|Year : 2014 | Volume
| Issue : 2 | Page : 55-62
Nonmelanoma skin cancers: An Indian perspective
Geeti Khullar1, Uma Nahar Saikia2, Dipankar De1, Bishan Das Radotra2
1 Department of Dermatology, Venereology and Leprology, Postgraduate Institute of Medical Education and Research, Chandigarh, Punjab and Haryana, India
2 Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, Punjab and Haryana, India
|Date of Web Publication||18-Dec-2014|
Uma Nahar Saikia
Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh - 160 012, Punjab and Haryana
Source of Support: None, Conflict of Interest: None
Nonmelanoma skin cancers (NMSCs), which mainly include basal cell carcinoma (BCC) and squamous cell carcinoma (SCC), are infrequent in the Indian subcontinent, compared with white skinned individuals. Although BCC in most cases arises de novo on sun-exposed sites, it may rarely develop in photoprotected areas and in the setting of certain risk factors. In contrast to BCC, SCC in dark skin has a tendency to develop in nonhealing ulcers, chronic scars, and inflammatory and infectious dermatoses. Histopathology is the gold standard in confirming the diagnosis and determining the prognosis. As the existing literature on NMSCs in India is limited mostly to case reports and few reviews only, this article is an attempt to create an awareness regarding the premalignant potential of an expanding list of cutaneous lesions, which would help in timely diagnosis and prompt treatment of NMSCs.
Keywords: Basal cell carcinoma, cutaneous, malignant, squamous cell carcinoma
|How to cite this article:|
Khullar G, Saikia UN, De D, Radotra BD. Nonmelanoma skin cancers: An Indian perspective. Indian J Dermatopathol Diagn Dermatol 2014;1:55-62
|How to cite this URL:|
Khullar G, Saikia UN, De D, Radotra BD. Nonmelanoma skin cancers: An Indian perspective. Indian J Dermatopathol Diagn Dermatol [serial online] 2014 [cited 2019 Feb 17];1:55-62. Available from: http://www.ijdpdd.com/text.asp?2014/1/2/55/147282
| Introduction|| |
Nonmelanoma skin cancers (NMSCs) or keratinocytic carcinomas largely comprise of squamous cell carcinoma (SCC) and basal cell carcinoma (BCC). These neoplasms are common in white-skinned individuals but are rare in dark skin phenotypes. The NMSCs comprise of 1%-2% of cutaneous neoplasms in Indians, in contrast to one-third in whites.  This is predominantly due to protection offered by melanin pigment against ultraviolet radiation (UVR)-induced DNA damage, which is responsible for carcinogenesis. SCC represents 30%-65% of skin cancers in blacks and Indians and 15%-25% in whites, whereas BCC contributes to 65%-75% of skin cancers in whites and 20%-30% in Asian Indians.  As these cutaneous malignancies are not reported in cancer registries, their exact incidence is not known. In addition, there is paucity of data on the risk factors, histopathologic classification and prognosis of NMSCs from the Indian subcontinent. We present a comprehensive review highlighting the epidemiologic factors, precursor lesions along with clinical and histopathologic variants of NMSCs (BCC and SCC) in the Indian scenario. The data were extracted and synthesized using search terms "non-melanoma skin cancer in India," "squamous cell carcinoma in India," and "basal cell carcinoma in India" in PubMed database.
| Basal Cell Carcinoma|| |
BCC is a malignant neoplasm of skin derived from the basal cells of the epidermis or hair follicles. It is the most common cutaneous malignancy in whites and the second most common after SCC in blacks, Asians, and Indians. In a retrospective 5-year study (2005-2009) of skin malignancies from India, 51.6% (31/60) cases were diagnosed as NMSCs, of which 83.9% were confirmed as SCC and 16.1% as BCC.  In contrast to this, a 10-year study (2003-2013) from North India, reported BCC to be more common than SCC [(67.5% vs 32.5% of NMSCs, respectively): Unpublished data].
Risk factors for BCC
UVR, particularly UVB is the most important etiopathogenic factor for BCC as 80% of the tumors are distributed on the head and neck region.  Intermittent periods of intense sun exposure instead of cumulative exposure increase the risk of BCC. The other predisposing factors include ionizing radiation, arsenic exposure,  inherited syndromes, and immunosuppression, particularly post-organ transplantation. Although most BCCs arise de novo, they may sometimes complicate scarring processes  and chronic dermatoses. A patient with generalized lichen planus (LP) developed a single indurated pigmented plaque on the face, which on histopathology showed findings of coexistent solid variant of BCC and LP.  The authors proposed that UVR is a common etiologic factor for BCC and actinic variant of LP. In addition, impaired immune surveillance as a consequence of chronic inflammation in LP may contribute to malignant change.  Other cutaneous lesions in which BCC may develop include lupus vulgaris,  verrucous epidermal nevus,  and nevus sebaceous. 
