Aesthetic facial concerns have been the main reason for dermatological consults in the last few years 1. Besides the common alterations related to the intrinsic and extrinsic aging processes, there is one that affects individuals of any age, both sexes, and all races – the so-called dark circles, periorbital darkening or periorbital melanosis (POM). Unfortunately, this manifestation worsens with skin sagging and abnormal lipid deposits that appear later in life 2,3. It seems likely that many factors contribute to this condition, including melanin deposition, increased vascularity (telangiectatic mats and reticular veins), chronic inflammation/edema, and skin redundancy 4. Many studies reported increased tendency for familial predisposition 5,6.
POM develops with respect to two major components: hemodynamic congestion (possible postinflammatory), where blood flow stagnation appears to be a determinant factor 7, and dermal melanin deposition. Dermal melanosis may be primary (congenital) or secondary to environmental factors such as excessive exposure to sun, exogenous or even unbalanced endogenous estrogen, pregnancy, and breast-feeding 8. The responsiveness of the skin to the noxious actions of different environmental and endogenous factors promotes changes in vascular integrity that lead to the accumulation of fluid, hydrophilic solutes, and hemoglobin chromophores within the tissue space 9. Histamine and the eicosanoids, prostaglandin E2 and leukotriene B4, produced mainly by keratinocytes, have been shown to be the key mediators of these responses through their potent vasodilator and chemotactic actions 10. Other possible causes of POM include the superficial location of vasculature, visible on the lower eyelid and accentuated by hypertransparency of the skin 11, induction by lead in Kohl 12, postinflammatory hyperpigmentation in patients with atopic dermatitis, allergic contact dermatitis, or trauma 13, skin laxity 14, and tear trough depression 15.
Dermoscopy (also known as epiluminescence microscopy, skin surface microscopy, incident-light microscopy, or dermatoscopy) is a noninvasive method that allows the in-vivo evaluation of colors and microstructures of the epidermis, the dermoepidermal junction, and the papillary dermis, which are not visible to the naked eye. These structures are specifically correlated to histologic features 16, thus forming the link between macroscopic clinical dermatology and microscopic dermatopathology 17.
Dermoscopic structures as described by several authors 18–20 are divided into global features, including reticular, globular, cobblestone, homogenous, and multicomponent, and local features, including pigment network, dots, globules, streaks, blotches, and structureless. Other features described include pseudonetwork, fingerprint-like structures, and milia-like cysts.
The aim of the present work was to assess the role of dermoscopy in evaluating cases of POM (vascular-pigmentary patterns), namely assessment of the degree of pigmentation, the presence of edema, and textural changes in addition to presence of erythema and/or telangiectasia.
Patients and methods
The present descriptive study was conducted at the Dermatology Outpatient Clinic of Kasr Al Ainy, Cairo University Hospitals, Egypt, between March 2012 and September 2012. The study was approved by the Dermatology Department Research Ethical Committee of the Faculty of Medicine, Cairo University. Thirty-five patients complaining of infraorbital/periorbital darkening presenting to the Dermatology Outpatient Clinic of Kasr Al Ainy who agreed to participate in the study and signed an informed written consent were included in the study. Inclusion criteria included patients with infraorbital/periorbital darkening, at least 18 years of both sexes, and all educational levels and socioeconomic backgrounds, with no therapy 4 weeks before study. Pregnant and lactating women were excluded from the study.
For all patients, personal and medical history taking was performed, including age, sex, occupation, family history, onset, course and duration of the condition, periorbital pruritus, perioral hyperpigmentation, respiratory allergy, history of previous treatment, history of medical disease, and use of kohl/eyeliner.
We determined the Fitzpatrick skin phototype of the patient. Evaluation of the patients was performed and a series of clinical and dermoscopic photographs (using DermLite II Pro; 3Gen Inc., San Juan Capistrano, California, USA) of the patient and the periorbital area were obtained at the time of consultation. The photographs were independently analyzed by three investigators; results were recorded and average evaluation was noted/or documented. In all cases, two major elements were considered: pigmentation and erythema/telangiectasia.
In an attempt to describe the condition of POM, photographs of patients (clinical and dermoscopic) were assessed using the following criteria:
- Grade of pigmentation (mild, moderate, severe).
- Periorbital edema (absent, present).
- Textural changes (periocular rhytides, skin laxity, dryness) (absent, present).
Photographs were taken from the upper eyelid for ease of exposure and lack of shadow from eyelashes on the lower lid margin and tear trough.
- Description of the different dermoscopic patterns of pigmentation was seen in the periorbital area.
- Presence of erythema and/or telangiectasia was determined.
Grade of pigmentation, presence of periorbital edema, textural changes, presence of pruritus, and presence of erythema were correlated to patients’ personal and medical history. Complete blood count was performed in all patients.
