Prevalence and Factors Associated with Cutaneous Manifestations of Type 2 Diabetes Mellitus
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ORIGINAL ARTICLE ISSN 2450–7458 Saadah Rasid , Leelavathi Muthupalaniappen , Adawiyah Jamil Pusat Perubatan Universiti Kebangsaan Malaysia, Kuala Lumpur, Malaysia Prevalence and factors associated with cutaneous manifestations of type 2 diabetes mellitus ABSTRACT 2.6 times the odds of developing SDWSAD (AOR: 2.646, Background. Type 2 diabetes mellitus (T2DM) is known 95% CI: 1.506–4.648 P = 0.001) and (AOR: 2.635, 95% to cause multiple systemic manifestations. However, CI: 1.107–6.268, P = 0.028) respectively. Those with there are limited studies describing cutaneous manifes- diabetic neuropathy and peripheral vascular disease tation among T2DM in Malaysia. The objective of this (PVD) had very high odds of developing SMDC such study was to determine the prevalence of cutaneous as diabetic foot and trophic ulcers (AOR: 23.259, 95% manifestation among T2DM patients, types of lesions CI: 1.191–454.2, P = 0.038) and (AOR: 102.36, 95% CI: and its associated factors. 4.013–2610, P = 0.005), respectively. Methods. A cross-sectional study was conducted Conclusion. The knowledge of these cutaneous among 271 T2DM patients at a primary care clinic in manifestations increases physician’s awareness and Kuala Lumpur. prompts early screening to reduce morbidity improve Results. More than one third (63.5%) of patients were quality of life. (Clin Diabetol 2020; 9; 6: 461–468) found to have cutaneous manifestations of T2DM. The most common manifestation was infections (34.7%) Key word: diabetes mellitus, skin manifestations, followed by Skin Diseases with Weak to Strong Associa- glycated hemoglobin A, prevalence tion with Diabetes (SDWSAD) (31.7%), Skin Manifesta- tion of Diabetic Complication (SMDC) (2.2%) and oth- Introduction ers cutaneous lesions (22.1%). Among the infections, South-East Asia accounts for more than 60% of the onychomycosis was the commonest type of infection world’s diabetes population [1]. The rapid rise in type 2 (27.7%) while diabetic dermopathy was the common- diabetes mellitus (T2DM) prevalence in Malaysia is est lesion of SDWSAD (29.7%). Males had almost two alarming with 70 to 80% of patients having poor gly- times the odds of developing cutaneous manifesta- cemic control [2]. Cutaneous manifestations of diabetes tions of T2DM, compared to females (adjusted odds mellitus appear at disease onset, after the disease is ratio [AOR]: 1.871, 95% CI: 1.108–3.160; P = 0.019). established or precede diabetes by many years. A cu- There was no association between glycemic control taneous condition is defined as any medical condition and cutaneous manifestations. However, males and that affects the system enclosing the body, including those with T2DM duration of five years and more had the skin, hair, nails, and related muscle and glands [3]. Cutaneous disorders due to T2DM are attributed to hyperglycemia which affects skin homeostasis resulting Address for correspondence: in altered keratinocytes metabolism and collagen pro- Nur Saádah Binti Mohd Abd Rasid perties [4, 5]. Relative insulin deficiency in T2DM causes Pusat Perubatan Universiti Kebangsaan Malaysia Jalan Yaacob Latif, Bandar Tun Razak poor growth and differentiation of keratinocyte [4, 5]. 56000 Kuala Lumpur, Malaysia Certain conditions such as skin tags and acanthosis nig- e-mail: [email protected] ricans are linked to hyperinsulinemia in the prediabetic Clinical Diabetology 2020, 9; 6: 461–468 DOI: 10.5603/DK.2020.0049 state while bullous diabeticorum, diabetic dermopathy Received: 30.06.2020 Accepted: 02.11.2020 and scleroderma are more often see in long stand- 461 Clinical Diabetology 2020, Vol. 9, No 6 ing T2DM [6]. Microvascular complications, impaired Section B recorded cutaneous manifestation of wound healing and other undetermined mechanisms T2DM that was diagnosed on the consultation day. A further contribute to cutaneous disease [7]. list of skin manifestations associated with T2DM was Prevalence of dermatological disorders due to derived from literature search and expert panel input T2DM ranges from 36% to as high as 88.3% [8, 9]. [13, 14]. Cutaneous manifestations of diabetes mellitus Factors associated with cutaneous manifestations were classified into 4 types which are skin diseases with are poor glycemic control (HbA1c > 7%) [10, 11] and weak to strong associations with diabetes (SDWSAD), duration of diabetes [8]. Longer disease duration have skin infections (SI), skin manifestations due to diabe- higher incidence of diabetic dermopathy [8]. Profiling tes complication (SMDC) and skin reaction to diabetic characteristics of T2DM and cutaneous manifesta- treatment [13, 14]. Skin reaction to diabetic treatment tions may help in early diagnosis of diabetes, used