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BRIEF COMMUNICATION
Year : 2017  |  Volume : 5  |  Issue : 1  |  Page : 35-38

Study of surface ocular tumours and its association with human immunodeficiency virus infection


Department of Ophthalmology, B. J. Medical College and Sassoon General Hospital, Pune, Maharashtra, India

Date of Submission22-Apr-2015
Date of Acceptance18-Apr-2016
Date of Web Publication6-Dec-2016

Correspondence Address:
Ranjana Pande
B 402, Felicita, Baner Pashan Link Road, Baner, Pune - 411 045, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2320-3897.195307

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  Abstract 

A retrospective analysis of 30 patients who were referred to our hospital (A tertiary referral center in Maharashtra) was done. Mass excisional biopsy for histopathology and screening for human immunodeficiency virus (HIV) of all 30 patients was done from 2010 to 2013. The data were analyzed, and the correlation between HIV status and surface ocular tumors was done. Thirty patients were enrolled. There were 17 males and 13 females giving an overall male:female ratio of 1.31:1. On the other hand, the ratio of male:female in the HIV-positive patients was 1.71:1. Their ages ranged from 22 to 74 years with a mean age of 39.7 years. Twenty-two patients were positive while eight patients were negative for the HIV. The CD4 counts of the patients varied from 58 cells/μl to 88 cells/μl with the median count of 70 cells/μl among those who were HIV-positive. Histopathological study showed ocular surface squamous neoplasia (OSSN) in 23 patients, i.e. 77% cases, sebaceous cell carcinoma in 4 cases, i.e. 13% cases, basal cell carcinoma in 2 cases, i.e. 7% cases, and nevus in 1 case, i.e. 3% cases. Among those who were HIV positive, the histopathology showed OSSN in 19 i.e. 86% cases, sebaceous cell carcinoma in 2 i.e. 9% cases, and basal cell carcinoma in 1 i.e. 4.5% cases. This study shows that OSSN is the most frequent surface ocular tumor and majority of HIV-positive patients with tumors are young and have less CD4 count.

Keywords: Human immunodeficiency virus, ocular surface squamous neoplasia, surface ocular tumors


How to cite this article:
Pande R, Joshi M. Study of surface ocular tumours and its association with human immunodeficiency virus infection. J Clin Ophthalmol Res 2017;5:35-8

How to cite this URL:
Pande R, Joshi M. Study of surface ocular tumours and its association with human immunodeficiency virus infection. J Clin Ophthalmol Res [serial online] 2017 [cited 2022 Jun 27];5:35-8. Available from: https://www.jcor.in/text.asp?2017/5/1/35/195307

India has seen the development of a pandemic of human immunodeficiency virus (HIV) infection in the past one decade. There has also been an increase in surface ocular tumors, and its incidence is collinear with the increase in HIV. Other causes that have led to ocular tumors in the past are factors such as advanced age, [1] male sex, [1],[2],[3] ultraviolet light B rays, [3],[4],[5] mutation of the p53 tumor suppressor gene, immunosuppression in organ transplant recipients, cigarette smoking and in some settings, and HPV infection. [6],[7],[8] Before HIV pandemic, surface ocular tumors such as ocular surface squamous neoplasia (OSSN) were not very common and noted to occur predominantly in the elderly for whom it was the third most common oculo orbital tumor after melanoma and lymphoma. However, the incidence of these tumors has increased tremendously in the present scenario. Spitzer et al. have shown that the OSSN is a marker for HIV infection in Malawi. [9]

The purpose of the study was to find a relation between surface ocular tumors and HIV infection.


  Materials and Methods Top


This was a retrospective study. The study population comprised all patients whom we diagnosed with ocular surface tumor who came to the ophthalmological outpatient department of our institution during 3 years, i.e., from May 2010 to May 2013. Our hospital being a tertiary referral center has patients who are referred to us from the western parts of Maharashtra. It is also a government referral center for patients with HIV and tuberculosis from the neighbouring districts. The prevalence of HIV in Maharashtra is 0.55% out of which more than half the cases are found in the western regions of the state.

Details such as age, sex, symptoms, and duration of symptoms of all patients were noted. Complete ophthalmological examination of all patients was carried out which included vision, slit lamp examination, intraocular pressure, fundus examination, oculomotor examination, and ultrasound biomicroscopy with 35 Hz probe was done to see the extent to which the tumor had spread and all structures that were involved due to the tumor.

Blood investigations of the patients were done. All routine tests such as hemoglobin, serum creatinine, urea, electrolytes, blood sugar, and testing for HIV were carried out. The retrovirus testing was done by the enzyme-linked immunosorbent assay method. Two tests were carried out with the second test taken as confirmatory. Those patients who were found to be negative were subjected to the HIV test again after 6 months.

