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Comparison of skin blood flow values (mean ± SEM) for unaffected skin, diabetic dermopathy sites, and scar sites at 35°C and 44°C.

Comparison of skin blood flow values (mean ± SEM) for unaffected skin, diabetic dermopathy sites, and scar sites at 35°C and 44°C.

Blood Flow at Several Reference Points in Dermopathy Patients With and Without Diabetes*
Blood Flow at Several Reference Points in Dermopathy Patients With and Without Diabetes*
1.
Melin  H An atrophic circumscribed skin lesion in the lower extremities of diabetics Acta Med Scand. 1964;176(suppl 423)1- 75
PubMed
2.
Murphy  RA Skin lesions in diabetic patients: the "spotted leg" syndrome Lahey Clin Found Bull. 1965;1410- 14
PubMed
3.
Binkley  GWGiraldo  BStoughton  RB Diabetic dermopathy: a clinical study Cutis. 1967;3955- 958
4.
Danowski  TXSabeh  GSarver  MEShelkrot  JFisher  ER Shin spots and diabetes mellitus Am J Med Sci. 1966;251570- 575
PubMedArticle
5.
Bauer  MLevan  NE Diabetic dermangiopathy: a spectrum including pretibial pigmented patches and necrobiosis lipoidica diabeticorum Br J Dermatol. 1970;83528- 535
PubMedArticle
6.
Huntley  AC Cutaneous manifestations of diabetes mellitus Dermatol Clin. 1989;7531- 546
PubMed
7.
Jelinek  JE Cutaneous manifestations of diabetes mellitus Int J Dermatol. 1994;33605- 617
PubMedArticle
8.
Fisher  ERDanowski  TS Histologic, histochemical, and electron microscopic features of the shin spots of diabetes mellitus Am J Clin Pathol. 1968;50547- 554
PubMed
9.
Shemer  ABegman  RLinn  SKantor  YFriedman-Birnbaum  RL Diabetic dermopathy and internal complications in diabetes mellitus Int J Dermatol. 1998;37113- 115
PubMedArticle
10.
Rendell  MBergman  TO'Donnell  GDrobny  EBorgos  JBonner  RF Microvascular blood flow, volume, and velocity measured by laser Doppler techniques in insulin dependent diabetes Diabetes. 1989;38819- 824
PubMedArticle
11.
Rendell  MBamisedun  O Diabetic cutaneous microangiopathy Am J Med. 1992;93611- 618
PubMedArticle
12.
Rendell  MSaxena  SShah  D Cutaneous blood flow and peripheral resistance in type II diabetes as compared to intermittent claudication patients Int J Angiology. In press
13.
Bonner  RNossal  R Model for laser Doppler measurements of blood flow in tissue Appl Opt. 1981;202097- 2107Article
14.
Nitzan  MFairs  SLERoberts  VC Simultaneous measurement of skin blood flow by the transient thermal-clearance method and laser Doppler flowmetry Med Biol Eng Comput. 1988;6407- 410Article
15.
Saumet  JLDittmar  ALeftheriotis  G Non-invasive measurement of skin blood flow: comparison between plethysmography, laser Doppler flowmeter and heat thermal clearance method Int J Microcirc Clin Exp. 1986;573- 83
PubMed
16.
Chung  RSBruch  DDearlove  J Endoscopic measurement of gastric mucosal flow by laser Doppler velocimetry: effect of chronic esophageal variceal sclerosis Am Surg. 1988;54116- 120
PubMed
17.
Engelhart  MKristensen  JK Evaluation of cutaneous blood flow responses by 133Xenon washout and a laser Doppler flowmeter J Invest Dermatol. 1983;8012- 15
PubMedArticle
18.
Kvietys  PRShepherd  APGranger  DN Laser-Doppler, H2 clearance, and microsphere estimates of mucosal blood flow Am J Physiol. 1985;249G221- G227
PubMed
19.
Winsor  THaumschild  DJWinsor  DWWang  WLuong  TN Clinical application of laser Doppler flowmetry for measurement of cutaneous circulation in health and disease Angiology. 1987;38727- 736
PubMedArticle
20.
Popoff  NW The digital vascular system Arch Pathol. 1934;18295- 330
21.
Rowell  LB Reflex control of the cutaneous vasculature J Invest Dermatol. 1977;69154- 166
PubMedArticle
22.
Timar-Banu  OBeauregard  HTousignant  J  et al.  Development of noninvasive and quantitative methodologies for the assessment of chronic ulcers and scars in humans Wound Repair Regen. 2001;9123- 132
PubMedArticle
23.
Musgrave  MAUmraw  NFish  JSGomez  MCartotto  RC The effect of silicone gel sheets on perfusion of hypertrophic burn scars J Burn Care Rehabil. 2002;23208- 214
PubMedArticle
24.
Ehrlich  HPKelley  SF Hypertrophic scar: an interruption in the remodeling of repair—a laser Doppler blood flow study Plast Reconstr Surg. 1992;90993- 998
PubMedArticle
25.
Lithner  F Cutaneous reactions of the extremities of diabetics to local thermal trauma Acta Med Scand. 1975;198319- 325
PubMedArticle
26.
Rendell  MSMilliken  BKFinnegan  MFFinney  DEHealy  JC The skin blood flow response in wound healing Microvasc Res. 1997;53222- 234
PubMedArticle
27.
Rendell  MSMilliken  BKFinnegan  MFFinney  DEHealy  JCBonner  RF A comparison of the microvascular response in the healing wound in the spontaneously hypertensive and non-hypertensive rat Int J Surg Investig. 2000;217- 25
PubMed
28.
Svedman  PSvedman  CNjalsson  T Epithelialization and blood flow in suction blister wounds on healthy volunteers J Invest Surg. 1991;4175- 189
PubMedArticle
29.
Atiles  LMileski  WPurdue  GHunt  JBaxter  C Laser Doppler flowmetry in burn wounds J Burn Care Rehabil. 1995;16388- 393
PubMedArticle
30.
Clark  JALeung  KSCheng  JCLeung  PC The hypertrophic scar and microcirculation properties Burns. 1996;22447- 450
PubMedArticle
Study
October 2004

