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Year : 2018  |  Volume : 25  |  Issue : 2  |  Page : 96-102  

Characteristics and factors related to eyelid basal cell carcinoma in Saudi Arabia

1 Department of Oculoplastic, King Khaled Eye Specialist Hospital, Riyadh, Saudi Arabia
2 Department of Education, King Khaled Eye Specialist Hospital, Riyadh, Saudi Arabia
3 Department of Pathology, King Khaled Eye Specialist Hospital, Riyadh, Saudi Arabia
4 Department of Research, King Khaled Eye Specialist Hospital, Riyadh, Saudi Arabia
5 Department of Ophthalmology, College of Medicine, King Saud University, Riyadh, Saudi Arabia
6 Department of Pathology, King Saud University, Riyadh, Saudi Arabia

Date of Web Publication18-Jul-2018

Correspondence Address:
Prof. Silvana Artioli Schellini
King Khaled Eye Specialist Hospital, Riyadh
Saudi Arabia
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/meajo.MEAJO_305_17

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PURPOSE: Data on basal cell carcinoma (BCC) from the Middle East are deficient. We present the features and management outcomes for BCC over the last 36 years in Saudi Arabia.
SUBJECTS AND METHODS: This retrospective chart review included BCC patients diagnosed and treated at Saudi Arabia between 1980 and 2016. Data were collected on patient demographics, clinical and histopathological characteristics of the lesions, management, and follow-up.
RESULTS: One hundred and twenty-six patients with BCC were included in this study. The incidence of BCC in Saudi Arabia is 0.8 cases a year. The median age of the patients was 71 years. BCC affected 58.9% of males. The lower lid was the most common site of occurrence (52.7%). Clinically, BCC was most commonly recognized as a mixed lesion (41.1%) and 50.4% were histologically nodular. Risk factors for poor prognosis included tumor localization in the medial aspect of the lid, tumor size > 5 mm, histological subtype being ulcerative or morphea forms, affected margins, and recurrent lesions.
CONCLUSION: BCC is a rare condition in Saudi Arabia. The clinical features and histopathology of BCC in Saudi Arabia are similar to the patterns observed in other regions of the world. Early detection and timely management mitigates the extensive destructive ocular/orbital damage due to BCC and results in better patient outcomes.

Keywords: Basal cell carcinoma, eyelid, eyelid tumor, prognostic factors, Saudi Arabia

How to cite this article:
Al Wohaib M, Al Ahmadi R, Al Essa D, Maktabbi A, Khandekar R, Al Sharif E, Al Katan H, Schellini SA, Al Shaikh O. Characteristics and factors related to eyelid basal cell carcinoma in Saudi Arabia. Middle East Afr J Ophthalmol 2018;25:96-102

How to cite this URL:
Al Wohaib M, Al Ahmadi R, Al Essa D, Maktabbi A, Khandekar R, Al Sharif E, Al Katan H, Schellini SA, Al Shaikh O. Characteristics and factors related to eyelid basal cell carcinoma in Saudi Arabia. Middle East Afr J Ophthalmol [serial online] 2018 [cited 2021 Oct 23];25:96-102. Available from: http://www.meajo.org/text.asp?2018/25/2/96/237035

   Introduction Top

It is diffi cult to estimate the prevalence and incidence of skin cancer due to insufficient data recorded in cancer registries.[1],[2] Estimates of the annual incidence of basal cell carcinoma (BCC) from two different regions in the US vary from 146 cases/100,000 population to 422 cases/100,000 population.[2] The overall crude incidence rate in the United Kingdom is 201.7/100,000/year (95% confidence interval: 200.1–203.4) and the incidence of BCC in Bulgaria is about 2000 cases/100,000 population.[1],[3]

The prevalence of BCC is increasing by 10% per year and the lifetime risk of developing BCC is approximately 30%.[4],[5] There are approximately 2.8 million new cases of BCC annually in the US and 700,000 new cases annually in Europe.[6]

BCC mainly affects areas of the body that are most exposed to sunlight, with 80% of BCCs located in the head, face, and neck.[2],[6] Around 20% of BCCs occur on the lids and BCC is responsible for 80%–90% of all malignant lid tumors.[7],[8],[9],[10],[11]

