|Year : 2017 | Volume
| Issue : 1 | Page : 9-14
Comparison of cutaneous manifestations of diabetic with nondiabetic patients: A case-control study
Banavasi S Girisha1, Neethu Viswanathan2
1 Department of Dermatology, K.S. Hegde Medical Academy, Mangalore, Karnataka, India
2 Consultant Dermatologist, Payyanur, Kerala, India
|Date of Web Publication||28-Dec-2016|
Banavasi S Girisha
Department of Dermatology, K.S. Hegde Charitable Hospital, Deralakatte, Mangalore - 575 018, Karnataka
Source of Support: None, Conflict of Interest: None
Background: Diabetes mellitus is a metabolic disorder characterized by raised fasting and postprandial blood glucose levels and a variety of multisystem complications. The prevalence of skin manifestations seems to be similar between type 1 and type 2 diabetes mellitus patients. Cutaneous manifestations usually develop following the diagnosis of diabetes, but in some patients, they are the initial presenting signs, thereby helping in the early diagnosis of diabetes mellitus. Objectives: The objective of this study is to describe the cutaneous lesions in patients with type 2 diabetes mellitus and to compare the pattern of skin manifestations in diabetics and nondiabetics in coastal Karnataka and neighboring districts of Kerala. Methodology: This case-control study included 400 patients with type 2 diabetes mellitus and cutaneous manifestations attending the outpatient Departments of Dermatology and General Medicine and those admitted under these departments. A total of 400 age and sex-matched nondiabetic patients were included as controls. Results: Cutaneous infections were noted in 148 (37%) diabetics of which fungal infections were the most common seen in 106 (26.5%) patients, followed by xerosis in 121 (30.25%) and acrochordons in 71 (17.75%) patients. Other dermatoses associated with diabetes mellitus noted were acanthosis nigricans (5.5%), scleredema diabeticorum (0.25%), diabetic bullae (0.5%), and Kyrle's disease (1%). Cutaneous changes associated with neurovascular complications included diabetic foot in 3%, diabetic dermopathy in 2%, and pigmented purpuric dermatosis in 0.25% of the diabetics. Conclusion: A joint effort between dermatology and general medicine is necessary for the early recognition and treatment of the skin conditions and also to ensure adequate metabolic control.
Keywords: Acrochordons, fungal infections, type 2 diabetes mellitus, xerosis
|How to cite this article:|
Girisha BS, Viswanathan N. Comparison of cutaneous manifestations of diabetic with nondiabetic patients: A case-control study. Clin Dermatol Rev 2017;1:9-14
|How to cite this URL:|
Girisha BS, Viswanathan N. Comparison of cutaneous manifestations of diabetic with nondiabetic patients: A case-control study. Clin Dermatol Rev [serial online] 2017 [cited 2018 Jun 19];1:9-14. Available from: http://www.cdriadvlkn.org/text.asp?2017/1/1/9/196944
| Introduction|| |
Diabetes mellitus is a metabolic disorder characterized by raised fasting and postprandial blood glucose levels and a variety of multisystem complications.  It is the most common endocrine disorder in the world and is known to affect 8.3% of the population.  In type 1 diabetes mellitus, there is complete or near total insulin deficiency. Type 2 diabetes mellitus is characterized by variable degrees of insulin resistance, impaired insulin secretion, and increased glucose production.  The prevalence of skin manifestations seems to be similar between type 1 and type 2 diabetes mellitus patients. However, cutaneous infections seem to be more frequent in type 2 diabetes mellitus and type 1 diabetes mellitus patients manifest more autoimmune type cutaneous lesions. , In most cases, the cutaneous manifestations usually develop following the diagnosis of diabetes but in some, skin manifestations are the initial presenting signs, thereby helping in the early diagnosis of diabetes mellitus. 
There are multiple factors that contribute to the pathogenesis of cutaneous conditions in this disorder which include abnormalities in carbohydrate metabolism, alteration in other metabolic pathways, vascular abnormalities such as microangiopathy, atherosclerosis, neuronal degeneration, and impaired host mechanisms. , The skin manifestations in diabetes mellitus can vary from minor to life-threatening.  The International Diabetes Federation has observed the total number of diabetic subjects to be around 40.9 million in India, and this is expected to come up to 69.9 million by the year 2025. ,
The objectives of the study was to describe the cutaneous lesions in patients with type 2 diabetes mellitus and to compare the pattern of skin manifestations in diabetics and nondiabetics in coastal Karnataka and neighboring districts of Kerala.
| Methodology|| |
The study was a hospital-based case-control study, conducted from January 2014 to January 2015. Ethical clearance was taken from the Institutional Ethics Committee before starting the study. A total of 400 patients with type 2 diabetes mellitus and cutaneous manifestations attending the out-patient Departments of Dermatology and General Medicine, and those admitted under these departments in Justice K.S. Hegde Charitable Hospital, Mangalore constituted the study group. Four hundred age- and gender-matched individuals with no history of diabetes mellitus and normal random blood sugar levels were taken as controls. Controls were taken from the patients attending Dermatology and General Medicine Outpatient/Inpatient Departments, so as to maintain a homogenous environment for both the cases and controls. Informed consent was taken from all the cases and controls included in the study.
