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Year : 2020  |  Volume : 10  |  Issue : 1  |  Page : 1-10

Adnexal tumors of the skin in Black Africans: A 21-year comparative morphological analysis

Department of Pathology, Faculty of Basic Clinical Sciences, Ahmadu Bello University and ABU Teaching Hospital, Zaria, Nigeria

Date of Submission08-Jul-2020
Date of Acceptance14-Sep-2020
Date of Web Publication06-May-2021

Correspondence Address:
Dr. Modupeola O Samaila
Department of Pathology, Faculty of Basic Clinical Sciences, College of Medical Sciences, Ahmadu Bello University and ABU Teaching Hospital, Zaria
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ais.ais_33_20

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Background: There is limited documented literature on the occurrence of tumors of the skin adnexae in the Black African population, and the seeming rarity of these tumors as earlier reported is not unrelated to misdiagnosis with other epidermal tumors, due to their complex, overlapping, and confusing morphological features, and lack of expertise in their diagnosis.
Material and Method: A morphological analysis of all diagnosed cases of adnexal tumors of the skin in a Pathology laboratory over a 21-year period (1999-2019) using formalin-fixed paraffin-processed hematoxylin and eosin stained slides and tissue blocks subjected to special stains and immunohistochemical analysis.
Results: One hundred and sixty-two adnexal tumors of the skin were diagnosed over the 21-year period. 115 were benign and 47 malignant with an overall male to female distribution of 67: 95. The mean age overall was 40.5 years, while the mean ages for benign and malignant lesions were 35.7 years and 50.9 years, respectively. The most common benign tumors were of eccrine and apocrine differentiation, while sebaceous carcinoma was the most common malignant tumor overall with a male predominance and closely followed by porocarcinoma with a female predisposition. Three (3) patients had recurrent tumors and the diagnosis of 17 cases with generic diagnoses of benign adnexal tumor and malignant adnexal tumors were reviewed based on the 2006 WHO classification of skin tumors.
Conclusion: There is an increase in the frequency of tumors of the skin adnexae in our setting due to improved diagnostic capabilities and better health-seeking awareness among patients. These tumors have different biologic potential in terms of aggressiveness and thus require definite diagnosis for further patient management.

Keywords: Adnexal skin tumors, benign skin tumors, female skin tumors, malignant skin tumors

How to cite this article:
Samaila MO. Adnexal tumors of the skin in Black Africans: A 21-year comparative morphological analysis. Arch Int Surg 2020;10:1-10

How to cite this URL:
Samaila MO. Adnexal tumors of the skin in Black Africans: A 21-year comparative morphological analysis. Arch Int Surg [serial online] 2020 [cited 2021 Jun 16];10:1-10. Available from:

  Introduction Top

There is limited literature on the occurrence of tumors of the skin adnexae in the Black African population.[1],[2],[3],[4] The seeming rarity of these adnexal tumors as earlier reported is not unrelated to misdiagnosis with other epidermal skin tumors, particularly squamous cell (SCC) and basal cell (BCC) carcinomas, due to the complex, overlapping, and confusing morphological features of adnexal tumors, as well as lack of expertise in their diagnosis.[1],[5],[6],[7] Previously, these tumors had generic unspecified diagnosis of benign or malignant adnexal tumors without further attempt at characterization based on the adnexae lineage from which the tumor might have originated. This diagnostic approach was also compounded by the abysmal small number of practicing pathologists in the country, lack of interest in dermatopathology sub specialty, and quite significantly, the abandoning of special stains in routine practice, as well the absence of ancillary diagnostic techniques such as immunohistochemistry and molecular testing due to their prohibitive cost in our low-middle income developing setting. These techniques are particularly useful for the tumors with familial or syndrome association as seen in trichoepithelioma, spiradenoma, cylindroma, nevus sebaceous, and sebaceous carcinoma which may occur as components of the Brooke-Spiegler, Brooke-Fordyce, Muir Torre and Cowden diseases.[5],[6],[8],[9],[10],[11] There is now an interest surge in dermatopathology practice among young pathologists and pathology trainees motivated in part by physicians' insistence on having definitive diagnoses and the now aggressive health-seeking awareness by patients. This study is a morphological analysis of tumors of the skin adnexae in the last 21 years in the Pathology department of a tertiary hospital, which also renders specialist referral service for skin biopsies. Thus, our experience is fairly representative of the national distribution of these lesions.