Skin Blood Flow in Diabetic Dermopathy

Author Affiliations

From the Department of Medicine, Creighton University School of Medicine, Omaha, Neb (Mr Wigington and Drs Ngo and Rendell), and Rose Salter Medical Research Foundation, Baltimore, Md (Dr Rendell). Dr Ngo is now with the Department of Medicine, University of Southern California, Keck School of Medicine of USC, Los Angeles. The authors have no relevant financial interest in this article.

Arch Dermatol. 2004;140(10):1248-1250. doi:10.1001/archderm.140.10.1248
Abstract

Background  Diabetic dermopathy has been termed the most common cutaneous finding in diabetes, occurring in as many as 40% of diabetic patients older than 50 years. Using laser Doppler technology, we tested the hypothesis that dermopathy lesions represented areas of cutaneous ischemia.

Design  A survey of cutaneous blood flow in diabetic patients with dermopathy and comparison of values with those in nondiabetic patients.

Setting  Outpatient clinic specializing in diabetes.

Patients  A consecutive sample of 61 diabetic patients (52 men and 9 women; mean ± SEM age, 58 ± 2 years) with dermopathy had blood flow measurements performed at the sites of dermopathy and at contiguous uninvolved sites. Flow values were also determined at several reference sites and compared with those in 41 nondiabetic control subjects (30 men and 11 women; mean age, 53 ± 3 years).

Results  Heat-stimulated blood flow values at the knee, ankle, and toe were about 50% lower for the dermopathy patients than for the nondiabetic controls. Yet, despite their reduced skin blood flow reserve, the dermopathy lesions did not show relative ischemia. At the basal temperature of 35°C, flow was 1.1 ± 0.1 mL /min per 100 g of tissue in apparently normal skin vs 2.2 ± 0.2 at dermopathy sites; at 44°C, flow at the normal sites was 7.9 ± 0.3 mL /min per 100 g of tissue vs 12.9 ± 0.6 at dermopathy sites (P<.01 for both comparisons).

Conclusions  Although patients with diabetic dermopathy exhibited reduced skin blood flow compared with nondiabetic volunteers, flow levels were considerably higher at the dermopathy sites than at contiguous uninvolved skin sites. These results refute the hypothesis that diabetic dermopathy represents local ischemia. However, it is still possible that the scarring represented by dermopathy lesions is related to decreased skin perfusion due to diabetes.

Diabetic dermopathy has been termed the most common cutaneous finding in diabetes, occurring in as many as 40% of diabetic patients older than 50 years.17 Diabetic dermopathy appears as round to oval atrophic hyperpigmented macules on the pretibial areas of the lower extremities. The lesions are usually bilateral and have an asymmetric distribution. Their histologic appearance is one of edema of the papillary dermis, thickened superficial blood vessels, extravasation of erythrocytes, and a mild lymphocytic infiltrate.8 The extravasated erythrocytes leave hemosiderin deposits, which provide the brownish hyperpigmentation. The presence of multiple lesions is pathognomonic for diabetes. No similar skin condition appears in nondiabetic patients.