Patients with type 1 diabetes mellitus, gestational diabetes, HIV, malignancies, those on dialysis, immunosuppressive drugs and those not consenting to participate in the study were excluded. Diabetics with glycosylated hemoglobin (HbA1c) <7% were placed under the good control group, and those with HbA1c ≥8% were placed under the poor control group.
Complete physical examination along with local examination of lesions, complete blood picture, fasting blood sugar, postprandial blood sugar, and HbA1c were done in all cases. Serum lipid profile, serum creatinine, and fundus examination were done to detect complications. Relevant microbiological and histopathological investigations were done wherever necessary to confirm the clinical diagnosis. Findings were recorded and results obtained were tabulated and statistically analyzed using Chi-square test for association of attributes.
| Results|| |
Among the 400 diabetics studied, 245 were males and 155 were females with a male:female ratio 1.58:1. Most of the diabetics in the study belong to fifth and sixth decades of life with the mean age 57.4 ± 11.6 years. Ninety-nine (24.75%) diabetic patients had a positive family history of diabetes mellitus. The mean duration of diabetes was 6.8 ± 6.24 years. Poorly controlled diabetics, consisting of 258 (64.5%) patients formed majority of the study group. Twelve (3%) patients were in intermediate glycemic control, and 130 (32.5%) patients were in good glycemic control group.
Among the associated systemic illnesses, hypertension was the most common disease seen in 200 (50%) diabetics followed by dyslipidemia in 68 (17%) and obesity in 17 (4.25%) patients. Chronic obstructive pulmonary disease in 17 (4.25%), hypothyroidism in 10 (2.5%), cerebrovascular accident and tuberculosis in 6 (1.25%) patients each were the other systemic disorders found in our study.
In this study, 145 (36.25%) patients were found to have nonproliferative diabetic retinopathy, 12 (3%) patients were found to have diabetic nephropathy and 5 (1.25%) patients had diabetic neuropathy. Most of the diabetic patients were on oral hypoglycemics, i.e., 243 (60.75%) patients followed by 55 (13.75%) patients on insulin. Nine (2.25%) patients were being treated with both insulin and oral hypoglycemics. Fourteen (3.5%) were on diet control. Details of treatment taken were not known in 30 (7.5%) patients while 49 (12.25%) patients were not on any form of treatment.
Various cutaneous manifestations observed in diabetics are shown in [Table 1] and [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5] and [Figure 6]. Comparison of the common cutaneous manifestations between cases and controls are shown in [Table 2] and [Figure 7].
|Figure 3: Balanoposthitis - Inflammation and fissuring of prepuce and glans|
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|Figure 6: Diffuse induration of upper back seen in scleredema diabeticorum|
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|Table 2: Comparison of frequencies of the common cutaneous manifestations between cases and controls|
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| Discussion|| |
Skin manifestations are seen frequently in diabetes mellitus and sometimes may signal the onset of this disorder. Without the control of diabetes mellitus, the mucocutaneous manifestations are often intractable. The majority of our patients had diabetes for a duration of 5 years or more. With the increase in duration of diabetes, nonenzymatic glycosylation of dermal collagen and mucopolysaccharides occurs which results in the various dermatological manifestations.  A comparison of the important dermatoses in this study with the current literature is given in [Table 3].
|Table 3: Comparison of the important dermatoses in this study with the current literature|
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Diabetes if not controlled predisposes the skin to multiple infections as well as increases the possibility of developing neurovascular and other systemic complications which can give rise to various dermatological manifestations. , Cutaneous infections were seen more among the patients with poor glycemic control as compared to those with good glycemic control though a significant relationship between glycemic control and the prevalence of cutaneous infections could not be obtained. Hyperglycemia affects host defenses by causing functional abnormality in leucocytes which results in diminished leukocyte response and impaired phagocytosis. The hyperosmolar serum reduces chemotaxis, and lack of insulin causes impaired cytokine release.  Yosipovitch et al. and Sawhney et al. also observed that majority of the patients with cutaneous lesions in their respective studies were under poor glycemic control. ,
The presence of fungal infections noted in about one-fourth of our patients could be because of decreased resistance, hot and humid climate prevalent in coastal area causing increased sweating and also the use of synthetic clothing. In the current study, candidal infections were more than dermatophytic infections which was similar to the study done by Bhat et al. 