Clinical variants and distribution
The clinical types include nodular, superficial spreading [Figure 1], pigmented [Figure 2], morpheaform and fibroepithelioma of Pinkus (FEP). Nodular BCC is the most common variant (60%) that presents as a translucent dome-shaped papule or nodule with rolled out margins, overlying telangiectasias, and central ulceration. Morphoeic or sclerodermiform BCC is a rare clinical type presenting as an ivory white to yellowish, firm, indurated plaque without thread-like elevated borders.  Although FEP was initially described as a premalignant lesion, its exact nosologic status is still controversial. It has been suggested as a variant of trichoblastoma, a benign counterpart of BCC or a malignant neoplasm. It presents as an erythematous, brown or skin-colored, sessile or pedunculated nodule with a broad base on the trunk and extremities. There is only one report of an Indian patient who had FEP coexisting with nodular BCC in the same lesion on histopathology, pointing toward its malignant behavior. 
|Figure 1: An erythematous to slightly pigmented plaque with rolled out margins and showing overlying telangiectasias, greyish-white scaling and ulceration on the superolateral margin suggestive of superficial basal cell carcinoma|
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|Figure 2: Hyperpigmented plaque with rolled out margins on the lateral aspect of the right supraorbital margin characteristic of pigmented variant of basal cell carcinoma|
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Majority of BCCs occur on the head and neck, most frequently above the line joining the angle of mouth and the tragus of ear. Rarely, it may arise at unusual sites, including scrotum, vulva,  and perianal area.  Periungual distribution is also uncommon and may present as a nonhealing ulcer and rarely as onycholysis or longitudinal melanonychia. Thumb is the most frequently affected digit.  Nipple-areola complex has also been reported as a rare site of occurrence of BCC from India.  In the absence of sun exposure, other risk factors such as advancing age, chronic irritation, immunosuppression, ionizing radiation, and coal tar exposure may contribute to tumor development at these sites [Figure 3]. Altered cell-matrix interactions have also been implicated in the development of BCC at sun-protected sites.  Thus it is important to identify tumors at an early stage at these rare sites due to their greater propensity for metastasis.
|Figure 3: Basal cell carcinoma presenting on a photoprotected site (left breast)|
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The common histologic variants include solid or nodular [Figure 4], micronodular, superficial, pigmented, infiltrative, morpheic, metatypical (basosquamous), and fibroepithelioma. Micronodular, infiltrative, metatypical, and morpheaform types are more likely to show local recurrence. Other less common variants include keratotic [Figure 5]a, adenoid [Figure 5]b, signet ring cell, clear cell, BCC with sebaceous, eccrine, matricial differentiation, adamantinoid, and granular types. Adenoid variant is characterized by tubular differentiation with lumen containing amorphous granular material and this variant presents on the lumbosacral area.  Histologically, it is low grade and has good prognosis. Basosquamous cell carcinoma (BSCC) is another rare histologic subtype of BCC characterized by areas of both basaloid and squamoid differentiation with a transition zone between the two. Predominantly, tumor cells show basaloid differentiation. On immunohistochemistry, cells are positive for Ber EP4 in the BCC zone and for epithelial membrane antigen in the SCC area. BSCC is associated with greater potential for recurrence and metastasis as compared to BCC. Ranjan et al. reported a patient of oculocutaneous albinism with an exophytic plaque that showed central ulceration and rolled out edges. Histology revealed areas of both SCC and BCC, however, immunohistochemistry was not done. 
|Figure 4: Photomicrograph showing classical basal cell carcinoma with peripheral palisading, retraction artefacts and focal pigmentation within tumour lobules (H and E, ×10)|
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In a retrospective analysis of clinicohistologic profile of 32 cases of BCC from South India, 28 were distributed on the head and neck, 2 on the upper limb, and 1 each on shoulder and abdomen. Histologically, classic morphology was noted in 11, pigmented in 10, adenoid in 4, morpheaform in 3, metatypical, eccrine, fibroepithelioma, and superficial spreading in 1 each. Abundant stroma separating the cells was a peculiar feature of morpheaform and fibroepithelioma types. 
