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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 5  |  Issue : 1  |  Page : 34-42

A study of epidemiological, etiological, and clinicopathological factors in periocular hyperpigmentation


1 Department of Dermatology, INHS Asvini, Mumbai, India
2 Department of Dermatology, Armed Forces Medical College, Pune, Maharashtra, India
3 Department of Pathology, Base Hospital, Delhi Cantt, New Delhi, India
4 Department of Dermatology, Base Hospital Barrackpore, Kolkata, West Bengal, India

Date of Web Publication29-May-2018

Correspondence Address:
Biju Vasudevan
Base Hospital Barrackpore, Kolkata, West Bengal 700120
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/Pigmentinternational. Pigmentinternational

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  Abstract 


Background: Periocular darkening, popularly known as “dark circles,” is a common condition globally. Pigment deposition, shadowing due to laxity, superficial location of vasculature and prominent nasojugal groove are recognized causative factors. Very few studies exist on its clinicopathological correlation, especially in the Asian population.
Materials and Methods: Eighty-two consecutive patients attending skin outpatient department (OPD) with periocular hyperpigmentation (POH) who agreed to follow the study protocol were included in this descriptive study, conducted in Maharashtra, India. They were evaluated clinically and also investigated with histopathology, special staining and immunohistochemistry of the periocular skin to study the various factors involved in the pathogenesis.
Results: 19.51% of the patients had a positive family history of POH, 90% gave history of exhaustion of periocular muscles, 41.46% had anemia, 8.54% gave history of aggravation during pregnancy and 7.32% had menstrual irregularities. Laxity of skin was present in 82.92% patients, visible veins in 50%, and sunken eyes with prominent infraorbital rim and shadowing in 26.82%. Periocular darkening due to pigment was present in only 17% patients, with mixed dermoepidermal pigmentation being present in majority (70.73%). Clinicopathological concordance was significant in case of dermal pigmentation (Fisher’s exact test P-value <0.05) in contrast to epidermal.
Conclusion: Periocular darkening was predominantly not due to pigment, but rather due to cutaneous laxity and vascular visibility through thin skin. Most of them with pigment had it in the dermis. Clinical dermal pigmentation correlated well with histology, unlike epidermal pigmentation. Iron and amyloid were not significant as etiological factors in our patients.

Keywords: Amyloid, hyperpigmentation, periocular, skin laxity


How to cite this article:
Chatterjee M, Suwal B, Malik A, Vasudevan B. A study of epidemiological, etiological, and clinicopathological factors in periocular hyperpigmentation. Pigment Int 2018;5:34-42

How to cite this URL:
Chatterjee M, Suwal B, Malik A, Vasudevan B. A study of epidemiological, etiological, and clinicopathological factors in periocular hyperpigmentation. Pigment Int [serial online] 2018 [cited 2018 Dec 17];5:34-42. Available from: http://www.pigmentinternational.com/text.asp?2018/5/1/34/233460




  Introduction Top


Periocular hyperpigmentation (POH) popularly known as “dark circles” is a common cosmetological problem in patients presenting to the dermatological outpatient department. Characterized by hyperpigmentation in the periorbital region, it is also referred to as infraorbital darkening, infraorbital skin discolouration and idiopathic cutaneous hyperchromia of the orbital region.[1] Genetic factors are involved in the etiopathogenesis, which is most probably determined by an autosomal dominant gene.[2] It is usually noted below the lower eyelids at the approach of puberty. There is a wide variation in its ultimate extent and intensity. Various other factors have been blamed in the etiopathogenesis namely: dermal melanin deposition, amyloidosis, lichen planus, and postinflammatory hyperpigmentation due to atopic or contact allergic dermatitis among others.[3],[4],[5],[6],[7] Shadowing because of lax skin, superficial location of vasculature and infraorbital depression are the other recognized risk factors.

There are very few studies in literature that have tried to ascertain the causes for POH, especially in the Asian population. Though this condition is not significant from the point of view of morbidity and mortality, it tends to affect the quality of life of patients and their social interactions.[8] This study has been conducted with the aim of looking into the etiopathogenesis and clinicohistopathological profile in patients with POH.


