Psoriatic arthritis (PsA) is one of the most common forms of spondyloarthritis in the world . It is characterized by the presence of arthritis, dactylitis, enthesitis, and skin psoriasis (PsO) . The prevalence of psoriatic disease is reported to be 3.15% in the United States . Very often, it progresses rapidly to permanent joint destruction, leading to functional impairment and deteriorated quality of life in patients . With the launch of new biologic agents for psoriatic diseases in the past few years, the awareness among physicians and the general public of this nasty condition is increasing, which has resulted in an overall increase in the number of diagnosed cases of psoriatic disease [4,5]. However, there is little updated epidemiological information on PsA in Hong Kong [1,3]. The majority of local data is based on a study of 127 Chinese PsA patients conducted over a decade ago in which the sample size was relatively small [1,3]. Thus, more PsA data is definitely needed.
Psoriatic patients are well known to be at an elevated risk of developing other health conditions or comorbidities, including uveitis, inflammatory bowel disease (IBD), hypertension and diabetes mellitus (DM) [6,7,8,9]. However, data about these conditions is sparse in our geography. In recent years, metabolic syndrome (MetS) was found to be an emerging prevalent comorbidity in psoriatic patients [10,11]. MetS was considered as a primary cause and a strong predictor of subclinical atherosclerosis, leading to fatal cardiovascular events in later life [10,11]. Mok et al. demonstrated that 38% of 109 PsA patients in Hong Kong suffer from MetS. Thus the incidence of MetS was significantly higher than the general population and also more common than other arthropathies including rheumatoid arthritis and ankylosing spondylitis . Multiple research studies throughout the world also consistently found high prevalence of MetS in patients with PsA, ranging from 25% in Japan to 40% in the United States [11,12]. However, the worldwide information about its risk factors was inconsistent and limited. Some investigators suggested MetS was closely related with skin severity, while others explained it was more connected to disease duration [13,14].
As the features of PsA are attributed to ethnicity, extrapolating data from other foreign studies may not be appropriate when analyzing the condition of ethnic Chinese . The primary objective of this study was to describe their demographics and relevant clinical parameters. The secondary objective was to evaluate the prevalence of various comorbidities in PsA and to explore their associated factors, with particular emphasis on MetS [6,7,8,9,10,11]. Through our study, we hope to gain a better understanding of the current status of Hong Kong Chinese PsA patients.
This was a cross-sectional observational study. The protocol was reviewed and approved by Kowloon East Cluster (KEC) Clinical Research Ethics Committee. The primary aim of this study was to describe the clinical characteristics of PsA patients in public hospitals in Hong Kong. The secondary aim was to evaluate the prevalence and the associated factors of MetS among them.
From June 2016 to January 2018, patients of Chinese ethnicity with PsA, aged 18 years or older, attending rheumatology clinics of Tseung Kwan O Hospital (TKOH) or United Christian Hospital (UCH) in Hong Kong were consecutively recruited for this study after obtaining their written consent. All participants fulfilled the Classification Criteria for Psoriatic Arthritis (CASPAR) .
Demographic and disease-related parameters including age, sex, body mass index (BMI), abdominal circumference, disease onset and duration and family history were recorded. PsA disease activity including (1) tender (68) and swollen joint count (66), (2) tender and chronic dactylitis count (0–20), (3) Leeds Enthesitis Index (LEI), (4) Psoriasis Area and Severity Index (PASI), (5) C-reactive protein (CRP) and (7) erythrocyte sedimentation rate (ESR) were measured, in all participants [12,17,18]. Positive family history was defined as those with affected first-degree relatives. Tender dactylitis was defined as diffuse swelling of digit with pain, while chronic or ‘cold’ dactylitis was defined as those without pain [14,17,18].
PsA was categorized into five subtypes: (1) oligoarthropathy (involving less than five joints), (2) polyarthropathy (involving five or more joints), (3) predominant distal interphalangeal joints disease, (4) predominant axial disease and (5) arthritis mutilans. This categorization was based on the examination by physicians and the symptoms reported by patients [1,16].
Comorbid conditions such as uveitis, IBD, diabetes mellitus (DM), hypertension and MetS were also recorded [4,5]. Besides ESR, CRP and human leukocyte antigen (HLA) B27, a blood test to ascertain fasting plasma glucose, triglycerides and high-density lipoprotein (HDL) cholesterol was included to identify MetS [19,20].