In a similar study from North India, the most common age group was 40-60 years with male-to-female ratio of 1.6:1. The lesions were distributed on head and neck in 91.2% cases. The most common histopathologic subtype was nodular (64.7%) followed by infiltrating (14.7%) variant. Pigmentation was noted in 44.2% of tumors. P53 expression was observed in 17.4% cases, of which majority were infiltrating type. Strong peripheral cell nuclear antigen (PCNA) nuclear positivity in 20%-30% cells was seen in infiltrating type, whereas noninfiltrating lesions showed staining only at the tumor periphery in 5%-20% cells. Eighty-five percent cases showed expression of antiapoptotic protein Bcl-2 and exhibited inverse relationship with p53 positivity. Weak focal expression of apoptotic protein Bax was noted in 11.8% cases. 
BCC is a slow-growing tumor that usually invades local structures and rarely metastasizes. Clinically, poor prognostic factors include tumor size > 2 cm, depth of invasion, mid-facial distribution, ill-defined margins, long-standing lesion, recurrent disease, and immunosuppression. Histologically, perineural and vascular invasion increase the risk of metastasis. A case of BCC on inner canthus of the eye and adjoining nasal bridge that metastasized to the muscles of cheek, intraparotid, and internal jugular group of lymph nodes has been reported from India. 
Squamous cell carcinoma
Squamous cell carcinoma encompasses primary malignant epithelial tumors of Malpighian differentiation that arise from suprabasal keratinocytes. The incidence rate of cutaneous SCC varies widely with geographic location, being 387/100,000 person years in Australia (2002), 60.2/100,000 person years in the United States (2006), and 22.65/100,000 person years in England (2000-2006).  UVR is an important environmental etiologic factor for SCC, particularly in white-skinned individuals. Total cumulative lifetime sun exposure resulting in p53 gene mutations is pathogenic for the development of SCC.
Other risk factors and precursor lesions for SCC
SCC has been described in the setting of a number of predisposing conditions, both genetic and acquired. Among Indian patients, genodermatoses that may give rise to SCC include xeroderma pigmentosum (XP),  oculocutaneous albinism,  epidermodysplasia verruciformis,  and epidermolysis bullosa.  The acquired precursor lesions are more common and include chronic inflammatory and scarring dermatoses, actinic keratosis [Figure 6], Bowen's disease, and risk factors, such as ionizing and thermal radiation, immunosuppression, human papilloma virus (HPV) infection, and chemical carcinogens such as arsenic.
|Figure 6: Noduloulcerative squamous cell carcinoma (SCC) with focal pigmentation on left cheek and multiple rough scaly pigmented plaques medial to SCC, on tip of the nose and above upper lip suggestive of pigmented actinic keratosis|
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Chronic arsenicosis-related skin tumors may involve both photodistributed and photoprotected sites and arise either de novo or from premalignant keratotic lesions. A study conducted on 24 patients with manifestations of chronic arsenicosis reported SCC in 10 (41.7%), Bowen's disease in 9 (35.5%), and BCC in 8 (33.3%) patients. Three patients developed SCC on precursor lesions of arsenical keratoses. The most common site of involvement was chest in 33.3%, followed by palms in 16.7% cases. 
Darker-skinned persons tend to develop SCC in long-standing scars and inflammatory and infectious dermatoses predominantly involving non-sun-exposed sites. Metastatic rate of SCC complicating chronic scarring conditions is approximately 20%-40%, compared with 1%-4% in tumors related to sun exposure.  Marjolin's ulcer is defined as SCC arising in chronic nonhealing wound, scar tissue, ulceration, sinus tract, or fistula. Postburn scar is the most common precursor lesion for Marjolin's ulcer.