  Materials and methods Top


This study was conducted at a tertiary care hospital.

Inclusion criteria: All the patients of POH attending the skin outpatient department (OPD) during the period between December 2010 and June 2012 and those who were willing to undergo a skin biopsy and all other laboratory investigations. Exclusion criteria were those who were on treatment for the condition to prevent vitiation of clinical and histopathological findings. The final sample size comprised 82 patients. A detailed history including that of drug intake, cosmetic use, and examination for collection of data on risk/aggravating factors and co-morbidities was taken on a standard proforma. Informed consent was obtained. Insitutional Ethical Committee (IEC) approval was obtained. The severity of POH was graded on a scale of 1–3 as follows: mild (grade 1): light brown, moderate (grade 2): dark brown, and severe (grade 3): black. All patients underwent a histopathological examination. Skin biopsy was taken from two sites (one from the affected periocular area and one from postauricular area as “internal control”) to see the difference in the degree of pigmentation. Hematoxylin & Eosin (H&E) stained sections were assessed for increased melanocytes, basal cell degeneration, melanin incontinence, and pigmentation. They were graded based on direct eyeballing assessment of the pathologist. It was correlated with immunohistochemistry of Melan-A and Tyrosinase stained sections. In addition, Perl’s and Congo Red stain tests were conducted to detect hemosiderin and amyloid, respectively.

Laboratory investigations including a complete blood count, peripheral blood smear (PBS), blood sugar, liver function test, and thyroid hormones were performed to find any associations. World Health Organization’s hemoglobin thresholds were used to define anemia. In non-pregnant women (>15 years), hemoglobin levels below 12 mg/dl were taken as anemia, while in men (>15 years), hemoglobin levels below 13 mg/dl was taken as anemia.

The findings were recorded on a standard proforma. Data were reported in accordance with standard statistical methods, and Fisher’s exact test was performed to evaluate the correlation between clinical and histopathological parameters.


  Results Top


Incidence of periocular hyperpigmentation

Out of 12,540 patients attending the skin OPD during the period of study, 3762 patients had POH, giving an incidence of 30%. Out of this subset, 2257 (60%) patients were female, and 1505 (40%) patients were male. Eighty-two patients fulfilled the inclusion criteria for the study. All the 82 patients included in the study gave history of gradual onset of the POH increasing gradually over a number of years.

Epidemiological factors

Of the 82 patients included in our study, 66 were women and 16 were men. The age of patients presenting with POH ranged from 17 to 67 years. The mean age of onset was 31.96 years. Most patients belonged to the 21–30 years age group (40.2%). Mean duration of presence of POH was 5.34 years. Majority of the patients were housewives (n = 51), followed by students (n = 21), while two were businessmen, seven were security guards and one was a teacher.

Risk factors

Nineteen patients gave a history of preceding excessive sun exposure and aggravation of POH by sunlight. Reduced hours of sleep was present in seven patients for prolonged durations. Sixty-seven (81.70%) out of 82 patients gave history of exhaustion to eyes, that is, inadequate rest to eyes. Sleeping for 6 h or less daily, studying for long hours, working on computers till late night, watching television or using mobiles for prolonged hours, were among the most common cause of inadequate rest to the eyes. Family history was present in 16 patients with POH; 10 of these 16 patients reported that their siblings also had POH while in six of them their mothers had similar dark circles. Seven women patients included in the study gave history that the dark circles began or were aggravated by pregnancy. Six female patients had menstrual irregularities. One patient had hypothyroidism prior to the development of POH. Two patients in addition to POH had Riehl-like melanosis of the other parts of the face as a consequence of applying fairness creams for a prolonged duration. One of our female patients in the study was on oral contraceptives (OCP), and she gave history that the POH had started six months after she began the intake of OCP’s. One of the patients, a male, developed telangiectasia in the periocular area as a result of applying topical steroids for more than 6 months.