In the current study, xerosis was the most common noninfectious cutaneous manifestation associated with diabetes mellitus followed by acrochordons. We found a significant association between diabetes and xerosis (P < 0.05). Xerosis ranged from mild skin dryness with minimal scales to severe dry skin with profuse scaling and asteatotic dermatitis. Advanced glycation products of proteins in the stratum corneum, as well as autonomic neuropathy, have been attributed to the pathogenesis of xerosis.  Association of diabetes with acrochordons was also significant (P < 0.001). This may be due to the insulin resistance and consequent hyperinsulinemia and increased insulin-like growth factors. 
The proportion of acanthosis nigricans among the diabetics in the study is similar to studies done on Indian patients. ,, Acanthosis nigricans is marked as a risk factor for developing type 2 diabetes mellitus. Raised levels of insulin act on insulin-like growth factor receptors leading to the development of acanthosis nigricans.  We did not find any significant association between diabetes and acanthosis nigricans.
Pruritus causes excoriations on the skin which increases the risk of developing of infections. Generalized pruritus may be seen secondary to complications such as xerosis, chronic renal insufficiency, and diabetic polyneuropathy. Certain antidiabetic drugs and dry skin which is aggravated by age and reduced sweating secondary to diabetic autonomic neuropathy have also been implicated in the pathogenesis of diabetic pruritus. 
Seborrheic keratosis is a proliferative skin condition where the role of growth factors has been suggested. Insulin-like growth factors cause keratinocyte and dermal fibroblast proliferation. We found a significant association of seborrheic keratosis with diabetes (P = 0.003). Ragunatha et al. also reported a similar prevalence of seborrheic keratosis in their study.  A higher frequency of cherry angioma was noted in diabetics as compared to nondiabetics, which was statistically significant (P < 0.05). Although a relationship between diabetes mellitus and cherry angioma is not established, several studies have noted large numbers of cherry angioma in many diabetics.
Diabetic foot, diabetic dermopathy, and diabetic bulla were less frequent in our study. Diabetic foot can result from a combination of multifactorial pathogenic mechanisms. Along with diabetic micro- and macro-angiopathy as well as neuropathy, skeletal deformities, and wearing of inappropriate footwear may contribute to the development of diabetic foot.  Several studies have shown that diabetic dermopathy seems to be a common finding in Western population than in the Indian population. Low percentage of diabetic bullae may be because the condition usually goes under-diagnosed as it may heal spontaneously in diabetics who do not seek medical attention.  A comparison of cutaneous manifestations in controlled and uncontrolled diabetes mellitus could not be made since majority were poorly controlled diabetics.
| Conclusion|| |
The frequency of cutaneous infections as well as diabetes-related dermatoses was higher among the diabetics than among nondiabetics. Patients with poorly controlled diabetes had more number of cutaneous infections and diabetes associated dermatoses. Our observations necessitate a joint effort between dermatology and general medicine for the early recognition and adequate treatment of the skin conditions and also to ensure adequate metabolic control to prevent the severity and recurrence of the skin lesions. Though in most cases, cutaneous conditions usually develop following the diagnosis of diabetes, in some these are the first presenting signs and help in the early diagnosis of diabetes. Thus, dermatologists play an important role in reducing morbidity and in improving the quality of life of diabetic patients.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Sarkany RP, Breathnach SM, Morris AA, Weismann K, Flynn PD. Metabolic and nutritional disorders. In: Burns T, Breathnach S, Cox N, Griffith C, editors. Rook's Textbook of Dermatology. 8 th
ed. Singapore: Blackwell Publishing Ltd.; 2010. p. 59.77-59.80.
Vahora R, Thakkar S, Marfatia Y. Skin, a mirror reflecting diabetes mellitus: A longitudinal study in a tertiary care hospital in Gujarat. Indian J Endocrinol Metab 2013;17:659-64.
Powers AC. Diabetes mellitus. In: Longo DL, Kasper DL, Jameson JL, Fauci AS, Hauser SL, Loscalzo J, editors. Harrison's Principles of Internal Medicine. 19 th
ed. U.S.A: McGraw Hill Ltd.; 2015. p. 2399-407.