It has been postulated that diabetic dermopathy is related to microangiopathy since the lesions are seen more frequently in patients with diabetes of long duration and with coexisting diabetic microvascular disease.9 In previous studies, we have demonstrated a disorder of skin blood flow in diabetic patients with no evidence of cutaneous disease. Although skin blood flow at basal body temperature is not different from that in nondiabetic subjects, there is a 40% to 50% reduction of heat-stimulated flow in diabetic patients compared with the nondiabetic control population.10 Heat stimulation elicits maximal vasodilation of the cutaneous microvasculature, so that the reduced flow values in diabetes indicate a loss of skin blood flow reserve. This impairment of blood flow reserve affects patients with type 1 and type 2 diabetes and presumably reflects a diabetic cutaneous microangiopathy.11,12 It is possible that diabetic dermopathy is related to diabetic microangiopathy, and that these lesions represent areas of ischemia. Therefore, to assess this possibility, we measured skin blood flow in diabetic dermopathy lesions and compared the results with those in normal skin areas.

METHODS
PATIENT SELECTION

We included male and female patients with type 1 or type 2 diabetes and evident diabetic dermopathy. Informed consent was obtained from each subject after the nature of all procedures and the protection of confidentiality had been fully explained.

SKIN BLOOD FLOW MEASUREMENTS

We used a Vasamedic Model 403B laser Doppler device (Vasamedics Inc, St Paul, Minn), which was designed based upon the original theoretical model of Bonner and Nossal.13 A low-power solid-state laser diode provides the coherent light source that is delivered through a fiber optic line to a probe affixed to the skin with an adhesive ring. Two separate fiber optic lines gather the photons from the skin surface and return them to a photodetector that converts them to a direct current (DC) electrical signal related to the level of scatter from stationary tissue and an additional small alternating current (AC) signal generated by Doppler-shifted photons. The AC/DC ratio is converted to the average number of Doppler shifts per photon. That number is proportional to the blood volume. A signal-processing algorithm converts a time domain autocorrelation to a frequency domain, which gives a mean frequency proportional to blood velocity. Blood flow is the product of linearized volume and velocity. A calibration factor of 6 mL · 100 g-1 · min-1 · 100 Hz has been derived on the basis of theoretical calculations to convert the laser Doppler flow parameter to conventional blood flow units13 and has been verified in numerous tissues using several reference techniques.1419

A Vasamedic module TCM 420 was used for controlling local skin temperature. Doppler fiber laser optic probes were inserted into a 19-mm-diameter thermal head attached to a separate solid-state controller. The temperature was controlled in the range of ±0.5°C of set point. The probe was placed so that the fiber optic ends did not lie directly over a vein or hair follicle. Mean flow was measured using a 5-second averaging time to encompass cardiac pulsatile activity.

We measured flow at sites of diabetic dermopathy. We also obtained measurements at nearby uninvolved sites with apparently normal skin. As reference points, we also performed readings at the following locations: (1) the plantar surface of the tip of the index finger (finger pulp); (2) the dorsal surface of the distal phalange of the index finger, immediately proximal to the nail bed (finger dorsum); (3) the plantar surface of the tip of the great toe (toe pulp); (4) the extensor surface of the distal phalange of the great toe, immediately proximal to the nail bed (toe dorsum); (5) the pretibial surface of the leg immediately below the patella (knee); and (6) the dorsal surface of the ankle, between the medial and lateral malleoli (ankle). The finger and toe pulps have a high density of arteriovenous anastomoses with a low resistance and high flow.20 The knee and ankle have a primarily nutritive capillary perfusion with high resistance and low flow.21 The dorsal surfaces of the finger and toe have a relatively high, primarily nutritive capillary perfusion.

STATISTICAL ANALYSIS

Comparisons were carried out by standard analysis of variance techniques. All results are presented as mean ± SEM.

RESULTS

We measured flow in 61 patients (52 men and 9 women; mean age, 58 ± 2 years) with diabetic dermopathy. The average duration of diabetes was 15 ± 1 years. The average hemoglobin A1c value in the diabetic group was 8.3% ± 0.2%. Retinopathy was observed in 45% of the patients, microalbuminuria in 50%, and neuropathy in 76%. Six patients had elevated serum creatinine levels. In this group of 61 patients, we performed measurements at a total of 243 sites of diabetic dermopathy and at 195 sites with no evident skin lesions. In addition, we measured flow at 26 sites of large scars unrelated to diabetes. There were 41 nondiabetic control subjects (30 men and 11 women; mean age, 53 ± 3 years). We performed measurements at the finger, toe, knee, and ankle in these control subjects. Consistent with our previous findings, blood flow values at 35°C at these sites on the extremities were similar in diabetic and nondiabetic subjects, but, at 44°C, flow values for the dermopathy patients were about 50% lower at the knee, ankle, and toe dorsum (Table).