The incidence and morbidity of BCC vary according to predisposing ethnic and genetic disorders (e.g., albinism, Gorlin syndrome, and xeroderma pigmentosum). Comorbidities, immunosuppression, and exposure to carcinogens such as arsenic may also predispose to BCC.[1],[7]

BCC is a result of a predisposed phenotype that is exposed to environmental risk factors. In addition, a relationship between BCC and occupation has been reported in farmers who are more likely to develop BCC at a younger age and have a greater risk of recurrence.[12]

Environmental and geographic factors play a significant role in the incidence and prevalence of BCC. Populations living near the equator or at higher altitudes are more likely to develop BCC. Exposure to ultraviolet (UV) radiation is the main risk factor and damage to the ozone layer has resulted in greater UV exposure.[7],[8],[13],[14]

There is a paucity of epidemiologic data on BCC in the Middle East region. Notably, BCC is the second-most common malignant tumor among adults examined in Saudi Arabia,[15] a desert country positioned in the Middle East, a geographic region of Southwest Asia in the northeastern hemisphere with latitude/longitude ranging from Jeddah 21°32'N, 39°10'E to Tabuk 28°23'N, 36°34'E. The population of Saudi Arabia follows Muslim customs, using clothes with long sleeves and covering the entire body, with only the face or the eyes exposed, and due to the climate and environment, most activities are indoor rather than outdoor and sun exposure is very limited which can influence the BCC occurrence.

Due to lack of data, the aim of the present study was to evaluate the demographic profile, epidemiological data, histopathological subtypes, and treatment outcomes of BCC of the eyelid in Saudi Arabia.

   Subjects and Methods Top

This retrospective study evaluated cases of BCC of the eyelid treated at two institutions in Riyadh, Saudi Arabia, from 1980 to 2016. Both institutions are the main national reference centers for treating the population from all regions of Saudi Arabia. This study was approved by an internal review board and consent was waived due to the retrospective nature of this study. This study adheres to the tenets of Declaration of Helsinki.

Patients were included if they were Saudi nationals or belonged to the Arabic Peninsula. There were no restrictions based on age, gender, place of residence, or socioeconomic status. Only patients who had surgery and a confirmed histopathologic diagnosis were included. Exclusion criteria were surgery that was performed elsewhere, inadequate data without histologic analysis, or <6-month follow-up.

Data were collected by chart review on patient demographics such as age, gender, occupation, and location of residence. Data were also collected on tumor characteristics including aspect and location on the lids, possibility of other tumors in the lids or the face, clinical diagnosis, type of surgical procedure to remove the lesion, size of the tumor and technique to repair the lid, histological diagnosis, involvement of surgical margins after removal, possible recurrence/relapse, and the postoperative course.

The lesions were examined under ambient room lighting or using slit lamp and documented with external photography. Treatment was based on incisional biopsy whenever necessary to confirm the diagnosis prior to surgical excision using frozen-section (FS) analysis of margins. The resected margins were not quantified but were large enough to obtain tumor-free margins. In all cases, the diagnosis was confirmed by histologic examination.

The pathology departments from both participating institutions followed the same standard procedures. For FS analysis, the tumor margins were identified, fixed in formalin, and processed for examination. Tissues were resubmitted for further evaluation until free margins were obtained. The main tumor specimen was fixed in formalin, and then the tissue was prepared in an automatic processor, embedded in paraffin, and stained with H and E. Two experts (two authors) examined and discussed the evaluation of margins and/or diagnosis as warranted. Data were collected on the size of the tumor in millimeters, histological type of lesion, and margin status. The tumors were classified according to the American Joint Committee on Cancer classification.

Surgical reconstruction of the lid was based on the size of the defect and surgeon's experience. The postoperative follow-up schedule was based on the treating physician's decision. The majority of patients were evaluated at 1 month postoperatively and then once a year, focusing mainly on the local aspect of the repaired area and signs of recurrence/relapse of BCC.

The data were collected on a pretested data collection form, transferred to an Excel spreadsheet (Microsoft Corp., Redmond, WA, USA), and were analyzed with Statistical Package for the Social Sciences software (SPSS 24; IBM Corp., Armonk, NY, USA). Descriptive and inferential analyses were performed for the demographic data. To estimate the geographic region of occurrence of BCC, the place of residence was noted and the frequency of occurrence of BCC in the Saudi population was calculated for each region. Survival rate was estimated after contact by phone with the patient or relatives.