In those patients who were found to be HIV positive, the blood CD4 counts were also done in the hospital laboratory.

The patients were then scheduled in the operation theater for an excisional biopsy. The specimen collected was kept in a formalin bulb and was immediately transported to the pathology laboratory where the tissue was fixed and after making a wax block, sections were made, and then stained and microscopic examination was carried out to detect the presence of any abnormal cells in the section.

All patients were subsequently subjected to the surgical excision of the tumor and followed up to note any recurrences for the same.


  Results Top


Thirty patients were enrolled. One eye of each patient was included in the study. There were 17 males and 13 females giving an overall male:female ratio of 1.31:1. On the other hand, the ratio of male:female in the HIV-positive patients was 1.71:1.

Their ages ranged from 22 to 74 years with a mean age of 39.7 years (2 standard deviation: 27.07-52.33) as shown in [Graph 1].



Twenty-two patients were positive while eight patients were negative for the HIV. The CD4 counts of the patients varied from 58 cells/μl to 88 cells/μl with the median count of 70 cells/μl among those who were HIV-positive.

The main presenting symptom was a growth in the presenting eye in 30 patients with average duration of around 1 year. The other presenting complaints were ocular pain in 12 patients, redness in 8 patients, decreased vision in 4 patients, and itching with tearing in the eye in 2 patients.

A total of twenty-three eyes in thirty patients had histological confirmation of squamous cell carcinoma.

[Figure 1] and [Figure 2] show OSSN in a couple of the patients.
Figure 1: Photograph of a patient who had ocular surface squamous neoplasia

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Figure 2: Another patient who was found on histopathology to have ocular surface squamous neoplasia

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Histopathological study showed OSSN in 23 patients, i.e., 77% cases, sebaceous cell carcinoma in 4 cases, i.e., 13% cases, basal cell carcinoma in 2 cases, i.e., 7% cases, and nevus in 1 case, i.e., 3% cases as in [Graph 2].



Among those who were HIV-positive, the histopathology showed OSSN in 19 i.e. 86% cases, sebaceous cell carcinoma in 2 i.e., 9% cases, and basal cell carcinoma in 1 i.e., 4.5% cases.


  Discussion Top


OSSN is found to be the most common surface ocular tumor in HIV patients.

In this study, the mean age of the patients presenting with this condition was 39.7 years (2 standard deviations: 27.07-52.33). This is lower than the mean ages of 45 years reported by Olurin et al. and 42 years reported by Ukponmwan et al. This may indicate a changing pattern in the presentation of the disease with a steady decrease in the age at presentation due to other modifying factors. However, it still falls within the period where it is found to be more common which is between the fourth and sixth decade. [1]

There is a male preponderance with male to female ratio of 1.31:1. The ratio is even higher in case of the HIV-positive patients (1.71:1). This is in accordance to other studies that have been done. [1],[2],[3]

The male preponderance is linked to their occupational exposure to sunlight. [3],[4],[5]

The prevalence of HIV seropositivity in this study was 73%. In Uganda, a study done found a prevalence of 71% while in Malawi, this was 86%. A case-control study in Rwanda also demonstrated that HIV infection is a risk factor for the development of squamous cell dysplasia and neoplasia of the conjunctiva. All studies included patients who presented in the ophthalmological outpatient department with conjunctival growth who were then scheduled for biopsy after due consent. Spitzer et al. have shown that the OSSN is a marker for HIV infection in Malawi.

These findings are all similar and suggest a strong association between HIV and squamous cell carcinoma of the conjunctiva. [10],[11],[12]

Recent studies in Africa have shown that the incidence of OSSN is on the rise in HIV-positive individuals. [13]

There is the presence of multiple tumor viruses detected in OSSN tissues. Infection with HIV resulting in immunosuppression may eventually tilt the balance in favor of the tumor viruses, leading to an increased the risk of cancer in the immune compromised individuals. The localization of these oncogenic proteins in the OSSN tissues shows an association; however, the establishment of a causal effect by any of the viruses, or a multiple of the viruses in an HIV atmosphere has yet to be fully confirmed.

Nakamura et al. suggested that human papilloma virus (HPV) probably does not act alone in initiating ocular neoplasia, but that other factors including the ultraviolet light were involved. [6]

The selection pressure that may exist as a consequence of competition between opportunistic infections may further lead to mutations occurring in the HPV types as well as the other infectious agents. In situ hybridization and immunohistochemistry studies showed that in the invasive OSSN tissues, the viruses were localized in similar tissue sections. Some of the viral genomes are likely to be integrated by their punctate signals and episomal viral DNA by their diffuse signal throughout the nucleus. [8]

Previous reports have suggested that infection with more than one HPV type enhances cervical cancer and oral squamous carcinoma. [7]

In tropical countries, secondary immunodeficiency attributable to chronic inflammation caused by parasitic or viral infections might contribute to tumor genesis. The high frequency of coinfection of human papilloma virus, ebstein bar virus, cytomegalovirus, and HIV in the OSSN patients may be a result of cooperative and complementary interactions of the viruses. In addition, we suggest that the disease might be more aggressive in HIV patients due to their immune dysfunction, abnormal cytokine, and chemokine expression, growth factor production, and exposure to ultraviolet rays.

