and personal and clinical data of patients with psoriasis regarding atherosclerosis|
Click here to view
Results in [Table 6] indicated that CIMT and PASI score were significantly positive correlated with BMI (r=0.52 and 0.453, respectively), duration of illness (r=0.68 and 0.581, respectively), MPV (r=0.73 and 0.682, respectively), systolic blood pressure (r=0.45 and 0.348, respectively), diastolic blood pressure (r=0.414 and 0.471, respectively), HbA1c (r=0.593 and 0.700, respectively), and NAFLD (r=0.541 and 0.755, respectively), in the patients with PS group. Moreover, CIMT was significantly positively correlated with the PASI score (r=0.79, P<0.001).
|Table 6 The relation between carotid intima-media thickness and Psoriasis Area and the Severity Index score with personal and clinical data of patients with psoriasis|
Click here to view
| Discussion|| |
In the present study, the age of onset of PS in patients ranged between 19 and 67 years, spanning a broad range, with a mean value of 40.35±9.07 years. Similarly, Icen et al.  recorded in their study on 90 Italian patients with PS that the disease started at age in the ranged of 18 and 80 years, with a mean value of 43.2±17.0 years. However, this finding differs from the result of Tollefson et al. , who investigated 100 Turkish children with PS and observed that the mean age of PS started at age ranged between 4 and 18 years, with a mean of 20±4.4 years. This difference may be attributed to the fact that PS is a common disease, less common in children, and more common in adults, with prevalence rates showing a worldwide geographic variation, which probably reflects the fact that PS is a complex disease influenced by both genetic and environmental factors .
Mean value of BMI of our patients with PS was 29.11±6.17, which was nonsignificantly increased (P = 0.057) compared with control group (28.76±6.02). However, our atherosclerotic psoriatic cases showed significantly higher BMI (P=0.027) compared with nonatherosclerotic PS group, which confirmed the fact that elevated BMI is one of the important cardiovascular risk factors in patients with PS . In agreement with our results, Choon et al.  detected no association between PS and BMI, and Kimhi et al.  detected an association between atherosclerotic changes in patients with PS and BMI. However, Armstrong et al.  found a significant increase in BMI in their study of 120 American patients with PS than their matched controls. This difference may be because of the number or race of the student population in each study.
Several studies clearly reported the association between PS and diabetes ,,. In our study, we observed an increased HbA1c and fasting plasma glucose level in patients with PS compared with healthy controls. Furthermore, HbA1c was found to be an independent predictor of severity of PS; this finding of our study is different from those of previous studies. This is probably because HbA1c was significantly associated with the duration of disease, suggesting long-standing inflammation similar to that in patients with PS.
Moreover, in our study, serum triglycerides and total cholesterol were higher in the patient group, and these failed to reach a statistically significant difference. In contrast to many previous studies ,, there was no significant positive correlation between serum lipid parameters and severity of PS. In accordance with many previous studies, we observe that levels of systolic and diastolic blood pressure were significantly elevated in patients with PS compared with controls ,. Blood pressures are predictors of cardiovascular risk, and our findings agree with the notion of a long-term increase in risk of hypertension and late adverse cardiovascular events in these individuals ,.
In the present study, the mean MPV in PS patients was 9.52±0.85 fl/ml, which is significantly (P<0.001) higher than of control group (7.11±0.36 fl/ml). This result agreed with Conpolat et al. , who reported that the mean MPV levels in patients with PS (8.7±0.9 fl/ml) was significantly (P<0.01) elevated than that of control group (7.3±0.8 fl/ml). Moreover, Kim et al. , reported MPV level was significantly increased in patients with PS (9.92±0.73 fl/ml) compared with controls (9.724±0.59 fl/ml). However, Saleh et al.  revealed a nonsignificant increase in the MPV in patients with PS than their matched controls. This conflicting result may be because of small sample size in the study done by Saleh et al. , as their study was conducted on 25 patients with PS and 25 healthy controls.
Within the PS case group, elevated MPV mean value (9.52±0.85 fl/ml) was significantly positively correlated with the PASI score (r=0.83, P<0.001) denoting that severe forms of PS is associated with more increase in platelet activity. In agreement with our study, Conpolat et al.  and Kim et al.  reported a significant correlation between an MPV and PASI score in their evaluated patients with PS. In contrast, Saleh et al.  denied this correlation. This difference could be attributed to the difference in the number and the race of patients with PS in each study, in addition, the time at which each study was performed, as PS is more active in winter. Moreover, PS has periods of exacerbation and remission, with a variable PASI score along the time/overtime .