   Results Top

This study analyzed 129 cases resulting in a mean of 3.58 cases/year. Six patients were ruled out due to the exclusion criteria. [Table 1] presents the demographic data and clinical features of the study sample. Median age at presentation was 71 years (25% quartile = 59.5; minimal age = 16 years; maximal age = 105 years). The youngest patient was 16 years old and was diagnosed with xeroderma pigmentosum. BCC was significantly more frequent in males (76 patients; 58.9%), with male/female ratio of 1:4. The interval between the patient noticing the lesion and presentation to one of the two institutions ranged between 1 and 5 years for 50 (38.8%) patients and after 5 years for 31 (24%) patients.
Table 1: Demographic and clinical profiles of patients with basal cell carcinoma in Saudi Arabia over the last 36 years

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There was a similar frequency of occurrence of the lesion between the right and left lids. The lesion was bilateral in two (1.6%) patients. The lower lid was most commonly affected (68 patients; 52.7%), followed by the medial canthus (21 patients; 16.3%). The lesion was large, affecting two regions in 16 (12.4%) patients and three or more regions in 6 (4.7%) patients. A total of 157 lid regions were affected in 129 patients.

One hundred and six (82.2%) patients denied any history of similar lesions and 128 (99.2%) patients presented with only a lesion on the lid.

According to clinical presentation, most cases had more than one clinical characteristic (53 mixed; 41.1%), followed by ulcerated (28; 21.7%), pigmented (20; 15.5%), and nodular (18; 14%) BCC [Table 1] and [Figure 1].
Figure 1: (a) Lesion at the medial canthus showing nodular and pigmented characteristics. (b) Histopathology: nodular basal cell carcinoma. (c) Lesion at the medial canthus showing an ulcerated lesion. (d) Histopathology: basal cell carcinoma morphea form, infiltrative type

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Management data were available for 128 patients. Incisional biopsy to confirm the diagnosis prior to surgery was performed in 96 (74.4%) patients and excision biopsy in 28 (21.7%) patients. Seventy-six (59.4%) patients, mainly with large lesions, were managed with FS analysis.

Reconstructive surgery included direct closure (50 patients; 38%), flap (24 patients; 17.8%), grafting (17 patients; 13.2), or complex procedures (30 patients; 23.3%). The tumor size according to the macroscopic examination was >5 mm in 110 (85.3%) patients and <5 mm in 13 (10.1%) patients. The tumor size was not recorded in 6 (4.7%) cases.

Histopathologic evaluation was performed on all cases and on the aspects of the tumor including recurrences/relapses [Table 2] and [Figure 1]. Nodular BCC was the most common (65, 50.4%), followed by ulcerative (17, 13.2%), basosquamous (15, 11.6%), morphea (14, 10.9%), sclerosing (5, 3.9%), and mixed (4, 3.1%).
Table 2: Histopathology type and relapse according to time and histological classification of basal cell carcinoma in Saudi Arabia

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The margins were free of tumor in 97 (75.2%) lesions and affected in 26 (20.2%) lesions. The details of the margins were not available in six lesions.

Recurrence of the lesion <5 years after surgery was noted in 13 (10.1%) patients. Twenty-six (20.2%) patients had a recurrence >5 years after management. No recurrence was detected during follow-up in 84 (68.3%) patients. Ulcerative and morphea forms of BCC were the most likely to relapse [Table 2].

Eight (6.2%) patients had lesions extending to the orbit. Six of these patients underwent exenteration. In five (83.3%) of the six exenteration cases, the lesion was located in the inferomedial aspect of the lids, three (50%) were basosquamous, two were morphea form, one was nodular, and three (50%) patients had other lesions on the face.

Frequency of occurrence according to the region in Saudi Arabia

The majority of patients with BCC were from the central (42/32.6%) region followed by the southern (30/23.3%), western (16/12.4%), northern (8/6.2%), and eastern (5/3.9%) regions.

Estimated survival rate

We contacted 125 patients or their relatives to verify they were alive. The remaining four patients could not be contacted and may be presumed dead and the cause of death was undetermined. Hence, we can deduce the BCC survival rate to be 96.9% in this population.