was excluded as the objective of this study was to as a surrogate marker for poor glycemic control and determine the cutaneous manifestations purely due microvascular complications in other organs. Hence to T2DM and not due to effect of treatment or other the aim of this study is to determine the prevalence of secondary causes. Hence lesions which fulfilled these cutaneous manifestation among patients with T2DM three categories were included: and to determine its associated factors. — Skin Diseases with Weak to Strong Associations with Diabetes (SDWSAD): diabetic dermopathy, Methods acanthosis nigricans, yellow skin, eruptive xan- A cross-sectional study was performed between thoma, oral leukoplakia, lichen planus, necrobiosis June and September 2019 at the primary care clinic of lipoidica, granuloma annulare and diabetic bullae. a university in Kuala Lumpur. Sample size of 246 was Diabetic dermopathy is described as asymptomatic calculated using Kish formula, 80% was taken as the well circumscribed pinkish or brownish atrophic highest prevalence cutaneous manifestation of T2DM (depressed) lesion on shin, thigh, forearm, scalp or [8] with 95% confidence interval and 5% absolute trunk. Lesion may arise in crops gradually resolve, precision. The final sample size was 271 as 10% was reappear and sometimes ulcerate; added to overcome possible incomplete data. Partici- — Skin infections (SI): impetigo, ecthyma, cellulitis, pants were selected using systematic random sampling folliculitis, furunculosis, carbuncles, erysipelas, vi- (sampling interval of 2) from the list of T2DM patients ral warts, tinea capitis, tinea pedis, tinea corporis, who registered for consultation. Type 1 diabetes mel- tinea cruris, tinea versicolor, tinea manuum, paro- litus (T1DM), pregnancy and patients with dermatoses nychia, onychomycosis, candidiasis. Infections due to physical factors such as burns, and trauma were of both dermal and mucosa surfaces were taken excluded. Written consent was obtained. A thorough into consideration encompassing all types of bac- physical examination from head to toe including terial and viral infections. All four clinical types genitalia was performed to evaluate the cutaneous of onychomycosis i.e. total dystrophic, white su- manifestations. perficial, candida, proximal and distal subungual A data collection form was designed to record the onychomycosis were all included under the broad intended data, based on a literature search and expert term of onychomycosis; opinion. Section A consists of socio-demographic in- — Skin manifestation of diabetic complication formation such as age, gender, ethnicity and clinical (SMDC): microangiopathy, macroangiopathy, profile such as duration of diabetes, diabetic compli- neuropathy e.g. diabetic foot and trophic ulcers. cation (neuropathy, nephropathy, retinopathy, and Patients presenting with of any of the cutaneous peripheral vascular disease), body mass index (BMI) and disorders related to T2DM was labelled as having cu- HbA1c level. Information on HbA1c, diabetic retinopa- taneous manifestations of T2DM. Other cutaneous le- thy, nephropathy and lipid levels was extracted from sions were recorded if found to be present. The primary participant’s electronic database. For the purpose of researcher received hands-on training from a qualified this study, HbA1c level of > 6.5% was considered as dermatologist and a family medicine specialist with poor glycemic control while ≤ 6.5% was considered as qualification in family practice dermatology prior to a good glycemic control [12]. Peripheral neuropathy the commencement of this study. Clinical diagnosis was was screened using 10-g monofilament, vibration made by the primary investigator. Inter-rater reliability sense using a 128-Hz tuning fork and ankle reflex [12]. for the clinical diagnosis between the 3 investigators Peripheral vascular disease (PVD) was objectively was performed using images of the lesions and meas- screened based on examination of distal pulses, capil- ured using Cohen’s Kappa to ensure the reliability of lary return time and skin color. the diagnosis. 462 Nur Saadah Mohd Abd Rasid et al., Cutaneous manifestations among diabetics The data collected was analyzed using SPSS (ver- Table 1. Sociodemographic and clinical characteristics of sion 25). Descriptive analysis was performed using the study participants frequencies and percentage. Simple and multiple lo- Variables n (%) Median (IQR) gistic regression analyses were used to determine the Age (years) 66 (13.0) association between type of cutaneous manifestation Gender with sociodemographic characteristics and clinical Male 141 (52) profile. Cohen’s Kappa was used to determine the Female 130 (48) agreement between the researchers’ diagnoses of the Ethnicity skin condition. This research was approved by the Re- Malay 131