Morphological findings

Clinically, 24 patients (29.26%) were classified as Grade I (light brown), 37 patients (45.12%) as Grade II (brown/dark brown color) and 21 patients (25.60%) as Grade III (black color) of periocular skin [[Figure 1]a, [Figure 1]b and [Figure 1]c, respectively]. In 12 patients, POH was not limited to the periocular area and extended to the cheeks. The patients had a linear extension of their hyperpigmentation of lower eyelids extending from the medial aspect of the eye along the nasojugal groove (a dividing line between the lower eyelid and cheek) toward the malar area and thus could be differentiated from the pigmentary demarcation lines.
Figure 1: Grades of severity of periocular pigmentation: (a) grade 1, (b) grade 2, and (c) grade 3

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Etiological factors

Concomitant presence of laxity of skin, visible veins and sunken eyes as assessed by stretch test is as given in [Table 1] [[Figure 2] and [Figure 3]]. Three patients had features of concomitant eyelid eczema, though they were not atopic.
Table 1: Etiological factors in periorbital hyperpigmentation

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Figure 2: Tear trough deformity

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Figure 3: (a) Laxity of skin, (b) sunken eyes, and (c) visible veins

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Associated conditions

Telangiectasia was present in two patients. Of the two patients, one was male and another female. The female patient with telangiectasia also had telangiectasia over V area of neck and upper chest and was diagnosed as a case of benign essential telangiectasia. The male patient had telangiectasia secondary to long-term steroid use (0.05% clobetasolpropionate cream). Twelve patients had concomitant melasma. Of the 12 patients with melasma, 11 were women and one was a male patient. Out of the 12 patients with melasma, three also had POH extending to cheeks along the nasojugal groove toward the malar area [Figure 4]. Freckles and lentigenes were also found in 11 patients.
Figure 4: Nasojugal pigmentation

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Investigations

Histopathology from affected periocular area

The grading of histopathological examination (HPE) changes by HPE, Melan-A and Tyrosinase was performed based on eyeballing in terms of visual analog scale in the standard measure (1-3 mild, 4-7 moderate and 8–10 severe) by a single histopathologist for the entire set of slides as no previous grading for the same is available [[Figure 5]a&[Figure 5]b, [Figure 5]c&[Figure 5]d, and [Figure 5]e&[Figure 5]f, respectively]. The correlation between clinical grading and corresponding histopathological findings of epidermis and dermis are summarized in Tables 2 and 3, respectively [Figure 6][Figure 7][Figure 8]. Biopsy of 46 patients also showed perivascular and periappendageal chronic inflammation. Additional findings included detection of increased melanocyte number in one patient and absence of basal cell degeneration in all of the biopsied tissues. Congo Red and Perl’s staining of the tissues of all patients was negative.
Figure 5: Staining of dermal pigmentation reveals: (a) mild pigmentation − H&E stain, (b) corresponding mild pigmentation on Melan-A stain, (c) moderate pigmentation − H&E stain, (d) corresponding moderate pigmentation on Melan-A stain, (e) severe pigmentation − H&E stain, and (f) corresponding severe pigmentation on Melan-A stain (all 40×)

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Table 3: Concordance between clinical grading and corresponding histopathological finding of dermis

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Figure 6: Clinicopathological correlation in mild pigmentation

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Figure 7: Clinicopathological correlation in moderate pigmentation

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Figure 8: Clinicopathological correlation in severe pigmentation

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Biopsies from control sites (postauricular region) in two patients showed variance from normal histopathological findings. One of the patient’s biopsies revealed mild increase in melanin pigment in basal layer, while the periocular area in the same patient showed mild melanin incontinence. Clinically, this patient had postinflammatory hyperpigmentation. The other control site abnormal biopsy showed mild melanin incontinence. The histopathology report from periocular skin of this patient revealed severe melanin incontinence, mild increase in pigmentation of the basal layer and severe dermal pigmentation. Clinically this patient had Riehl-like melanosis.

Lab investigations

Thirty-four out of 82 patients had hemoglobin levels lesser than normal range. Twenty-nine out of 34 patients with anemia were women and five were male patients. PBS was tested, which revealed iron deficiency anemia as the cause in all 34 patients with anemia. One of the female patients in our study was a case of hypothyroidism since 3 years. She was on regular medication since onset. However, her thyroid function test was within normal limits during the study. All the other laboratory investigations were within normal limits for all patients.