Yet, despite the reduced skin blood flow reserve in the patients with dermopathy, the lesions themselves did not show relative ischemia. To the contrary, flow at the dermopathy sites was significantly higher than at contiguous uninvolved apparently normal skin sites (Figure). At the basal temperature of 35°C, flow was 1.1 ± 0.1 mL/min per 100 g of tissue in normal skin vs 2.2 ± 0.2 at dermopathy sites; at 44°C, flow at the normal sites was 7.9 ± 0.3 mL/min per 100 g of tissue vs 12.9 ± 0.6 at dermopathy sites (P<.01 for both comparisons). The readings obtained at diabetic dermopathy sites were similar to those obtained at scar sites unrelated to diabetes (Figure).

COMMENT

Although diabetic dermopathy is a well-recognized cutaneous manifestation of diabetes, the etiology of this condition is unknown. In prior work, we have demonstrated that skin blood flow reserve is reduced in diabetic patients. This decrease in skin blood flow reserve correlates with increasing duration of diabetes and with the presence of retinopathy and proteinuria, but not with neuropathy.11 Therefore, we have proposed that decreased skin blood flow reserve represents a true cutaneous diabetic microangiopathy.

We explored the possibility that diabetic dermopathy is related to this cutaneous microangiopathy. Our patients had an average duration of diabetes of about 15 years, with a high incidence of retinopathy, microalbuminuria, and neuropathy. They had significantly decreased skin blood flow reserve compared with a control group of nondiabetic subjects, yet blood flow values at the dermopathy sites were not low as would be expected if they represent areas of ischemia. To the contrary, flow levels were considerably higher at dermopathy sites than at contiguous uninvolved skin. The flow values at dermopathy sites were similar to those found in scar sites. Other investigators have documented that blood flow is increased in hypertrophic but not atrophic scars.2224 These results suggest that diabetic dermopathy lesions are, in fact, scars. Patients typically ascribe their dermopathy lesions to prior trauma. In fact, it has been possible to produce lesions resembling diabetic dermopathy by local thermal trauma.25

Although our results appear to refute the hypothesis that diabetic dermopathy represents local ischemia, it is still plausible that decreased skin blood flow leads to the development of diabetic dermopathy. It is possible that an active cutaneous flow is required for healing to proceed with minimal scar formation. A pronounced hyperemic response occurs early in the process of wound healing.26,27 Studies of burn wounds suggest that wounds that heal rapidly without scarring have higher initial perfusion than those with slow healing.2830 Perhaps skin perfusion in diabetic patients may be insufficient to heal wounds without scarring. Even minor trauma may lead to scar formation in these patients. This could be the etiology of the lesions of diabetic dermopathy. Further studies must focus on this possibility.

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Article Information

Correspondence: Marc Rendell, MD, Creighton Diabetes Center, Suite 6715, 601 N 30th St, Omaha, NE 68131 (Rendell@asndi.com).

Accepted for publication May 17, 2004.

This work was presented in part at the Southern California Regional Meeting, Chapter 1 of the American College of Physicians; April 3, 2004; Los Angeles, Calif.

We are grateful for support in the writing of the manuscript provided by the Rose Salter Medical Research Foundation, Baltimore, Md.