MetS as defined by the International Diabetes Federation (IDF) criteria for Asians includes central obesity plus any two of the following four factors: (1) high triglycerides (>= 1.7 mmol/L) or on any lipid-lowering agent, (2) low HDL cholesterol (<1.03 mmol/L in males and <1.29 mmol/L in females) or on any lipid-lowering agent, (3) raised blood pressure (BP) with systolic BP >=130 mm Hg or diastolic BP >=85 mm Hg or on any anti-hypertensive agent and (4) raised fasting plasma glucose (>= 5.6 mmol/L) or current diagnosis of type 2 DM [19,20]. Central obesity was defined as the abdominal circumference being >= 80 cm in females and 90 cm in males [19,20].
2.1 Statistical Analysis
Data obtained was analyzed by using the Statistical Package for the Social Sciences (SPSS) 17.0 for Mac (Chicago, IL, US). All clinical and related parameters were expressed as percentages and mean ± standard deviation (SD) or median with interquartile range.
Potential factors associated with MetS were investigated by comparing those with and without MetS. Univariate analysis was performed using the Student t-test or Mann-Whitney U test for continuous variables as appropriate, and chi-square test for categorical variables. Variables with a p-value of < 0.1 from univariate analysis were fed into a subsequent logistic regression model to determine the associated factors of MetS. Statistical significance was defined as a p-value of less than 0.05 in a two-tailed test.
3.1 Patients’ characteristics
A total of 210 PsA patients attended the TKOH and UCH Rheumatology clinic from June 2016 to January 2018, and nine of them refused to participate the study. A final number of 201 eligible patients were recruited. Out of them, 77 were female and 124 were male, with a mean age of 52.4 ± 12.2 years. The mean BMI was 24.8 ± 4.1 kg/m2, and the mean abdominal circumference was 92.2 ± 11.0 cm for males and 85.6 ± 11.5 cm for females, respectively. The mean age of onset of PsO and PsA was 36.6 ± 14.2 and 44.5 ± 12.6 years, respectively. At the time of investigation, the mean disease duration of PsO and PsA was 15.7 ± 11.2 and 8.0 ±-7.4 years, respectively. Positive family history of PsO and PsA was present in 14.4% and 2% of the patients, respectively.
The majority of the patients (139/201) reported PsO preceding arthritis, while 44 of them (21.9%) reported simultaneous occurrence of PsO and arthritis. The rest (18/201) suffered from arthritis before skin lesions were noted. Skin psoriasis was reported in 83.6% of the patients (168/201), with the median PASI score of 2.8 (1.2, 6.4). Thirty-four of the patients (20.2%) had severe skin condition, with a PASI score > 10.
The median detected tender joint count (68) was 1 (0, 2) and the swollen joint count (66) was 0 (0, 3) at the time of survey. The median ESR level was 23 (11.5, 46) mm/h and median CRP level was 3.6 (3.1, 10.6) mg/L. Fourteen (9.6%) of the 157 PsA patients carried the HLA-B27 gene.
Both tender enthesitis and tender dactylitis were uncommon in the PsA participants at the time of the survey, with a prevalence of 10.5% (21/201) and 4.5% (9/201), respectively. Among those with tender enthesitis and tender dactylitis, the median LEI was 1 (1, 2) and median tender dactylitis count was 2 (1, 2.5). Sixty-five of the patients (32.3%) had chronic or ‘cold’ dactylitis with a median count of 3 (2, 4).
Regarding the arthritis subtypes, 81 (40.3%) were classified as belonging to the oligoarthropathy group, followed by polyarthropathy group (28.4%), predominant axial joint disease (18.4%), predominant distal interphalangeal joint disease (11.4%), and arthritis multilans (1.5%).
3.2 Comorbid conditions
None of the PsA patients had coexisting IBD, while 9 patients (4.5%) reported history of uveitis. Among the participating patients, 129 (64.2%) had central obesity, of which 71 were males and 58 were females. Of the patients, 37 (18.4%) and 66 (32.8%) had background history of DM and hypertension, respectively.
Excluding those with pre-existing DM, 22.9% (46/201) had raised fasting plasma glucose (>= 5.6 mmol/L). Finally, 72 patients (35.8%) were found to have MetS, of which 46 were males and 26 were females. Table 1 summarizes the clinical characteristics and comorbidities of all PsA patients.