   Discussion Top

We observed 129 patients with BCC treated over a duration of 36 years, yielding a relatively low mean frequency of 3.6 cases a year. This is notable because BCC is the second-most common malignancy in Saudi Arabia, responsible for 23% of the malignancies in people older than 15 years. The prevalence of BCC has increased significantly in the last 30 years in the region.[15]

Similar to studies from other countries, most of the patients in the current study were elderly.[2],[9],[16],[17] BCC in children is very rare, and early presentation of BCC is possible in patients with albinism or xeroderma pigmentosum (as in one 16-year-old patient in our study).[18]

There was a greater preponderance of males than females with BCC in our study, similar to studies from North America, Iran, and Brazil.[2],[12],[17],[19] However, others reported a greater preponderance among females or a similar incidence between genders.[16],[20] The difference in incidence between genders may reflect the difference in the nature of activities and exposure to risk factors.[12] Racial and cultural factors may also influence the gender distribution of BCC.[12]

BCC is more likely to affect individuals with blonde hair and blue eyes.[13] However, this phenotype is very unusual in Saudi Arabia and the Saudi phenotype is protective against BCC.

In the current study, BCC was most commonly located in the lower lid and medial canthus, a finding similar to that of studies carried out in other countries, probably due to corneal light reflection onto the lower lid, associated with chronic irritation of chemical or physical factors related to the tears.[7],[8],[9],[16],[21],[22] The upper lid is rarely affected likely due to protection conferred by the brow.[8]

In our study, 82.2% of patients had the first lesion on the lid and 99.2% of the patients only had lid lesions. However, studies from other countries reported that approximately 41% of patients had BCC in other locations and 33.4% of patients may have another BCC on the face.[23]

Although Saudi Arabia is a tropical desert, with hot temperatures and very dry weather for most of the year, the Muslim lifestyle with the population wearing long-sleeved clothing and covering the head and face for most outdoor activities represents a protective factor against sun exposure which can explain the low rates of BCC of the lids in Saudi Arabia.

Most of our patients were from the central Saudi Arabia and both hospitals were in Riyadh, a city that is highly populated (6,704,000 inhabitants from the estimated population of 32.28 million for the country). To more accurately evaluate the distribution of BCC in Saudi Arabia, a study is required based on geographic locale of BCC cases.

In our study, the mixed pattern was the most common clinical presentation. However, the most common clinical presentation of BCC is nodular or nodular with a central rodent ulcer because of the overlying ulceration.[17],[22] The pigmented BCC, which is considered a type of nodular BCC, was present in 15.5% of our patients probably because pigmented BCC is common in dark-skin complexion individuals [5] as it is usual in the Middle East. However, pigmented types were the least common for others who studied population of the same region.[12]

Some lesions can clinically simulate other entities as morphea form of BCC may simulate chronic blepharitis being important to observe the absence of lashes which is a characteristic feature in malignant tumors.[22]

Despite the easily detectable lesion on the lids, almost 70% of the patients in the current study took more than 1 year to seek treatment, with lesions measuring more than 5 mm, called “giant tumors” in 85.3% of the patients and affecting more than one aspect of the lid.[5]

Excisional biopsy with predetermined margin is an easy and popular technique to treat BCC. However, 74.4% of the cases in this study underwent an incisional biopsy probably due to the large size of the lesions, requiring a confirmation of the diagnosis prior to a more aggressive surgical approach.

Surgical excision with FS analysis ensures unaffected surgical margins and is considered the gold standard procedure to treat large BCCs.[2],[22] However, intraoperative FS analysis extends surgical time, increases cost, and requires the presence of an experienced pathologist at the medical center.[22] FS analysis is strongly recommended for more aggressive tumors and clinical and histological subtypes that are likely to have incomplete excision or recurrent tumors, reducing the chance of a subsequent recurrence.[8],[22],[24] When the lesion is small, circumscribed with well-defined margins, FS analysis can be avoided.

In our study, reconstructive surgery included direct closure in only 38% of the patients, confirming that the tumors were large. Another study reported that 70% of cases were treated with direct closure.[16]

Histologically, approximately 50% of our lesions were nodular, which is generally the most common histological type of BCC.[17] The infiltrative pattern (morphea form, multicentric, and sclerosing) was observed in 15.6% of our cases and occurred in 23.8% of lesions in another country.[16] We observed more chances of recurrence in ulcerative and morphea forms of BCC, which concurs with other studies.[22] The more aggressive nature and evolution of the infiltrative BCC are related to the undefined margins.