References
1.
Melin  H An atrophic circumscribed skin lesion in the lower extremities of diabetics Acta Med Scand. 1964;176(suppl 423)1- 75
PubMed
2.
Murphy  RA Skin lesions in diabetic patients: the "spotted leg" syndrome Lahey Clin Found Bull. 1965;1410- 14
PubMed
3.
Binkley  GWGiraldo  BStoughton  RB Diabetic dermopathy: a clinical study Cutis. 1967;3955- 958
4.
Danowski  TXSabeh  GSarver  MEShelkrot  JFisher  ER Shin spots and diabetes mellitus Am J Med Sci. 1966;251570- 575
PubMedArticle
5.
Bauer  MLevan  NE Diabetic dermangiopathy: a spectrum including pretibial pigmented patches and necrobiosis lipoidica diabeticorum Br J Dermatol. 1970;83528- 535
PubMedArticle
6.
Huntley  AC Cutaneous manifestations of diabetes mellitus Dermatol Clin. 1989;7531- 546
PubMed
7.
Jelinek  JE Cutaneous manifestations of diabetes mellitus Int J Dermatol. 1994;33605- 617
PubMedArticle
8.
Fisher  ERDanowski  TS Histologic, histochemical, and electron microscopic features of the shin spots of diabetes mellitus Am J Clin Pathol. 1968;50547- 554
PubMed
9.
Shemer  ABegman  RLinn  SKantor  YFriedman-Birnbaum  RL Diabetic dermopathy and internal complications in diabetes mellitus Int J Dermatol. 1998;37113- 115
PubMedArticle
10.
Rendell  MBergman  TO'Donnell  GDrobny  EBorgos  JBonner  RF Microvascular blood flow, volume, and velocity measured by laser Doppler techniques in insulin dependent diabetes Diabetes. 1989;38819- 824
PubMedArticle
11.
Rendell  MBamisedun  O Diabetic cutaneous microangiopathy Am J Med. 1992;93611- 618
PubMedArticle
12.
Rendell  MSaxena  SShah  D Cutaneous blood flow and peripheral resistance in type II diabetes as compared to intermittent claudication patients Int J Angiology. In press
13.
Bonner  RNossal  R Model for laser Doppler measurements of blood flow in tissue Appl Opt. 1981;202097- 2107Article
14.
Nitzan  MFairs  SLERoberts  VC Simultaneous measurement of skin blood flow by the transient thermal-clearance method and laser Doppler flowmetry Med Biol Eng Comput. 1988;6407- 410Article
15.
Saumet  JLDittmar  ALeftheriotis  G Non-invasive measurement of skin blood flow: comparison between plethysmography, laser Doppler flowmeter and heat thermal clearance method Int J Microcirc Clin Exp. 1986;573- 83
PubMed
16.
Chung  RSBruch  DDearlove  J Endoscopic measurement of gastric mucosal flow by laser Doppler velocimetry: effect of chronic esophageal variceal sclerosis Am Surg. 1988;54116- 120
PubMed
17.
Engelhart  MKristensen  JK Evaluation of cutaneous blood flow responses by 133Xenon washout and a laser Doppler flowmeter J Invest Dermatol. 1983;8012- 15
PubMedArticle
18.
Kvietys  PRShepherd  APGranger  DN Laser-Doppler, H2 clearance, and microsphere estimates of mucosal blood flow Am J Physiol. 1985;249G221- G227
PubMed
19.
Winsor  THaumschild  DJWinsor  DWWang  WLuong  TN Clinical application of laser Doppler flowmetry for measurement of cutaneous circulation in health and disease Angiology. 1987;38727- 736
PubMedArticle
20.
Popoff  NW The digital vascular system Arch Pathol. 1934;18295- 330
21.
Rowell  LB Reflex control of the cutaneous vasculature J Invest Dermatol. 1977;69154- 166
PubMedArticle
22.
Timar-Banu  OBeauregard  HTousignant  J  et al.  Development of noninvasive and quantitative methodologies for the assessment of chronic ulcers and scars in humans Wound Repair Regen. 2001;9123- 132
PubMedArticle
23.
Musgrave  MAUmraw  NFish  JSGomez  MCartotto  RC The effect of silicone gel sheets on perfusion of hypertrophic burn scars J Burn Care Rehabil. 2002;23208- 214
PubMedArticle
24.
Ehrlich  HPKelley  SF Hypertrophic scar: an interruption in the remodeling of repair—a laser Doppler blood flow study Plast Reconstr Surg. 1992;90993- 998
PubMedArticle
25.
Lithner  F Cutaneous reactions of the extremities of diabetics to local thermal trauma Acta Med Scand. 1975;198319- 325
PubMedArticle
26.
Rendell  MSMilliken  BKFinnegan  MFFinney  DEHealy  JC The skin blood flow response in wound healing Microvasc Res. 1997;53222- 234
PubMedArticle
27.
Rendell  MSMilliken  BKFinnegan  MFFinney  DEHealy  JCBonner  RF A comparison of the microvascular response in the healing wound in the spontaneously hypertensive and non-hypertensive rat Int J Surg Investig. 2000;217- 25
PubMed
28.
Svedman  PSvedman  CNjalsson  T Epithelialization and blood flow in suction blister wounds on healthy volunteers J Invest Surg. 1991;4175- 189
PubMedArticle
29.
Atiles  LMileski  WPurdue  GHunt  JBaxter  C Laser Doppler flowmetry in burn wounds J Burn Care Rehabil. 1995;16388- 393
PubMedArticle
30.
Clark  JALeung  KSCheng  JCLeung  PC The hypertrophic scar and microcirculation properties Burns. 1996;22447- 450
PubMedArticle
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