In studying the association between an MPV and other evaluated different variables in our PS patients, there were significant positive correlations between an MPV and age, BMI, duration of PS, and CIMT. The reported positive correlation between MPV levels and BMI in this study is supported by the result reported in the study by Shimodaira et al.  (r=0.06, P<0.05). In addition, Conpolat et al.  confirmed our result regarding the observed significant positive correlation between an MPV and duration of PS. In view of these findings, we can suggest that platelet reactivity, evaluated by High MPV, may have an active role not only in PS development but also in its outcome.
Ultrasonography data of the present study showed that the mean value of CIMT was 0.82±0.15 mm in patients with PS and 0.61±0.1 mm in the control group. A comparison between both revealed a highly significant difference (P<0.001), confirming that PS was associated with subclinical atherosclerosis ,. Furthermore, in a PS patient group, CIMT mean value was significantly correlated with age, BMI, duration of disease, and its severity, in addition to the evaluated MPV. The significant increase in CIMT mean value in patients with PS than controls and its significant positive correlations with studied parameters (age, BMI, duration of PS, PASI score, systolic and diastolic blood pressures, HbA1c, and NAFLD) were supported by several studies such as El-Mongy et al. , Enany et al. , and Elsheikh et al. .
In contrast, Youssef et al.  and Asha et al. , did not find any correlation of CIMT with PS duration or its severity. This was perhaps because of a quite young age group of their patients (25–45 and 31–40 years, respectively) and fluctuating course of the disease. Moreover, the atherosclerotic PS cases had significantly longer disease duration and severe and progressive form of PS than nonatherosclerotic cases. In addition to observing positive correlations between CIMT and age, duration of PS, PASI score, and BMI, we may conclude that elderly patients with PS with increased BMI and long-duration, severe, and progressive forms of PS are more prone to develop atherosclerosis than young patients with short-duration, stationary, and less severe form of the disease.
| Conclusion|| |
PS is associated with high MPV, so MPV is a good indicator of PS severity. Thus, MPV is a good positive test for early detection of premature atherosclerosis in patients with PS. This study may confirm previous observation indicating increased platelet activation in PS. Increased platelet activity could contribute to increasing the atherosclerotic risk in patients with PS.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Grozdev I, Korman N, Tsankov N. Psoriasis as a systemic disease. Clin Dermatol 2014; 32:343–350.
Lima XT, Minnillo R, Spencer JM. Psoriasis prevalence among the 2009 ADD National melanoma, Skin Cancer Screening Program participant. J Eur Acad Dermatol Venereol 2013; 27:680–685.
Goff KL, Karimkhani C, Boyers LN. The global burden of psoriasis skin disease. Br J Dermatol 2015; 172:1665–1668.
Horreau C, Pouplard C, Brenaut E. Cardiovascular morbidity and mortality in psoriasis and psoriatic arthritis: a systematic literature review. J Eur Acad Dermatol Venereol 2013; 27(Suppl 3):12–29.
Bauer M, Caviezel S, Teynor A. Carotid intima-media thickness as a biomarker of subclinical atherosclerosis. Swiss MED Wkly 2012; 142:w13705.
Gisondi P, Girolomoni G. Psoriasis and atherothrombotic diseases: disease-specific and non-disease-specific risk factors. Semin Thromb Hemost 2009; 35:313–324.
Kasperska-Zajac A, Brzoza Z, Rogala B. Platelet function in cutaneous diseases. Platelets 2008; 19:317–321.
Chu SG, Becker RC, Berger PB. Mean platelet volume as predictor of cardiovascular risk: a systematic review and meta-analysis. J Thromb Haemost 2010; 8:148–156.
Margetic S. Inflammation and hemostasis. Biochem Med (Zagreb) 2012; 22:49–62.
Markovic D, Carevic V, Bonacin D. Correlation between mean platelet volume and total risk of cardiovascular disease. J Am Coll Cardiol 2013; 40:418–423.
Kim DS, Jungsoo L, Sung HK. Mean platelet volume is elevated in patients with psoriasis vulgaris. Yonsei Med J 2015; 17:2315–2326.
Saleh HM, Attia EA, Onsy AM. Platelet activation: a link between psoriasis and subclinical atherosclerosis. Br J Dermatol 2013; 122:7665–7685.
Ruggiero D, Paolillo S, Ratta GD. Endothelial function as a marker of pre-clinical atherosclerosis: assessment techniques and clinical implications. Monaldi Arch Chest Dis 2013; 80:106–110.
Karoli R, Fatima J, Shukla V. A study of cardio-metabolic risk profile in patients with psoriasis. J Assoc Physicians India 2013; 150:798–803.
George S, Thomas P, Helmuth H. Mean platelet volume may represent a predictive parameter for overall vascular mortality and ischemic heart disease. J Arterioscler Thromb Vasc Biol 2011; 31:1215–1218.