  Discussion Top


Most patients of POH in our study belonged to the 21–30 years age group (40.2%) probably due to increased cosmetic awareness among them. The mean duration of POH in the 82 study patients was 5.34 years (range: 1–28 years). While 70 patients in our study had periorbital hyperpigmentation for less than 10 years, 12 patients had it for more than 10 years, though the latter group did not show increased extent of pigmentation. In our study, more women were affected with dark circles. Few studies in literature have shown that incidence ratio between females and males was 1:1, while some have shown preponderance in females as compared to men.[9],[10]

People from diverse backgrounds and occupations were affected namely housewives, working men and women, security guards, and students. It seems probable that when exposed to similar factors and environment, any individual is susceptible to developing POH. Also, more than occupation per se, circumstances that predispose patients to increased light and sun exposure and exhaustion of periocular muscles seem to play a role in the development of dark circles. The housewives gave history of having to walk to drop and pick up children from school, collection of milk and daytime sun exposure during shopping, housework (putting clothes to dry, etc.) leading to their increased exposure. A similar higher incidence in housewives has been reported by Sheth et al.[11]

In our study, 16 (19.51%) patients had positive family history. In few studies, a familial character with dominant autosomal inheritance and variable expression of the genes has been mentioned.[12],[13] Positive family history with similar incidence has been reported by many workers.[14]

Significantly, 67 (81.70%) of the patients included in the study gave history of exhaustion of eyes, that is, inadequate rest to eye in the form of staying up late either watching television, studying, using computers or mobiles for long hours, or night duty in case of guards, etc. All 67 patients gave history of sleeping for 6 h or less per day. There are few previous reports that have mentioned exhaustion of periocular muscles as a cause of dark circles.[12],[14]

With regards to sun exposure, 19 (23.9%) of our patients gave history of excessive sun exposure prior to onset of POH, blaming it for the pigmentation. Patients gave history of 10–56 h of sun exposure per week. Most of the students gave history of sun exposure while commuting to and from college. Guards attributed the nature of their job to excessive sun exposure, for example, guard duty during the day (8 h/day).

We also sought to investigate the hormonal factors as a possible cause of dark circles: out of 66 women in our study, seven gave the history of aggravation of dark circles during pregnancy. One of the patients in our study was on treatment for hypothyroidism during the duration of the study. There are previous studies, which show increased incidence of dark circles in females due to hormones and also citing hormones as causative agents.[15],[16] However, a study conducted by Sarkar, to the contrary, did not find any correlation between periorbital hyperpigmentation and hormones.[17] One female patient also gave history of use of OCP pills preceding onset of POH. Some other drugs apart from OCPs that have been linked to dark circles in the available literature are psoralen, minocycline, anti-psychotics, NSAIDs, gold, and chemotherapy.[18] We did not find any correlation with drug intake or application in the remaining 81 patients.

Two of our patients (one male and one female) were diagnosed as cases of Riehl-like melanosis. Both patients gave history of application of fairness cream for a prolonged period prior to onset of pigmentation. Some of the components of fairness creams applied over a prolonged duration could have led to increased pigmentation and needs to be used with caution. We did not find any literature incriminating cosmetic products as a cause of dark circles.

Among other risk factors, melasma as a co-morbidity was evaluated. Out of the 12 patients with concomitant melasma, three also had periocular pigmentation extending to cheeks along the nasojugal groove. A study by Aguilera also makes similar observation and mentions of POH extending from the eye to the cheekbone and halfway down the sides of the nose root. Concomitant presence of conditions such as melasma, freckles and lentigenes, which are primarily photo aggravated, may indicate toward sunlight exposure being an important aggravating factor in the etiology of periorbital hyperpigmentation.

Three patients had eyelid dermatitis and gave history of itching and scratching of the region. All three patients were female, and clinically all three patients had concomitant laxity of skin and visible veins. A report by Gendler denotes itchy and irritating skin conditions like atopic dermatitis and contact dermatitis as causes of POH.[4] However, none of the patients in our study gave history of atopic dermatitis.