  Materials and Method Top

We conducted a twenty- one year analysis of all diagnosed cases of tumors of the skin adnexae in the department of Pathology, Ahmadu Bello University Teaching Hospital, Zaria. All skin biopsies received in the department from 1999-2019 were retrieved from the departmental records. Formalin-fixed and paraffin-processed stored hematoxylin and eosin stained slides and tissue blocks were retrieved for newer slides in cases of faded and/or broken and/or missing slides. All neoplastic skin cases were retrieved, studied and analyzed, and skin adnexal tumors cases were extracted and collated. The adnexal tumors reviewed were categorized along adnexal line of differentiation and classified using the 2006 World Health Organization's skin tumors classification. Special stains such as periodic acid Schiff (PAS), diastase, and mucicarmine were used in confirmation of clear cell lesions, hyaline globules presence, malignant adnexal tumors of eccrine/apocrine differentiation, and differentiating trichoepithelioma from basal cell carcinoma. Oil red O, Sudan black, and immunohistochemical antibodies markers CEA, EMA, AE1/AE3, S100 were used in confirmation of sebaceous carcinoma, particularly the extraocular cases and for differential tumor diagnosis in poorly differentiated malignant adnexal cases and possible metastasis.

  Results Top

A hundred and sixty two (162) tumors of the skin adnexae were diagnosed over the 21 year study period (1999 2019). Overall, there were one hundred and fifteen (115) benign [Table 1] and forty seven (47) malignant cases [Table 2] accounting for 71% and 29%, respectively. The overall male to female distribution was 1:1.4. Of the 115 benign cases, the male to female distribution was 1:1.5, while the 47 malignant cases had 21 males and 26 females.
Table 1: Sex distribution of patients with benign Eccrine/Apocrine skin tumor differentiation

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Table 2: Sex distribution of patients with malignant Eccrine/ Apocrine skin tumor differentiation

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The ages ranged from 4 to 90 years with an overall mean age of 40.5 years. The peak age distribution overall was in the third to fifth decades of life [Table 3]. The average age for benign tumors was 35.7 years and the youngest patient aged 4 years presented with a perianal poroma. The average age for malignant tumors was 50.9 years with a range of 25–90 years and peak age in the fifth decade of life [Table 3]. The 25 years and 90 years old males had ocular sebaceous carcinoma and porocarcinoma of the knee, respectively. Interestingly, the 90-year-old man also had another primary carcinoma of the eosophagus.
Table 3: Age distribution of patients with skin adnexal tumors

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Overall, there were 112 (69.1%) tumors of eccrine/apocrine (sweat gland) differentiation with 87 (77.7%) benign and 25 (22.3%) malignant cases accounting for 53.7% and 15.4%, respectively, of the overall cases. The most common tumors were poroma (29 cases: 25.8%) and its malignant counterpart of porocarcinoma (15 cases: 13.3%), chondroid syringoma (11 cases: 9.8%), and hidradenoma (11 cases: 9.8%) [Table 1] and [Table 4]a, [Figure 1],[Figure 2],[Figure 3],[Figure 4],[Figure 5]. The tumors of follicular differentiation accounted for 14.2% (23 cases) overall with 18 (78.3%) benign and 5 (21.7%) malignant cases accounting for 11.1% and 3.1%, respectively. The most common follicular lesions were pilomatricoma and trichoepithelioma, while trichilemmal carcinoma was the most common malignant variant [Table 1] and [Table 4]b, [Figure 6][Figure 7][Figure 8][Figure 9]. Tumors of sebaceous differentiation accounted for 16.7% (27) cases overall with 17 (63%) sebaceous carcinoma of predominantly the ocular subtype having a male predominance, while the benign sebaceous cases accounted for 6.1% (10 cases) overall [Table 1] and [Table 4]c, [Figure 10].
Figure 1 (Poroma): Tumor lobules of fairly uniform cuboidal cells attached to overlying epidermis H&E stain, Mag ×40

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Figure 2 (Polymorphous sweat gland carcinoma): Tumor composed of fairly uniform cells with moderate eosinophilic cytoplasm display in papillary, tubular, and cribriform array. H& E stain, Mag × 100