Timshina DK, Thappa DM, Agrawal A. A clinical study of dermatoses in diabetes to establish its markers. Indian J Dermatol 2012;57:20-5.
Ferringer T, Miller F 3 rd
. Cutaneous manifestations of diabetes mellitus. Dermatol Clin 2002;20:483-92.
Goyal A, Raina S, Kaushal SS, Mahajan V, Sharma NL. Pattern of cutaneous manifestations in diabetes mellitus. Indian J Dermatol 2010;55:39-41.
Bhat YJ, Gupta V, Kudyar RP. Cutaneous manifestations of diabetes mellitus. Int J Diabetes Dev Ctries 2006;26:152-5.
Kataria U, Chhillar D. Cutaneous manifestations of diabetes mellitus in controlled and uncontrolled state. Int Arch Integr Med 2015;2:90-3.
Rao MNS, Lakshmi PV, Kumar PJ. A prospective study of cutaneous abnormalities in patients with diabetes mellitus.IJPCBS 2015;5:276-86.
Ragunatha S, Anitha B, Inamadar AC, Palit A, Devarmani SS. Cutaneous disorders in 500 diabetic patients attending diabetic clinic. Indian J Dermatol 2011;56:160-4.
Foss NT, Polon DP, Takada MH, Foss-Freitas MC, Foss MC. Skin lesions in diabetic patients. Rev Saude Publica 2005;39:677-82.
Puri N. A study on the cutaneous manifestations of diabetes mellitus. Our Dermatol Online 2012;3:83-6.
Chatterjee N, Chattopadhyay C, Sengupta N, Das C, Sarma N, Pal SK. An observational study of cutaneous manifestations in diabetes mellitus in a tertiary care Hospital of Eastern India. Indian J Endocrinol Metab 2014;18:217-20.
Tseng HW, Ger LP, Liang CK, Liou HH, Lam HC. High prevalence of cutaneous manifestations in the elderly with diabetes mellitus: An institution-based cross-sectional study in Taiwan. J Eur Acad Dermatol Venereol 2015;29:1631-5.
Al-Mutairi N, Zaki A, Sharma AK, Al-Sheltawi M. Cutaneous manifestations of diabetes mellitus. Study from Farwaniya hospital, Kuwait. Med Princ Pract 2006;15:427-30.
Sasmaz S, Buyukbese M, Cetinkaya A, Celik M, Arican O. The prevalence of skin disorders in type-2 diabetic patients. Internet J Dermatol 2004. Available from: http://print.ispub.com/api/0/ispub-article/8588. [Last accessed on 2016 May 20].
Jatav RK, Kumbhare MB, Chennamaneni R. Cutaneous manifestations of diabetes mellitus in adult patients of Telangana region of South India. Eur J Acad Essays 2014;1:38-44.
Mahajan S, Koranne RV, Sharma SK. Cutaneous manifestation of diabetes mellitus. Indian J Dermatol Venereol Leprol 2003;69:105-8.
Nigam PK, Pande S. Pattern of dermatoses in diabetics. Indian J Dermatol Venereol Leprol 2003;69:83-5.
Raghu TY, Vinayak V, Kanthraj GR, Girisha BS. Study of cutaneous manifestations of diabetes mellitus. Indian J Dermatol 2004;49:73-5.
Yosipovitch G, Hodak E, Vardi P, Shraga I, Karp M, Sprecher E, et al.
The prevalence of cutaneous manifestations in IDDM patients and their association with diabetes risk factors and microvascular complications. Diabetes Care 1998;21:506-9.
Sawhney M, Talwar OP, Tutakne MA, Rajpathak SD. Diabetic dermoangiopathy: A clinico-pathological correlation. Indian J Dermatol Venereol Leprol 1992;58:173-8.
Bhargava P, Mathur SK, Mathur DK, Malpani S, Goel S, Agarwal US, et al.
Acrochordon, diabetes and associations. Indian J Dermatol Venereol Leprol 1996;62:226-8.
Burke JP, Hale DE, Hazuda HP, Stern MP. A quantitative scale of acanthosis nigricans. Diabetes Care 1999;22:1655-9.
Sreedevi C, Car N, Pavlic-Renar I. Dermatologic lesions in diabetes mellitus. Diabetol Croat 2002;31:147-54.
Gkogkolou P, Böhm M. Skin disorders in diabetes mellitus. J Dtsch Dermatol Ges 2014;12:847-64.
Gupta V, Gulati N, Bahl J, Bajwa J, Dhawan N. Bullosis diabeticorum: Rare presentation in a common disease. Case Rep Endocrinol 2014;2014:862912.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]
[Table 1], [Table 2], [Table 3]