Inflammatory dermatoses that predispose to SCC
A large spectrum of chronic inflammatory dermatoses that may develop into SCC have been described from India. Chronic inflammation stimulates the production of growth factors resulting in neoplastic proliferation of the epidermal cells. SCC presenting over buttocks and perianal area has been described in a patient with disseminated lesions of porokeratosis of Mibelli.  SCC complicating psoriatic vulgaris is rare in the absence of treatment with PUVA and immunosuppressants. Gupta et al. reported a case of verrucous growth overlying psoriatic plaques with histopathology showing well-differentiated SCC.  Deshmukh et al. described a patient with multiple SCCs resulting from continuous trauma and inflammation in lichen simplex chronicus.  In lichen planus, oral lesions are at a greater risk of malignant change (0.3%-3%) compared with the cutaneous lesions (0.4%). , Among cutaneous lesions, lichen planus hypertrophicus (LPH) is most frequently associated with SCC.  SCC may also arise in plaques of discoid lupus erythematosus (DLE) both on sun-exposed and sun-protected sites. , The incidence of SCC evolving in lesions of DLE has been reported to be 3.3% with a latent period of 26-41 years.  Exposure to ultraviolet light, long-standing inflammation, associated scarring, and treatment-related immunosuppression in those with coexisting SLE, may all contribute to the increased risk of SCC in DLE patients. Lichen sclerosus et atrophicus (LSA) of the anogenital region is also associated with malignant potential.  The risk of developing SCC on a background of penile LSA (clinical and/or histologic) is approximately 5.8% and the latent period is approximately 10-23 years. Rarely, long-standing plaque of necrobiosis lipoidica diabeticorum (NLD) may develop overlying ulceration suggestive of SCC. Necrosis in the dermis leading to poor blood supply to the epidermal cells results in increased keratinization and malignant transformation.  Although vitiligo patches are devoid of melanin, the incidence of SCC arising in vitiliginous skin is rare. PUVA therapy is an independent risk factor in these patients. A patient with generalized vitiligo developed malignant transformation on the dorsum of hand, a sun-exposed site. He worked in outdoor environment for long periods and had not received immunosuppressants or phototherapy.  The rarity of neoplastic change in vitiligo has been attributed to upregulation of p53 gene and equal potential of vitiliginous skin to repair UVR-induced DNA damage as uninvolved skin. Foot ulcers resulting from peripheral neuropathy and vasculopathy are a frequent complication in diabetes mellitus and SCC may rarely occur in long-standing nonhealing ulcers. 
Cutaneous infections that predispose to SCC
SCC may rarely develop in lesions of lupus vulgaris. Failure to respond to an adequate course of antitubercular treatment may provide a clue in diagnosing neoplastic transformation.  Long-standing inadequately treated tinea corporis has shown malignant degeneration into well-differentiated SCC with bony invasion.  Neoplastic transformation has been described in granuloma inguinale.  Chronic lymphedema of penoscrotal region secondary to filariasis has been reported to develop SCC as a result of lack of recognition of tumor-associated antigens in the presence of impaired afferent lymphatic drainage.  In a study evaluating malignant transformation in 79 cases of trophic ulcers in leprosy, 11 patients were diagnosed with SCC. Well-differentiated type was seen in 10 patients and verrucous carcinoma in 1 patient. Rapid enlargement of the ulcer in long-standing cases may point toward malignancy. 
Predisposing factor unique to India
Thermal radiation due to kangri, which is used as an indigenous source of heat in Kashmir region, is an important risk factor for SCC. The premalignant cutaneous lesion associated with its use is erythema ab igne. Hassan et al. analyzed the histopathologic changes of cutaneous lesions secondary to kangri use in 30 cases. Erythema ab igne alone was present in all the cases, Bowen's disease in 20 and SCC in 10 cases overlying erythema ab igne. 
Verrucous carcinoma, a well-differentiated variant of SCC, is characterized by less aggressive behavior. It can occur in the oral cavity, anogenital mucosa, plantar skin (carcinoma cuniculatum), and other cutaneous sites. A clinicopathologic study carried out in 12 cases of carcinoma cuniculatum from India demonstrated the most common site as plantar aspect of foot (4), followed by flank (3), leg (2), face (2), and palm (1). The predisposing factors were trauma and chronic scarring. The histopathology showed papillomatosis with club-shaped downgrowths of epidermis extending into deeper tissue. The tumor showed cleft-like spaces with overlying parakeratosis. Basement membrane was intact, cellular atypia and mitotic activity were absent.  Nair et al. described verrucous carcinoma overlying plaques of erythema elevatum diutinum (EED) on the dorsum of hand. 
Histopathologic variants of SCC and their clinical behavior
Cassarino et al. has categorized cutaneous SCC into high risk (>10% risk), intermediate (3%-10%), low (≤2%), and indeterminate subtypes.  De novo SCC, SCC associated with predisposing factors, invasive Bowen's disease, adenosquamous carcinoma, and malignant proliferating pilar tumors are included in the high-risk group. Those associated with intermediate risk include adenoid SCC, intraepidermal epithelioma with invasion and lymphoepithelioma-like carcinoma of the skin, whereas low-risk SCCs include those arising in actinic keratosis, HPV-associated SCC, tricholemmal carcinoma, and spindle cell SCC (unassociated with radiation). Signet ring cell, follicular, papillary SCC, SCC arising in adnexal cysts, squamoid eccrine ductal carcinoma, and clear-cell SCC fall in the indeterminate category. An unusual case of a spindle cell SCC that presented as painful nodule with discharging sinuses and blackish nasal discharge over nose, extending to the forehead and angle of mouth has been described from India. 