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Figure 3 (Chondroid syringoma): Mixed tumor of epithelial and mesenchymal tissues H&E stain, Mag × 40

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Figure 4 (Hidradenoma): Fairly uniform lobules of cuboidal cells within a fibrocollagenized dermis H&E stain, Mag × 100

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Figure 5 (Pilomatricoma): Cystic cavity containing ghost cells and amorphous debris, cyst wall lined by basaloid cells. Note overlying epidermis in upper right corner. H&E stain, Mag × 100

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Figure 6 (Porocarcinoma): Nests pf large polygonal cells with hyperchromatic nuclei and moderate cytoplasm H& E stain, Mag × 100

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Figure 7 (Pilomatrix carcinoma): Malignant basaloid cells, marked nuclear pleomorphism with moderate cytoplasm H&E stain, Mag × 100

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Figure 8 (Trichilemmal carcinoma): Epidermal lentigenous tumor growth, malignant cells with bizarre hyperchromatic nuclei H& E stain, Mag × 100

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Figure 9 (Trichoepithelioma): Nests and lobules of basaloid cells, admixed with keratocysts and mesenchymal body in a fibrocollagenized stroma H&E stain, Mag × 40

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Figure 10 (Sebaceous carcinoma): Lobules of malignant sebaceous cells H& E stain, Mag × 400

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The sites of involvement of lesions were grouped into the face comprising the forehead, cheek, nose, lips, eyelid, and periorbital; the head comprising the scalp, peri-auricular, and ear; the trunk comprised the neck, chest, breast, abdomen, and back; the upper extremity (shoulder, arm, forearm, hand, palm, fingers), the pelvis (loin, vulva, pubis, gluteal, perianal), and the lower extremity (thigh, leg, foot, knee, sole). The most common site of involvement was the face 44 (27.2%), with the head and lower extremity having almost equal distribution of 36 (22.2%) and 35 (21.6%) cases, respectively [Table 5]. Clinical presentations were of well-circumscribed nodules, masses, pedunculated nodules, exophytic masses, and ulcerations with duration of lesions prior to presentation ranging from 2 months to several years. Clinically, less than 20% patients had correctly specified lineage skin adnexal tumor diagnosis prior to histological diagnosis. Three patients with respective histological diagnosis of trichilemmal carcinoma, microcystic carcinoma, and ocular sebaceous carcinoma presented with recurrence within 6–12 months of initial surgical excision and histological diagnosis.
Table 5: Distribution of all skin adnexal tumors by site of affectation

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Histologically, 7 cases of previously diagnosed acrospiroma were reviewed to hidradenoma (5) and poroma (2). Five cases diagnosed as benign adnexal/mixed tumor were reviewed to chondroid syringoma (2) and pleomorphic adenoma (3), while 7 cases diagnosed as malignant adnexal tumor were reviewed to porocarcinoma (4) and hidradenocarcinoma (3). The pleomorphic adenoma cases were excluded from the study.

  Discussion Top

There is an upsurge in the frequency of diagnosis of tumors of the skin adnexae globally and particularly in developing settings due to growing interest in these intriguing tumors of mixed histiogenesis.[12],[13],[14],[15],[16],[17]

Of the 162 cases analyzed in this study, 20.4% (33) were recorded in the first decade (1999-2008), while 79.6% (129) cases were recorded in the second decade (2009-2019), almost quadrupling the cases in the first decade with an annual average of 12 cases. Available studies on adnexal tumors display comparable annual frequency distribution pattern, though an earlier report from Zaria averaged 3 cases annually.[1],[13],[16],[17] This upsurge in frequency is hinged on improved specialty training, diagnostic capability, and availability of adjunct diagnostic techniques and thus negates the notion of rarity of these tumors from several reports. However, adnexal tumors are uncommon in occurrence when compared with skin tumors such as basal cell carcinoma (BCC), squamous cell carcinoma (SCC), and melanoma.