The data were coded and entered in the statistical package SPSS (version16.0; SPSS Inc., Chicago, Illinois, USA). The data were summarized using the mean and SD for continuous quantitative data as well as the percentage for categorical data. Comparison between continuous data of the studied groups was assessed using the t-test when parametric and one-way analysis of variance test when nonparametric, whereas the χ2-test was used for comparison of categorical data. All statistical tests were considered significant at a P value less than 0.05.
Thirty-five patients, 33 (94.3%) females and two (5.7%) males, with periorbital darkening were included in the present study (Table 1).
Six (17.1%) patients were skin phototype III, 21 (60%) were skin phototype IV, and eight (22.9%) were skin phototype V. Three sisters and three siblings (two brothers and a sister) participated in this study. Among participants in the study, the condition initiated at the age of 10 years or thereafter, with 40% developing it before the age of 20 years, 64.3% between 20 and 40 years, and in those above 40 years (5.7%) skin redundancy and periocular rhytides were obvious.
Regarding the degree of pigmentation as revealed in the clinical photographs, 14 (40%) patients showed mild degree of pigmentation, 15 (42.9%) showed moderate degree of pigmentation, and six (17.1%) showed marked degree of pigmentation (Fig. 1). Thirteen (37.1%) patients had periorbital edema and 22 (62.9%) exhibited textural changes (Table 2).
Dermoscopic photographs of patients
Upon analysis of dermoscopic photos, erythema was detected in 33 (94.3%) patients and was associated with telangiectasia (Fig. 2) in 26 (74.3%) patients. Three different dermoscopic patterns of pigmentation were described; the most common was pseudonetwork (45.7%) (Fig. 3), followed by the blotchy pigmentation pattern (Fig. 4), which was seen in 20%, whereas in the remaining 34.3% of patients, multicomponent pigmentation pattern (Fig. 5) was recorded (Fig. 6).
Increased degree of pigmentation in patients was associated with the presence of anemia (P=0.046) (Fig. 7), with higher skin phototype (P=0.046), and increased age of patients (P=0.007), respectively. Occurrence of textural changes of periorbital skin was associated with the presence of pruritus (P=0.007), increased age of patients (P=0.001), and duration of POM (P=0.038).
In the present work, we performed a descriptive study to assess the degree of periorbital darkening, presence of erythema and/or telangiectasia, and presence of periorbital edema and textural changes in patients complaining of periorbital darkening. We aimed to describe the different dermoscopic patterns of pigmentation seen in the periorbital area.
In the present study, 35 patients, 33 (94.3%) female and two (5.7%) male, with periorbital darkening were included. It was observed to be more common in female patients as reported by Aguilera 21. On the basis of the history taking and the presence of two pairs of siblings in the present study, we suggest familial occurrence of POM, and this supports previous studies 5,6. In all, 64.3% of our patients developed POM between the age of 20 and 40 years; similarly, Aguilera 21 stated that POM may be present in individuals from childhood onwards but seems to be more common among adults. In patients above 40 years (5.7%), skin redundancy and periocular rhytides were obvious. Skin laxity, which may be secondary to photoaging, imparts a shadowing appearance on the lower eyelids that results in infraorbital dark circles 14.
Regarding the degree of pigmentation as revealed in the clinical photographs, 14 (40%) patients showed mild degree of pigmentation, 15 (42.9%) showed moderate degree of pigmentation, and six (17.1%) showed marked degree of pigmentation. Thirteen (37.1%) patients had periorbital edema and 22 (62.9%) exhibited textural changes.
Interestingly, we detected that increased degree of pigmentation in patients was associated with the presence of anemia, which has been described to cause redistribution of blood flow where selective vasoconstriction of blood vessels subserving certain areas allows more blood to flow into the critical areas. The main donor sites that sacrifice their aerobic lifestyle are the skin and kidneys 22. Moreover, presence of pruritus was associated with textural changes of periorbital skin. Pruritus leads to excessive eyelid friction, subsequently leading to textural changes and postinflammatory hyperpigmentation 13. In the present work, the degree of pigmentation worsened with aging, which suggest the progressive nature of this condition. POM worsens with skin sagging and abnormal lipid deposits that appear later in life 2,3. Moreover, POM increased with higher skin types (IV, V), which suggest that patients with darker complexions suffer from deeper degree of pigmentation.
Upon analysis of dermoscopic photos, the majority of patients showed a vascular component – erythema in 33 (94.3%) patients associated with telangiectasia in 26 (74.3%) patients. Three different dermoscopic patterns of pigmentation were described; the most common was the pseudonetwork (45.7%), which is defined as a diffuse pigmentation that appears interrupted by multiple round, nonpigmented follicular openings 18. Blotchy pattern caused by a large concentration of melanin pigment localized throughout the epidermis and/or dermis, visually obscuring the underlying structures 19, was seen in 20%, whereas in the remaining 34.3% of patients, multicomponent pigmentation pattern, comprising two or more features, was recorded.