In a retrospective study (unpublished data) that evaluated the predisposing factors and histopathologic type of cutaneous SCC over a period of 10 years (2003-2013), the most common site of involvement was lower limbs (41.5%) followed by head and neck (30.5%). Marjolin's ulcer was the most frequent predisposing factor observed in 43.9%, followed by inflammatory and genodermatoses in 12.2% patients. The subdivision in the latter group was as follows: 4.9% cases of genital LSA, 3.7% of DLE, 2.4% of LPH, and 1.2% of XP. No precursor lesion was identified in 42.7% patients. Histopathologically, not otherwise specified (NOS) type was observed in 40.2% cases, keratinizing type in 36.6% [Figure 7], poorly differentiated [Figure 8], verrucous and spindle cell in 4.9% each, moderately differentiated in 3.7%, basaloid in 2.4%, acantholytic and adenosquamous in 1.2% each. In a retrospective 5-year study (2005-2009) on clinicohistopathologic aspects of NMSCs, SCC comprised of 83.9% and BCC 16.1% cases. The most common age group affected in BCC group was 60-80 years, whereas that for SCC was 40-60 years. The most common site of involvement of SCC was head and neck (50%) followed by lower limb (38.4%), whereas 80% of BCCs presented on head and neck and 20% on lower limb. Histopathologically, 46% of SCCs were classified as well differentiated, 43.2% as moderately differentiated, and 11.5% as poorly differentiated. Solid nodular type was the most common variant (80%) of BCC, followed by keratotic in 20% cases.  A study from northeast India analyzing NMSCs in the head and neck region showed that SCC was more common than BCC (24 vs 13, respectively). BCC was more frequent in older age group (61-70 years) compared with SCC (40-50 years). Upper lip was the most common site for both BCC and SCC. Histopathology showed well-differentiated type to be the most common among SCC and solid type in BCC. 
|Figure 7: Photomicrograph showing ulcerated epidermis with tumor showing features of keratinizing squamous cell carcinoma infiltrating into the dermis (H and E, ×10)|
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|Figure 8: Photomicrograph showing atypical cells having vesicular nuclei, prominent nucleoli, and increased mitosis with area of necrosis in poorly differentiated squamous cell carcinoma (H and E, ×20)|
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Besides BCC and SCC, NMSCs also encompass rare malignancies such as sarcomas, Merkel cell carcinoma, and cutaneous metastasis from internal organs. Dermatofibrosarcoma protuberans (DFSP) accounts for <2% of all soft tissue sarcomas and <0.1% of all cutaneous neoplasms.  It is the most common sarcoma of cutaneous origin. DFSP commonly presents on the trunk and is an indolent low-grade tumor with a tendency for local invasion. Primary cutaneous leiomyosarcoma constitutes approximately 2%-3% of all superficial soft tissue sarcomas. It has two subtypes: Superficial dermal form that arises from the arrector pili muscle and the deep subcutaneous type from the smooth muscle of the vessel wall. Human immunodeficiency virus (HIV)-associated Kaposi sarcoma is rare in India due to low prevalence of human herpes virus- 8 in the country. It has been reported as the presenting manifestation of HIV infection from India.  Cutaneous angiosarcoma is a rare aggressive tumor that mostly presents on the head and neck region. The onset may be sporadic, following radiation therapy or long-standing lymphedema. Merkel cell carcinoma is a neuroendocrine carcinoma of the skin rarely described from India.  It is usually located on the sun-exposed sites and associated with poor prognosis.
Cutaneous metastases may occur in the setting of a known primary malignancy or may be the first indication of a silent neoplasm. In a 5-year clinicopathologic study from India, the prevalence of cutaneous metastases from internal malignancies was 2%.  Breast was the most common site of primary tumor in females, whereas in males skin metastases originated from gastric, colon, and neuroendocrine carcinoma of lung in one patient each. In 56% (8/14) cases, cutaneous metastasis was the presenting sign of an unknown primary neoplasm, of which prebiopsy clinical diagnosis was considered in only one case. 
| Conclusion|| |
Although the presence of eumelanin in dark skin is protective against the development of NMSCs, cutaneous BCC and SCC are increasingly being diagnosed in the Indian population. This is possibly because of a myriad of chronic dermatoses that have been associated with malignant potential, particularly for SCC. Dermatologists should be aware of the predisposing lesions and follow them on long-term basis for early detection of malignant change. Histopathology is valuable in establishing the diagnosis and identification of the histologic subtypes of SCC and BCC. Well-differentiated SCC and nodular BCC represent the most frequent histopathologic variants reported from India.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8]
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