Overall, the study recorded a female preponderance comparable to reported studies by Nair, Radhika et al., and Saha et al.,[16],[18],[19] though studies by Samaila, Pujani et al., Sharma et al., and Yaqoob et al. had equal gender distribution.[1],[12],[13],[17] Pantola et al. reported a slight male preponderance.[20] Notable, adnexal tumors such as hidradenoma, hidradenoma papilliferum, papillary eccrine adenoma, and syringoma have a documented female preponderance[5],[11] which was also seen in this study. However, the distinct male prevalence of pilomatrix carcinoma was not seen in our solitary case, while the female prevalence of proliferating trichilemmal cyst (pilar tumor) and sebaceous carcinoma was also upturned in favor of males.[11],[21]

Age of predilection was in the 3rd to 5th decades of life in this study, and the wide age distribution is fairly represented in similar studies.[12],[13],[14],[16],[17],[18],[19],[20] The average age of 40.5 years overall is also comparable with other reports;[17],[22] Nair had the second decade as the most common while Saha et al.'s mean age was approximately 24 years.[16],[19] The average age of 50.9 years for malignant diseases in this analysis is a decade earlier among our African population compared to reports by Radhika et al. and Yaqoob et al.[11],[18] In general, malignancies occur 1–2 decades earlier in African population.

The sites of predilection were the face, head, and lower extremity. These sites are comparable with documented literature and other studies in Delhi, India, Zaria, and Lagos on adnexal tumor distribution pattern.[3],[5],[11],[12],[13],[14] Accurate clinical diagnosis of less than 20% reenforces the absolute need of submitting surgical specimens for histopathological diagnosis in patient's further management and counselling, particularly in lesions associated with syndromes or genetic mutations.

Benign neoplasms accounted for approximately 71% (115) of the cases, while 69.1% (112) of all the tumors analyzed were of eccrine and apocrine (sweat gland) differentiation. Comparable findings were recorded by authors from various centers.[1],[13],[18],[20],[23],[24] In this series, poroma was the most common benign tumor with a female predisposition. Poromas are morphologically composed of fairly uniform cuboidal cells dispersed in lobules within a moderate fibro-collagenized stroma and always have epidermal connection. In the past, histological variants of poroma and hidradenoma cases were often diagnosed as acrospiroma, a term that is a composite of three distinct tumors of poroma, dermal duct tumor, and hidradenoma simplex. Chondroid syringoma, and hidradenoma were the second most common benign tumors and each accounted for 6.8%, 9.5%, and 9.8% of the overall tumors, benign tumors, and sweat gland tumors, respectively. The morphological variants of hidradenoma diagnosed included nodular, solid, clear cell, and nodulo-cystic and unlike poroma, hidradenoma has no epidermal component. Hidradenoma was the most common lesion documented by Sharma et al. and Radhika et al.[13],[18] Chondroid syringoma is a mixed tumor comprised both epithelial and mesenchymal tissues and may be misdiagnosed as pleomorphic adenoma of the parotid gland, another mixed tumor, particularly when the site of involvement is not specified and a generic diagnosis of benign mixed tumor is given as seen in three reviewed cases. Solitary cases of tubular (apocrine) adenoma and papillary eccrine adenoma occurred on the face and leg of two females. Some authors believe that these two lesions are the same tumor; however, morphologically, the presence of apocrine glands and ducts with decapitation secretions is in keeping with tubular apocrine adenoma, while ducts lacking decapitation secretions, a dense concentric stroma with keratin filled cysts and microcysts are seen in papillary eccrine adenoma.[11] Both lesions have ducts and tubules lined by 2 to more lining cells with papillary projections. All six cases of hidradenoma papilliferum were seen in females and involved the vulva or mons pubis predominantly. The morphologic similarity between spiradenoma and cylindroma made some authors to coin the term spiradenocylindroma or cylindrospiradenoma[25] but these two lesions can be differentiated based on the thickened hyaline basement membrane that separates tumor islands thus simulating a jigsaw puzzle appearance in cylindroma and the presence of hyaline cylinder within tumor islands, which is absent in spiradenoma.[5],[11]