Incomplete excision was detected in 20.2% of the resected lesions, similar to others.[16] Incomplete excision has been reported to range from 1.5% to 28.5%, occurring mainly laterally than in the deep margins and may carry a higher risk of local recurrence.[4],[24] Risk of recurrence is approximately 5%–14% of patients when the lesion is completely excised, increasing to 40%–50% depending on incomplete surgical excision.[8],[13],[17],[21] However, compromised histologic margins do not necessarily predict relapse.[16],[17]

This controversy indicates that positive margin is not the only factor as recurrence occurs in 26.5% of patients who present with infiltrative histological types of BCC, while in the nodular type, recurrence occurs in 6.4% of patients.[21] In addition, recurrence is higher in larger tumors, being >23%–40% in tumors >2 or 3 cm, decreasing to <10%–12% if tumors are <2 cm.[3],[7],[22] However, it is debatable if size is a determining factor for recurrence because incomplete excision is more common in larger lesions.[24]

Information about the margin and type of lesion also can determine the duration of follow-up. On an average, one in every ten BCCs relapse and recurrence occurs within 8–30 months after primary surgery.[10] Even the extension of free margin to prevent recurrence is debatable.[13] When BCC is noninfiltrative, 4-mm margins free of tumor after excision can achieve a zero recurrence rate and long-term follow-up is not needed. However, patients with infiltrative or previously recurrent BCCs likely require long-term follow-up.[16] Previous studies indicate that approximately 50% of recurrences occur 2 years after resection.[7],[8] Therefore, it is important to have long-term follow-up, especially for patients with a high risk for recurrence based on pathological subtypes, location, size, margins, immunosuppression, radiation treatment, and evidence of perineural involvement.[7],[8]

In our study, cases with orbital invasion that warranted exenteration were larger tumors, located in the inferomedial aspect of the orbit and morphea form types. BCCs with these characteristics are most likely to evolve to orbital extension.[8] Structures related to the lacrimal drainage system are present in the medial canthus, inducing the surgeon to remove less tissue with the risk of remaining tumor and favoring orbital invasion.[2],[22] Orbital invasion is commonly related to misdiagnosed or inadequately treated BCC.[11] Imaging studies of patients with orbital invasion may indicate bone and soft-tissue involvement.[8] Factors indicating poor prognosis in BCC include location in the central face, large tumors (size >5 cm), pathological subtype (worst in ulcerative, morphea form, or other infiltrative subtypes), deep tumor location, perineural or perivascular invasion, incomplete excision, and prior recurrent lesions.[5],[6],[24] In addition, immunosuppression, previous radiotherapy, and distant metastasis are also factors linked to poor prognosis.[4],[6]

The high survival rates reported in our study confirmed the well-documented low morbidity of BCC.[22] In general, BCC is easy to detect, progresses slowly, does not metastasize, and accounts for <0.1% of patient deaths. However, the lesion can invade and destroy adjacent tissues such as the orbit, conjunctiva, cornea, paranasal sinuses, nasal cavity, and central nervous system, causing major complications.[16],[22]

The retrospective nature of the study is a limitation. However, our study documents the main features of BCC in Saudi Arabia. In addition, we add to the scant data on BCC in Saudi Arabia. These data may be used for public health policy or for public health education.

   Conclusion Top

The environment in Saudi Arabia is a risk factor for BCC, but the incidence is low probably because of national customs, traditions, and lower sun exposure. BCC in Saudi Arabia had a similar pattern to that reported in other countries, as tumor mainly localized in the inferior lid, larger than 5 mm in diameter, nodular subtype and ulcerative/morphea form histopathological types that were the most likely to relapse. Poor prognosis was associated with late presentation for treatment and large lesions requiring more extensive surgical approaches. The key decision in reducing morbidity is to confirm the diagnosis and patients need to be educated on the risk of BCC and present for treatment in a timely fashion.

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Conflicts of interest

There are no conflicts of interest.

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  [Figure 1]

  [Table 1], [Table 2]


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