In this study, squamous cell carcinoma of the conjunctiva has been shown to be a marker of HIV seropositivity or AIDS in patients. It is suggested that all patients presenting with squamous cell carcinoma in India should be tested for HIV seropositivity. [14]

The study is one of the pioneer studies on ocular surface tumors and seeing their relation to HIV infection. The study has however been done on a small group of patients, and additional studies need to be done on a larger group of patients. The study has not shown any correlation between OSSN in tissues and various viruses in its causation due to the limitation of the resources available to us. Therefore, more studies are clearly needed to fully establish a role for these viruses in OSSN.


  Conclusions Top


OSSN is the most frequent surface ocular tumor and majority of HIV-positive patients with tumors are young and have less CD4 count.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Ukponmwan CU, Igbokwe UO, Aligbe JU. Squamous cell carcinoma of the conjunctiva in Benin City, Nigeria. Niger J Clin Pract 2002;5:143-7.  Back to cited text no. 1
    
2.
Abiose A, Adido J. Invasive squamous cell carcinoma of the conjunctiva in Kaduna. Niger J Ophthalmol 1986;2:34-9.  Back to cited text no. 2
    
3.
Tunc M, Char DH, Crawford B, Miller T. Intraepithelial and invasive squamous cell carcinoma of the conjunctiva: Analysis of 60 cases. Br J Ophthalmol 1999;83:98-103.  Back to cited text no. 3
    
4.
Newton R, Ferlay J, Reeves G, Beral V, Parkin DM. Effect of ambient solar ultraviolet radiation on incidence of squamous-cell carcinoma of the eye. Lancet 1996;347:1450-1.  Back to cited text no. 4
    
5.
McKelvie PA, Daniell M, McNab A, Loughnan M, Santamaria JD. Squamous cell carcinoma of the conjunctiva: A series of 26 cases. Br J Ophthalmol 2002;86:168-73.  Back to cited text no. 5
    
6.
Nakamura Y, Mashima Y, Kameyama K, Mukai M, Oguchi Y. Detection of human papillomavirus infection in squamous tumours of the conjunctiva and lacrimal sac by immunohistochemistry, in situ hybridisation, and polymerase chain reaction. Br J Ophthalmol 1997;81:308-13.  Back to cited text no. 6
    
7.
Premoli-De-Percoco G, Ramírez JL, Galindo I. Correlation between HPV types associated with oral squamous cell carcinoma and cervicovaginal cytology: An in situ hybridization study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;86:77-81.  Back to cited text no. 7
    
8.
Yang YY, Koh LW, Tsai JH, Tsai CH, Wong EF, Lin SJ, et al. Involvement of viral and chemical factors with oral cancer in Taiwan. Jpn J Clin Oncol 2004;34:176-83.  Back to cited text no. 8
    
9.
Spitzer MS, Batumba NH, Chirambo T, Bartz-Schmidt KU, Kayange P, Kalua K, et al. Ocular surface squamous neoplasia as the first apparent manifestation of HIV infection in Malawi. Clin Experiment Ophthalmol 2008;36:422-5.  Back to cited text no. 9
    
10.
Kestelyn P, Stevens AM, Ndayambaje A, Hanssens M, van de Perre P. HIV and conjunctival malignancies. Lancet 1990;336:51-2.  Back to cited text no. 10
    
11.
Waddell KM, Lewallen S, Lucas SB, Atenyi-Agaba C, Herrington CS, Liomba G. Carcinoma of the conjunctiva and HIV infection in Uganda and Malawi. Br J Ophthalmol 1996;80:503-8.  Back to cited text no. 11
    
12.
Ateenyi-Agaba C. Conjunctival squamous-cell carcinoma associated with HIV infection in Kampala, Uganda. Lancet 1995;345:695-6.  Back to cited text no. 12
    
13.
Gichuhi S, Sagoo MS, Weiss HA, Burton MJ. Epidemiology of ocular surface squamous neoplasia in Africa. Trop Med Int Health 2013;18:1424-43.  Back to cited text no. 13
    
14.
Mahomed A, Chetty R. Human immunodeficiency virus infection, Bcl-2, p53 protein, and Ki-67 analysis in ocular surface squamous neoplasia. Arch Ophthalmol 2002;120:554-8.  Back to cited text no. 14
    


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