Demographics and characteristics of PsA patients (n=201).
|Number (%)||Mean (+/- SD)|
|Male / Female ratio||124 / 77 (61.7 / 38.3)|
|Age (years)||52.4 +/- 12.2|
|Body mass index, BMI (kg/m2)||24.8 +/- 4.1|
|Age onset of PsO (years)||36.6 +/- 14.2|
|Duration of PsO (years)||15.7 +/- 11.2|
|Age onset of PsA (years)||44.5 +/- 12.6|
|Duration of PsA (years)||8.0 +/- 7.4|
|Abdominal circumference (cm), males||92.2 +/- 11.0|
|Abdominal circumference (cm), females||85.6 +/- 11.5|
|Positive family history of PsO||29 (14.4)|
|Positive family history of PsA||4 (2.0)|
|HLA-B27, n=157||14 (9.6)|
|Swollen joint count (0-66), median||1 (0, 2)|
|Tender joint count (0-68), median||0 (0, 3)|
|Patients with tender dactylitis||9 (4.5)|
|Tender dactylitis (0-20), median, n=9||2 (1, 2.5)|
|Patients with cold dactylitis||65 (32.3)|
|Cold dactylitis count (0-20), median, n=65||3 (2, 4)|
|Patients with enthesitis||21 (10.5)|
|Leeds enthesitis index (0-6), median, n=21||1 (1, 2)|
|Positive skin condition||168 (83.6)|
|PASI score (0-72), median, n=168||2.8 (1.2, 6.4)|
|Severe skin condition (PASI>10), n=168||34 (20.2)|
|ESR (mm/hr), median||23 (11.5, 46)|
|CRP (mg/L), median||3.6 (3.1, 10.6)|
|Oligoarticular (< 5 joints)||81 (40.3)|
|Polyarticular (>= 5 joints)||57 (28.4)|
|Predominant axial||37 (18.4)|
|Predominant distal interphalangeal joints||23 (11.4)|
|Arthritis multilans||3 (1.5)|
|Central obesity||129 (64.2)|
|Diabetes mellitus||37 (18.4)|
|Glucose intolerance||46 (22.9)|
|Metabolic syndrome||72 (35.8)|
|Inflammatory bowel disease||0|
3.3 Association with metabolic syndrome
In univariate analysis level, (1) age onset of PsA, (2) PsA disease duration, (3) PsO disease duration and (4) tender joint count were found to be closely associated with MetS. Table 2 summarizes the univariate analysis of associated factors for MetS in PsA.
Univariate analysis of PsA patients with and without metabolic syndrome (MetS).
|Parameter||Patients with MetS||Patients without MetS||P value|
|N= 72||N = 129|
|Male, No. (%)||46 (63.9)||78 (60.4)|
|Female, No. (%)||26 (36.1)||51 (39.6)|
|Age onset of PsO, mean +/- SD||35.7 +/- 13.8||38.3 +/- 14.7||0.22|
|Duration of PsO, mean +/- SD||18.0 +/- 12.2||14.5 +/- 10.4||0.03|
|Age onset of PsA, mean +/- SD||46.5 +/- 12.2||43.4 +/- 12.7||0.09|
|Duration of PsA, mean +/- SD||9.8 +/- 8.4||7.0 +/- 6.7||0.01|
|Swollen joint-count (0-66), median||1 (0, 4)||0 (0, 2)||0.21|
|Tender joint-count (0-68), median||1 (0, 3)||0.5 (0, 2)||0.09|
|Leeds Enthesitis Index (0-6), median||0 (0, 0)||0 (0, 0)||0.22|
|Acute dactylitis-count (0-20), median||0 (0, 0)||0 (0, 0)||0.73|
|Chronic dactylitis-count (0-20), median||0 (0, 2)||0 (0, 2)||0.15|
|PASI score (0-72), median||1.9 (0.2, 5.7)||2.1 (0.4, 5.3)||0.93|
|Severe skin condition (PASI >10), No. (%)||15 (21.1)||19 (14.6)||0.24|
|ESR (mm/hr), median||24 (15, 48)||23 (10, 40)||0.16|
|CRP (mg/L), median||3 (44, 98)||3.5 (3.1, 11)||0.81|
Subsequent logistic regression model identified that both age of onset and disease duration of PsA were significantly associated with MetS, with a p-value of 0.02 and 0.018, respectively. Older age of onset (46.5 ± 12.2 vs 43.4 ± 12.7 years) or longer disease duration (9.8 ± 8.4 vs 7.0 ± 6.7 years) of PsA increased the likelihood of developing MetS. No associations with MetS were found with ESR or CRP levels, PASI, dactylitis count, enthesitis index, swollen joint count, age onset of PsO and severe skin status.