Benign tumors of follicular differentiation included pilomatricoma, trichoepithelioma, trichoadenoma, and proliferating trichilemmal cyst (pilar tumor). Two unrelated patients with trichoepithelioma had multiple variable-sized papules and nodules on the head, scalp, and face and also had affected family members. Occurrence of multiple trichoepithelioma is familial and seen in the Brooke-Spiegler-Fordyce disease,[8],[9] though our patients were not subjected to molecular or genetic testing due to unavailability and financial constraints. It is also important to differentiate trichoepithelioma from basal cell carcinoma which is a common diagnostic pitfall, particularly the keratotic and morpheariform BCC variants. Presence of stroma mucin and tumor-stroma retraction may be useful in BCC, while presence of papillary mesenchymal body, which is a cup-like nest of basaloid cell nests engulfing fibroblasts and follicular germinative cells are diagnostic pearls in trichoepithelioma.[26] Nevus sebaceous was the most common sebaceous benign lesion though some authors believe that it is a harmatoma and not neoplastic due to the conglomerate morphologic features of all adnexae seen depending on age of patients at time of presentation.[11]

Malignant adnexal tumors (MAT) are thought to be rarer than the benign counterparts from several reported studies.[12],[14],[18],[24] They accounted for 29% of cases analyzed and had a predilection for middle-aged females and elderly males in this study. Overall, malignant tumors of sweat gland differentiation were the most common; however, sebaceous carcinoma was the single most common malignancy with its ocular subtype accounting for 12 of the 17 cases seen in this study. Sebaceous carcinoma preferentially affected males in our setting in contrast to documented literature of female predominance.[11],[21] Tumor differentiation ranged from well differentiated to poorly differentiated particularly with the extra-ocular subtype that required immunohistochemistry for further characterization. Porocarcinoma was the second most common malignant adnexal tumor, and none of the patients had a previous histologic diagnosis of poroma to suggest malignant degeneration. Porocarcinoma and malignant proliferating trichilemmal tumor (MPTT) have potential for misdiagnosis as SCC due to areas of squamoid differentiation.[11],[16] Residual proliferating trichilemmal cyst is often present in MPTT and should be identified while poroid cell and ductular differentiation is a guide for Porocarcinoma. The MPTT in this analysis was located in the gluteus of an elderly aged man. Trichilemmal carcinoma was the most common malignant tumor of follicular differentiation. Morphologically, tumor cells exhibited marked cytological atypia, numerous bizarre mitosis, and confinement to the epidermis with prominent involvement of the rete ridges. Unspecified generic diagnosis of MAT as seen in 7 cases should be discouraged because individual malignant tumor have different aggressive potential and treatment should be targeted to reduce attendant morbidity. Porocarcinoma, pilomatrix carcinoma, apocrine carcinoma, and sebaceous carcinoma are high-grade tumors compared with low-grade microcystic adnexal carcinoma, mucin producing carcinoma, adenoid cystic carcinoma, and polymorphous sweat gland carcinoma (PSGC).[5],[11] PSGC may be misdiagnosed as a benign tumor due to the varied histologic features with cylindroma-like areas, though tumor cells have uniform vesicular nuclei and prominent nucleoli.

Recurrence is associated with some malignant adnexal tumors such as polymorphous sweat gland carcinoma, apocrine carcinoma, malignant chondroid syringoma, microcystic adnexal carcinoma, and pilomatrix carcinoma while incomplete excision is common with benign lesions.[11] Recurrence should also be differentiated from patients who had incisional biopsy for histologic diagnosis before definitive surgery. Three of our patients, with trichilemmal carcinoma, microcystic carcinoma, and sebaceous carcinoma had recurrent diseases 6–12 months following initial excision and histological diagnosis.

Immunohistochemistry is a useful diagnostic tool in general tumor diagnosis and was used in further characterization of some of the adnexal tumors in this study; however, it requires expert interpretation in conjunction with morphological features to achieve definitive diagnosis. Use and interpretation of immunohistochemical antibodies in isolation without recourse to morphological features is a futile exercise and waste of resources. Also, majority of the benign adnexal tumors in particular do not require immunohistochemistry for diagnosis. This view is supported by Pujani et al. in their study.[12]

In conclusion, there is an increase in the incidence of skin adnexal tumors in our setting due to better diagnostic acumen, heightened awareness, and use of ancillary diagnostic aids. These tumors have propensity for middle-aged females in our setting with different biologic potential and may be associated with recurrences. Further studies may be able to explain the female propensity particularly as cosmetic usage is not limited to any particular gender in recent time. The use of strict morphological criteria will aid identification of adnexal line of tumor differentiation for definitive diagnosis. Generic unspecified diagnosis should be discouraged in skin adnexal tumor diagnosis to reduce attendant morbidity.

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  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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