The Prevalence of Ocular Manifestations in the Various Types of Common Skin Disorders at Tertiary Hospital in Ahmedabad, India

Aim The article aims to study the prevalence and ocular manifestations of the various types of common skin disorders at a tertiary hospital in Ahmedabad, India. Materials and methods Five hundred patients were studied in the ophthalmology department from September 2017 to September 2019. Results Out of the 500 patients that were included in our study, 312 were males, and 188 were females. In our study, lid involvement was seen most commonly in patients with herpes zoster ophthalmicus (HZO). Plexiform neurofibroma was seen in eight (14.5%) patients with neurofibromatosis (NF). Cicatricial ectropion was found in half of the patients with ichthyosis. Lagophthalmos was present in 10 (20.4%) patients with leprosy. Conjunctivitis was seen commonly in HZO patients. Papillary conjunctivitis was seen in half of the atopic dermatitis cases. Steven Johnson's syndrome (SJS) was associated with pseudomembranous conjunctivitis. Conjunctival xerosis was seen only in patients with Sjogren's syndrome. The cornea was most commonly involved in patients of HZO. Decreased corneal sensation was seen in leprosy and HZO. Lisch nodules were seen in NF cases. Anterior uveitis was found in seven (6.3%) patients with HZO. Glaucoma was seen most commonly in patients with Sturge Weber syndrome (SWS), followed by leprosy. Facial nerve palsy was seen in patients with leprosy. Episcleritis was seen in patients with leprosy and SWS. Conclusion We conclude that ocular involvement in skin disease is a common feature and could be a major component of the development of various systemic skin disorders.


Introduction
Dermatology disorders can have numerous ocular manifestations. Common dermatological disorders can manifest with mild to severe ocular manifestations that can result in ocular damage, and sometimes it can even cause vision loss. Dermatology patients are prescribed long-term medications like steroids, hydroxychloroquine, retinoic acid, immunosuppressive agent, which can cause indirect side effects on the eyes and is one of the leading causes of ocular manifestations in dermatology patients. So thorough examination, ophthalmological referral, and long-term follow-up of dermatology patients are paramount important. The early detection of the clinical relationship between ocular manifestations and dermatological disease is important for the proper management of the patient because many dermatology diseases can manifest initially with ocular findings. In our study, we included the most common and significant ocular manifestations in major dermatological diseases, which should be studied and analyzed for further understanding and management of the patients.
Herpes zoster ophthalmicus (HZO) is characterized by an eruption of multiple vesicles strictly on one side of the face along with the distribution of the ophthalmic division of the trigeminal nerve, preceded by severe neuralgia and constitutional symptoms. HZO is caused by the varicella-zoster virus, which reactivated from its dormant status in the dorsal ganglion cells of the central nervous system [1]. An endogenous reactivation of latent virus occurs in elderly persons. Mild cases of HZO may develop conjunctivitis, superficial punctate keratitis, and subepithelial infiltrates, while severe cases include sclerokeratitis, interstitial keratitis, and neurotrophic keratopathy.
Herpes simplex virus (HSV) type 1 causes ocular manifestations like herpes keratitis, stromal keratitis, iridocyclitis, and acute retinal necrosis in older patients leading to visual impairment. Conventionally, the diagnosis of HSV keratitis is based on a history of recurrent keratitis, as well as typical clinical manifestations in the infected eye [2]. Primary herpetic infection is found in non-immune persons. The primary infection may take a mild or a fatal course if encephalitis develops. The disease may cause mild fever, malaise, and non-suppurative preauricular lymphadenopathy. The infection remains subclinical in affected persons. Reactivation of the virus occurs following poor general body resistance in conditions like debilitating diseases, stress, use of corticosteroids and immunosuppressive agents. In Toma et al. study, HSV-1 DNA was found in 93% of human trigeminal ganglia [3].
Ocular rosacea is a chronic inflammatory condition that affects the skin and oil glands. Meibomian glands in the eyelid, which produce the oil component of the tear film, are affected in rosacea. Ocular manifestations include chronic red eyes, styes, chalazia, and severe photophobia. Patients can develop infiltrative marginal keratitis and scarring of the cornea. It involves more than 50% of patients with dermatology diseases [4]. Neurofibromatosis (NF) is a type of phacomatosis with a genetic abnormality that affects neural tissue growth and affects the nervous system, skin, eyes, and other organs. Genetic abnormalities are either passed on by parents or occur spontaneously at conception. NF is divided into two primary subgroups: type 1 (NF1) peripheral neurofibromatosis and type 2 (NF2) central neurofibromatosis. Eyelid neurofibroma is a type of phacomatosis where progressively fast-growing lid tumor tends to develop early in younger age groups, obscures the visual axis, and eventually affects the vision of the patient.
Leprosy or Hansen's disease is a chronic infectious disease caused by an intracellular rod-shaped acid-fast bacilli Mycobacterium leprae which affects the skin, nasal mucosa, peripheral nerves, and the anterior segment of the eye [5]. Ocular manifestations include cataract, lagophthalmos, reduced corneal sensations, exposure keratopathy, and uveitis. A corneal ulcer may occur due to an acute microbial infection or as a secondary infection in exposure keratitis.
Psoriasis is an uncommon disease that often involves the eye. It affects males and females equally [6]. Skin can present with persistent scaly plaques, flaking, itch, and pain. The ocular manifestations include conjunctivitis, chronic blepharitis, keratitis, trichiasis, symblepharon, anterior uveitis, and retinal vasculitis. Uveitis in psoriasis patients is chronic, a bilateral condition found in older age groups, while human leukocyte antigen B27 (HLA B27) anterior uveitis is unilateral with potent posterior ocular involvement. Prolonged courses of systemic corticosteroids for psoriasis management may cause posterior subcapsular cataracts.
This article aims to study the prevalence of ocular manifestations in different types of dermatology diseases at a general hospital in Ahmedabad, India.