Jin R, Grunkemeier GL, Furnary AP, Handy JR Jr. Is obesity a risk factor for mortality in coronary artery bypass surgery? Circulation 2008; 111:3359–3365.
VandeKerkhof PC, Schalkwijk J. Psoriasis. In: Bolognia JL, Jorizzo JL, Rapini RP, editors. Dermatology. 2nd ed. Spain: Mosby; 2008. pp. 115–148.
Schmitt J, Wozel G. The psoriasis area and severity index is the adequate criterion to define severity in chronic plaque-type psoriasis. Dermatology 2002; 210:194–199.
Icen M, Crowson CS, McEvoy MT. Trends in incidence of adult-onset psoriasis over three decades: a population-based study. J Am Acad Dermatol 2009; 60:394–415.
Tollefson MM, Crowson CS, McEvoy MT. Incidence of psoriasis in children: a population-based study. J Am Acad Dermatol 2010; 62:979–987.
Parisi R, Symmons DP, Griffiths CE. Identification and Management of Psoriasis and Associated Comorbidity (IMPACT) project team. Global epidemiology of psoriasis: a systematic review of incidence and prevalence. J Invest Dermatol 2013; 133:377–385.
Federman DG, Shelling M, Prodanovich S. Psoriasis: an opportunity to identify cardiovascular risk. Br J Dermatol 2009; 160:1–7.
Choon SE, Ngim CF, Premaa S, Tey KW, Nalini MN. Clinico-epidemiological profile, including body mass index of Malaysian children with psoriasis. Med J Malaysia 2016; 162:633–636.
Kimhi O, Caspi D, Bornstein NM. Prevalence and risk factors of atherosclerosis in patients with psoriatic arthritis. Semin Arthritis Rheum 2007; 36:203–209.
Armstrong AW, Harskamp TT, Armstrong EJ. The association between psoriasis and obesity a systemic review and meta-analysis, observational studies. Br J Dermatol 2012; 22:I61–174.
Brunner H, Cockcroft JR, Deanfield J. Endothelial function and dysfunction. Part II: association with cardiovascular risk factors and diseases. J Hypertens 2005; 23:233–246.
Neimann AL, Shin DB, Wang X, Dmochowska A. The prevalence of cardiovascular risk factors in patients with psoriasis. J Am Acad Dermatol 2006; 55:829–835.
Yudkin JS. Insulin resistance and the metabolic syndrome − or the pitfalls of epidemiology. Diabetologia 2007; 50:1576–1586.
El Asmi MA, Zidi W, Mebazaa A. Serum lipid level in Tunisian patients with psoriasis. Clin Lab 2014; 60:1043–1047.
Enany B, El Zohiery AK, Elhilaly R, Badr T. Carotid intima-media thickness and serum leptin in psoriasis. Herz 2012; 37:527–533.
Griffiths CE, Barker JN. Pathogenesis and clinical features of psoriasis. Lancet 2007; 370:263–271.
Armstrong AW, Voyles SV, Armstrong EJ, Fuller EN, Rutledge JC. Angiogenesis and oxidative stress: common mechanisms linking psoriasis with atherosclerosis. J Dermatol Sci 2011; 63:1–9.
Conpolat F, Akpinar H, Eskioglu F. Mean platelet volume in psoriasis and psoriatic arthritis. Clin Rheumatol 2010; 185:3412–3622.
Kisiel D, Krupnick AS, Gelman AE. Non-hematopoietic allograft cells directly activate CD8+ T cells and trigger acute rejection: an alternative mechanism of allorecognition. Nat Med 2016; 8:233–239.
Shimodaira M, Niwa T, Nakajima K, Kobayashi M, Hanyu N, Nakayama T. Correlation between mean platelet volume and fasting plasm glucose levels in prediabetic and normoglycemic individuals. Cardiovasc Diabetol 2013; 5:12–14.
Asha K, Suman B, Archana S, Aggarwal A. Association of carotid intima-media thickness with leptin and apolipoprotein B/apolipoprotein A-I ratio reveals imminent predictors of subclinical atherosclerosis in psoriasis patients. Acta Medica (Hradec Kralove) 2014; 57:21–27.
El-Mongy S, Fathy H, Abdelaziz A. Subclinical atherosclerosis in patients with chronic psoriasis: a potential association. J Eur Acad Dermatol Venereol 2010; 24:661–666.
Elsheikh RG, Amin TE, El-Ashmawy AA, El-Fttah Abdalla SIA. Evaluation of subclinical atherosclerosis in Egyptian psoriatic patients. J Saudi Heart Assoc 2014; 26:63–71.
Youssef SS, Hosny S, Bakr I. Susceptibility to atherosclerosis in patients with psoriasis and psoriatic arthritis as determined by increased carotid artery intima-media thickness. J Pan Arab League Dermatol 2009; 20:159–172.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]