The present study supports the widely held belief that PsA is an extremely heterogeneous disease, with variable age of onset, family history, arthritis pattern, genetic linkage and extra-articular manifestations, i.e. uveitis and IBD.
Our collected data shows that PsO lesions could start at a wide range of ages from 8 to 79 years. For the age of onset of PsA, it demonstrated a unimodal distribution with a peak at 50 years (figure 1). However, the temporal relationship between PsO and PsA was rather unpredictable, varying widely from -16 to 36 years. The majority of arthritis manifested in the first few years after skin lesions, with a median of 5 years (0, 14). Nearly a quarter of the patients (22%) had cutaneous and joint manifestations simultaneously, and only a minority (9%) had arthritis before skin disease. This may have led to difficult and delayed diagnosis of PsA. Generally, the collected information in our study was similar to Western patient data [21,22]. Figure 2 shows the time interval between PsO and arthritis in all the PsA patients.
Although no gender difference in PsA has been suggested, our collected data showed that males were more commonly affected than females (1.6:1) [1,22]. In fact, male predominance was also demonstrated in other Asian countries, such as Thailand, Korea and Japan [23,24].
Discrepancy from Western data could be attributed to a different sample size and ethnicity. More trials are needed to verify the phenomenon of male predominance in Asians.
Both oligoarticular and polyarticular arthritis remained the most common subtypes. Their prevalence depended on the time course of disease when the patients were examined [1,16]. Oligoarticular arthritis may progress to polyarticular involvement or multilans type if left untreated. With advances in effective therapy and treat-to-target approaches, progression to arthritis multilans was minimal. Tender dactylitis was uncommon (4.5%), but chronic or ‘cold’ dactylitis was noted in 32% of the patients. This finding indicated that the treatment of acute digital inflammation was not as prompt as expected [1,18]. Educating and increasing awareness among general practitioners and the general public about this typical sign of PsA may help to reduce its progression to chronic deformity.
The underlying cause of PsA is believed to be an interplay of multiple elements, particularly genetic factors . The PSOLAR study of 12,000 skin psoriasis patients in North and Latin America found that 45.5% and 10.3% of them had a positive family history of PsO and PsA, respectively . However, the role of genetic factors seemed to be less strong in Asians [23,26,27,28]. Positive family history of PsO was found in approximately 15% of our patients, probably due to less prevalent HLA-B27 or other genetic predispositions in Hong Kong and Asia [20,26,27,28]. A recent Japanese trial by Tanaka et al. highlighted an even smaller percentage (4%) of PsA cohorts with a family history of PsO . To date, there is no data about the frequency of HLA-B27 in the local PsA population. Due to financial constraints, only 78% of the patients (157/201) in our cohort had their HLA-B27 status checked. Of these, 9.6% carried the gene, which is similar to data reported in mainland China, which was 2–9% . In Caucasians, HLA-B27 was reported to be present in more than 25% of patients with PsA[18,23]. The relatively low HLA-B27 distribution in the Chinese PsA population could further explain its weak association with uveitis (4.5%) in our cohort compared with others [22,27,28]. Furthermore, uveitis was reported to be more common in axial spondyloarthritis patients, and only 18.4% of our PsA participants were reported to have that condition . Thus, the total reported uveitis was expected to be low. None of our cohorts reported IBD. This could be explained by a low HLA-B27 prevalence, or alternatively, they could have subclinical or asymptomatic intestinal inflammation .
In the current study, PsA was found to be notably associated with DM, hypertension and MetS. A prospective study of 1,065 Canadian PsA patients from 1978 to 2014 found an increased risk of DM in PsA (43% and higher) when compared to the general population, particularly in those with active disease (higher tender joint counts and PASI) and high BMI . Some researchers suggested that PsO triggers generalized body inflammation, which enhances the release of insulin-like growth factor (IGF-1), causing diabetes, while others believe vice versa . A 2013 meta-analysis highlighted that PsA patients were prone to developing hypertension, with an odds ratio of 2.07; 95% CI 1.41–3.04 . Furthermore, they tended to have difficult-to-control blood pressure and more likely to be treated with multiple antihypertensive agents . Based on this and other collected data, regular screening for diabetes and hypertension in patients with PsA should always be encouraged.