In 2012, Verschoore et al.23 used SIAscopy technique ‘spectrophotometric intracutaneous analysis (SIA)’, a new objective noninvasive method to measure the concentration of melanin in epidermis and of hemoglobin, collagen, and melanin in the papillary dermis. SIAscopy analysis revealed significant differences in the concentration of total melanin, of dermal melanin, and of hemoglobin between POM skin and normal skin of the same patient. The authors confirmed that not only melanin deposits but also blood stasis may play a role in the pathogenesis of POM and cause the darkening of skin under eyes. They also emphasized that SIAscopy is a reliable and useful diagnostic tool for POM. Patients in the present study showed various combinations of the above-mentioned findings, which concur with the study by Verschoore and colleagues who stated that POM does not have a clear etiopathogenesis and was, in other words, multifactorial.
In 2006, Watanabe et al.4 studied periorbital biopsies of 12 Japanese patients with POM, showing that all of them had dermal melanosis in the histology. According to the authors, the melanosis could be interpreted as dermal melanocytosis based on the findings of the anti-S100 protein and Masson-Fontana Silver stainings.
Eumelanin pigment has a brown color. However, on dermoscopy, eumelanin is seen as an array of colors depending primarily on its position in the skin. In addition, other colors are seen on dermoscopy including red (due to vascularity and/or inflammation), white (due to depigmentation and/or scarring), yellow (due to sebaceous material and/or hyperkeratosis), orange (due to serum resulting from erosion or superficial ulceration), and jet black (due to coagulated blood) 24.
The pigment eumelanin is brown. However, on dermoscopy, eumelanin is seen as an array of colors depending primarily on its position in the skin. Thus, eumelanin in the stratum corneum is black, in the remainder of the epidermis and upper cutis is brown, in the papillary dermis is gray, and in the lower papillary and reticular dermis is blue. When melanin is present in large quantity in several layers, the color is black 24.
Roh and Chung 14 stated that infraorbital dark circles are due to the visible prominence of the vasculature contained within the orbicularis oculi muscle rather than subcutaneous vascular plexus. They noted that this condition usually involves the entire lower eyelids, with a violaceous appearance consistent with prominent blood vessels covered by a thin layer of skin. The violaceous appearance is more prominent in the inner aspect of the lower eyelids and is usually accentuated during menstruation. When the lower eyelid skin is manually stretched, the area of relative darkness spreads out without blanching but results in deepening of the violaceous color, which could be used as a useful diagnostic test to confirm the vascularity. This phenomenon seems to result from the underlying vascularity becoming more visible through the skin that has been pulled thin. In addition, prominent periocular veins may lead to the impression of dark circles around the eyes 25.
Ranu et al.26 assessed 200 patients with POM using mexameter, which assesses melanin content and erythema level. They found the most common form to be the vascular type (41.8%), characterized by presence of erythema predominantly involving the inner aspect of the lower eyelids, with prominent capillaries or telangiectasia or the presence of bluish discoloration of the lower eyelid due to visible blue veins, which became more prominent when the overlying skin is stretched. The next most common form (38.6%) was constitutional, which was characterized by the presence of a curved band of brownish to black hyperpigmentation of the lower eyelid skin along the shape of the orbital rim with velvety texture, often involving the upper eyelids. The next common forms were postinflammatory hyperpigmentation and shadow effects due to an overhanging tarsal muscle, eye bags, or a deep tear trough.
We can conclude that POM is a common problem seen in both sexes, more frequently in female individuals, although the number of male individuals included in our study was limited. This could be due to the reluctance to seek medical treatment. Another limitation in this study is the lack of normal controls. Dermoscopic evaluation of periorbital darkening/melanosis appears valuable, particularly in the determination of the degree and pattern of pigmentation as well as the extent of vascular involvement, which in turn would reflect on the choice of therapy. Patients with POM with predominant pigmentation could be treated by topical agents containing hypopigmenting agents such as hydroquinone, vitamin C, arbutin and liquorice extract, chemical peeling, and lasers such as Nd:YAG. For predominantly vascular type of POM, topical vitamin K products and vascular lasers would be more appropriate. More studies are needed to evaluate the use of dermoscopy as a tool to evaluate efficacy of treatment of periorbital darkening.
Large scale studies are needed to disclose different dermoscopic patterns of pigmentation, possibly not described in this work.
The authors are thankful to Professor Mona El Lawindy, Professor of Public Health, Faculty of Medicine, Cairo University, for accomplishing the statistical analysis of this study.
Conflicts of interest
There are no conflicts of interest.
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Keywords:© 2014 Egyptian Women's Dermatologic Society
blotchy; degree of pigmentation; dermoscopy; multicomponent; periorbital darkening; pseudonetwork