As probable etiological factors, skin laxity, visible superficial veins, sunken eyes/shadowing and dark circles due to pigment were also evaluated. Laxity of skin, visible veins and sunken eyes were present in significant proportion of patients included in our study. So, these could be important causes or contributory factors in increasing the appearance of dark circles. These have been shown to be aggravating factors in few other studies too.[19],[20],[21] Vascular, constitutional, postinflammatory hyperpigmentation and shadow effects were found to be the main etiological factors in a pan Asian study by Ranu et al.[22] Histopathological findings revealed that purely epidermal pigmentation was present in only one patient. Purely dermal pigmentation in the form of melanin incontinence with normal epidermis and normal basal layer pigmentation was present in 23 patients. However, most patients (58 of the 82 patients) had both epidermal and dermal pigmentation. Immunohistochemistry (IHC) and H&E staining of the epidermis revealed that POH predominantly has a dermal pigmentation component and hence, most epidermal pigment removal modalities may not work for majority of these cases. Few other studies also revealed similar picture wherein dermal melanosis and melanocytes was found to be more contributory to the development of dark circles.[3],[16],[21]

Perl’s stain was tested in all biopsied skin to differentiate pigmentation due to melanin from hemosiderin deposition. Perl’s stain was negative in all cases. So, we can infer that pigmentation evident in all our cases with hyperpigmentation either in epidermis, dermis or both were due to melanin and not hemosiderin (iron). Congo Red was negative for all, thereby ruling out amyloid as a cause of POH in the 82 patients included in our study. Melanin incontinence was present in 73 patients, of whom 44 had mild melanin incontinence, 21 had moderate melanin incontinence whereas eight had severe melanin incontinence.

On analysis, it was found that there was no difference in the degree of staining with H&E or immunohistochemistry with either Melan-A or Tyrosinase. All three stains could equally detect the degree and location of pigment. So, in centers where IHC may not be available, only H&E may be performed to ascertain the degree and location of hyperpigmentation in the biopsied skin. The added benefit of IHC compared to H&E could be to confirm whether the pigmentation seen is due to melanin containing cells or otherwise.

Concordance between clinical grading and H&E, Melan-A and Tyrosinase staining of epidermis was analyzed using Fisher’s exact test. There was no significant association between clinical grading of POH and histopathological analysis of epidermal pigmentation, but there was a significant association between clinical grading of POH and dermal pigment as revealed by the three stains. Hence, clinical impression correlates well only with dermal pigment. So, clinical impression is enough to diagnose dermal pigmentation, and a biopsy may not be required. However, if the pigment is clinically epidermal, then histopathological correlation is required since a number of these may histopathologically turn out to be dermal and hence, therapy directed at epidermal pigment may not work. Another interesting finding in our study was the presence of perivascular and periappendageal chronic inflammation in 46 patients. This indicates that topical non-steroidal anti-inflammatory agents may probably have a role to play in the management of some of these cases.

Only two patients had abnormal histopathology in the control sites, to emphasize the fact that the pathology was localized to the periocular area in the other patients. Both these patients had milder variants of periocular findings in the control site postauricular, most probably due to the same etiology (postinflammatory in one and Riehl-like melanosis in the other) causing the findings in these two patients due to the involvement of the area postauricular by extension from the face.

As most of our patients also had laxity of skin, visible veins, sunken eyes/shadowing and dark circles due to pigment, we suggest that treatment modality aimed at the cause of POH would yield better results. Since this paper is not aimed at a detailed discussion on therapy, the same would not be detailed here.


  Conclusion Top


Periocular darkening is predominantly not due to pigment, but rather due to cutaneous laxity and vascular visibility through thin skin. Excessive sun exposure, positive family history, anemia, and exhaustion of periorbital muscles are important risk factors. Most of the pigmentation is dermal and will, therefore, be difficult to treat. Clinical dermal pigmentation correlates well with histology, unlike epidermal pigmentation. Hemosiderin deposition and amyloidosis are not very significant etiological factors in such patients.

Limitations

The fact that this is a descriptive study without a control group is its main limitation. However, internal control in each patient helped us to overcome this limitation to a certain extent.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Acknowledgements

This study has been possible by the IADVL-L’Oreal Research Grant.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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