MetS is composed of a spectrum of risk factors, including central obesity, dyslipidaemia, hypertension and glucose intolerance [19,20]. Ample evidence suggested that MetS was highly linked with psoriatic conditions, irrespective of ethnicities and dietary habits [10,11,12]. However, the precise associative mechanism between MetS and psoriatic disease is unknown. Multiple cytokines including tumor necrosis factor (TNF) alpha, interleukin (IL) 6, 17 and 23, IGF-1 and adipokines (leptin, adiponectin and resistin) have been proposed to play a pivotal role [30,31]. Proinflammatory cytokines in PsO or PsA may trigger hypothalamic-pituitary axis imbalance and result in hypertension, DM and central obesity [30,31]. Vice versa, the abundance of adipokines in fatty tissue in overweight patients can stimulate the systemic inflammatory process, causing skin inflammation and arthritis [30,31].
Till now, only a few studies have investigated the risk factors of MetS in psoriatic conditions[19,20]. A 2011 population-based study in United Kingdom demonstrated that the development of MetS increased with PsO skin severity in a dose–response manner . The odds of having MetS in mild and severe PsO (PASI >10) was 1.22 and 1.98, respectively . Studies by Parodi et al. in 2014 and Itani et al. in 2016 showed a similar outcome; however, musculoskeletal inflammation load was not considered in all of them [19,20].
In 2013, Sharma et al. reported that MetS was particularly prevalent in those PsA patients with a longer duration of skin condition and active joint disease as can be gleaned from a high Bath Ankylosing Spondylitis Activity Index (BASDAI), but their sample size was relatively small (n=100) . In 2014, Haroon et al. reviewed 283 PsA patients and found that MetS was present in 44% of them . MetS was significantly associated with severe PsA condition, with odds ratio of 4.5; however, their definition of severe PsA disease was not universally applied . Our results identified that both age of onset or disease duration of PsA were strongly associated with MetS, but not with arthritis, skin conditions and inflammatory markers. It is a pity that no study using similar methodology exists for comparison [13,14,19,20].
We further identified that psoriatic patient with older age of onset of arthritis (46.5 ± 12.2 years) or longer arthritis duration (9.8 ± 8.4 years) were more vulnerable to developing MetS. Currently, there is no consensus in screening for this cardio-metabolic risk; some researchers suggested evaluating for the risk every 5 years, or every 2 years if a positive family history of cardiovascular events exists . In view of our collected data, MetS screening should be performed regularly and more frequent in case of those patients in older age and with a longer duration of arthritis.
There were some limitations in this study. First, the occurrence of certain clinical characteristics of PsA, such as the arthritis pattern and skin extent, depended on the time point of the disease when the patient was examined. The prevalence of the comorbid conditions may be underestimated in the study, since they can develop in the later life of psoriatic patients. Furthermore, there was a recall bias in reporting the disease onset of PsO and PsA, which is a common issue in cross-sectional studies.
Second, the study was confined to two regional hospitals. The collected data could not reflect the general condition of PsA patients across Hong Kong. Third, the factors including the arthritis pattern (particularly those with axial spondyloarthritis), disease remission status and the use of different medications (e.g. DMARDS, steroids and biologics) were not well addressed in investigating the associating factors of MetS . They all can definitely affect and relate to the systemic inflammation in psoriatic patients, in whom metabolic balance may be affected.
Finally, most of our recruited PsA participants were under treatment and had low disease activity. As the occurrence of MetS is closely related to systemic inflammation [6,19,20], this may have affected the detection of MetS among our patients. Hopefully, a larger scale prospective research study will be conducted in the future to understand more about this commonly encountered arthropathy and its comorbidities.
PsA is one of the most prevalent arthropathies in Hong Kong, but information about its clinical features and comorbidities is relatively insufficient. PsA is a highly heterogeneous disease involving different body organs including peripheral and axial joints, skin, entheses, eyes and bowels.
Furthermore, it is also extensively associated with other comorbidities, especially metabolic syndrome. Regular screening of PsA-related comorbidities is highly recommended in view of their high prevalence and mortality. Hopefully, a larger scale PsA epidemiological study in Hong Kong can be conducted in the near future to add to our knowledge of its clinical characteristics.
The authors would like to express appreciation to all the participants for their contribution and time to the project. They would like to thank TKOH and UCH rheumatology specialty nurses, Ms Cheryl Cheng, Ms Cheung and Ms Lee for their continued support to this time-consuming task. Moreover, the authors also thank Dr. Cynthia Chan and Dr. Janice Wong for their invaluable advice on editing and proofreading.
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