Materials And Methods
Our study is an observational retrospective study carried out on patients with dermatological diseases who were presented to the ophthalmology department in a tertiary hospital from September 2017 to September 2019. Patients were treated with comprehensive combined care with the dermatology department. We obtained approval from the Institutional Review Board of AMC MET Medical College, affiliated with Gujarat University, and written consent from the 500 patients with dermatology diseases with ocular manifestations we studied. Patients, who were unwilling to participate in the study and patients suffering from any mental, neurological, or debilitating illness, which hampers examination, were excluded from the study. Age, sex, and type of skin disease were noted. Patients having skin disease were examined clinically to rule out any associated ocular condition. After consulting with the dermatology department, all dermatological findings and treatments were noted. The past history of the patient was recorded, including any medications for skin disease and the duration of a particular disease. Best-corrected visual acuity of the patient was taken by Snellen's chart. Intraocular pressure of both eyes was measured in all indicated patients. In any cases of corneal epithelial defects or corneal erosions, corneal staining was done by using 2% fluorescein strips. In all cases of dry eyes, we have done Schirmer's test for five minutes using Whatman® number 41 filter paper. Those patients who are suspected of having glaucoma were sent for investigations like perimetry and optical coherence tomography. If needed, radiological investigations like X-ray orbit, magnetic resonance imaging, and computed tomography scan were done. The number of patients with a particular disease having specific ophthalmic manifestations was calculated and analyzed.
Of 111 patients with HZO, 60 (54.05%) patients were males, and 51 (45.9%) were females, with a male to female ratio of 1.17:1. A similar finding was seen in the study by Dubey et al. in South India, where the male to female ratio was l.84:1 [7]. Sehgal et al. also noted that males are affected more than females [7][8][9]. In our study, the commonest age group of presentation among the patients with HZO was 51-60 years. HZO was most commonly seen in elder age groups: 52 (46.8%) patients from the 51-60 age group and 55 (49.5%) from the 61-70 age group. Sehgal et al. found a high incidence in the fourth and fifth decades [8]. In our study, the most common lid manifestations were vesicles seen in 91 (81.9%) patients and scarring seen in 10 (9.0%) patients with HZO, similarly to the study conducted by Nigran et al. [9]. In our study, anterior uveitis was seen in seven (6.3%) patients with HZO. Herpetic anterior uveitis was the most common cause of viral anterior uveitis accounting for 5-10% of all uveitis cases in the western world and 0.9-8.3% of all infectious uveitis in India [10].
A total of the 60 patients had the herpes simplex virus; 40 (66.6%) patients were males, and 20 (33.3%) patients were females giving a male to female ratio of 2:1. A study conducted by Kaul et al. in North India estimated the incidence of HSV1 as 33.3% [11], while in our study, the incidence of HSV1 was 12.0%. In our study, epithelial keratitis was seen in 10 (16.6%) patients with HSV, which corresponds with the Fukuda et al. study reporting the highest number of copies of HSV-DNA in herpetic epithelial keratitis, followed by active stromal keratitis and persistent epithelial defect. Their detection rate was higher at 88.1% for epithelial keratitis and 59.1% for stromal keratitis [12].
Ocular rosacea was seen in more than half of the patients with dermatology disease, indicating a high prevalence rate of ocular manifestation [14]. Rosacea most commonly affects middle-aged adults [15]. The mean age in our study was found to be 25 years. Lid inflammation and oil gland dysfunction are common findings in patients with ocular rosacea leading to dry eye [16].
A total of the 55 patients had neurofibromatosis; 37 (67.27%) were males, and 18 (37.2%) were females. This corresponds with the study conducted by Odebode et al., in which there was a definite male predominance, affecting 60 males and 38 females with a total of 98 patients [17]. The commonest age group with 45 (81.8%) patients presented to us was between 20-40 years. In our study, eight (14.5%) of the 55 patients with neurofibromatosis had plexiform neurofibroma, while lisch nodules were the commonest manifestation present in 41 (74.5%) patients [18].
A total of the 35 patients with psoriasis, 25 (71.4%) patients were males, and 10 (28.5%) were females giving a male to female ratio of 2.5:1. There is a slight male predominance, probably due to better access of male patients to healthcare services in our country. This finding is similar to the study reported earlier [23]. Among the 35 patients with psoriasis, in our study, we found conjunctivitis to be the most common manifestation seen in 12 (34.2%) patients. Seven (20%) patients had chronic anterior uveitis. Catsaru-Catsari et al. found that blepharoconjunctivitis was the most common ocular manifestation of psoriasis [24].

Conclusions
In our study, the most common skin diseases associated with ophthalmic manifestations were herpes zoster ophthalmicus, herpes simplex virus, ocular rosacea, neurofibromatosis, leprosy, and psoriasis. Viral skin diseases are most commonly associated with ocular manifestations. Viral skin diseases are common and potentially devastating diseases that demonstrate significant ophthalmic morbidity if not adequately diagnosed and treated.
The majority of the ocular manifestations are seen in the anterior segment of the eye. Among phakomatosis, neurofibromatosis is associated with lisch nodules and plexiform neurofibromas. Meticulous slit-lamp examination for the presence of lisch nodule is a simple, non-invasive, inexpensive method of diagnosing neurofibromatosis accurately. As the majority of dermatological diseases are associated with ocular features, complete ocular evaluation is necessary for every patient with dermatological disease.