versão On-line ISSN 1806-4841
An. Bras. Dermatol. v.78 n.1 Rio de Janeiro jan./fev. 2003
CLINICAL, LABORATORY AND THERAPEUTIC INVESTIGATION
Basal cell carcinomas: anatomopathological and clinical study of 704 tumors*
Aurilene Monteiro BandeiraI; Valdir BandeiraII; José Figueredo da SilvaIII; Edmilson MazzaIV
IAdjunct Prof. of Dermatology, Federal
University of Pernambuco (UFPE) and Masters degree in Anatomic Pathology, UFPE
IIAdjunct Prof. of Anatomic Pathology, UFPE and Pernambuco University
IIITitular Prof. of General Pathology UFPE
IVAssistant Prof., Dept. of Statistics, UFPE
A retrospective and anatomopathological study was performed on 704 basal carcinomas
of 623 patients, diagnosed from 1991 to 1996, at the Dermatopathology section
of the Dermatology Clinic of the Hospital das Clinicas, UFPE and at a private
dermatopathology laboratory in the city of Recife.
OBJECTIVE: To characterize the clinical and anatomopathological aspects of the basal cell carcinomas diagnosed by the two services of Pernambuco region.
METHODS: For the clinical study, the data were collected from the patient files and for the anatomopathological, macro and microscopic study a revision was made of the histological specimens. For determination of vertical growth, methods were used based on Clark and Breslow's histoprognostic techniques applied to malignant melanoma.
RESULTS: Clinical: the highest incidence was in the feminine sex (55.7%) and in the 55 to 72-year-old age group. Disease duration was highly variable, ranging from one month to 40 years, and the head was the most frequent topographical area (73.8%), mainly nasal (21.1%) and zygomatic (18.5%). The nodular pigmented form (47.4%) was found most frequently and the size of the lesions did not depend on the disease duration. Histologically the patterns considered based only on the parenchymal arrangements, were the adenoid, compact, plexiform Pinkus fibroepithelioma, pseudocystic, reticulated, superficial and trichoepithelioid, though predominantly the adenoid form (28.3%). The mean growth involved 2/3 of the reticular dermis (32.4%), and the deepest tumors presented intense fibroplasia. There was concomitance of several cellular types within a single tumor and melanin pigment was found mostly in the trichoepithelioid type.
CONCLUSION: The clinical and anatomopathological characterization of the basal cell carcinomas is of fundamental importance at these services, where there is no major difference between groups, calling attention to behavioral definitions and propositions for the histopathological report of these tumors.
Keywords: carcinoma, basal cell.
The first clinical descriptions of basal cell carcinoma were made by Jacob in 18271 when he showed that the ulceration differed from cancroid, without determining regional adenopathy. He proposed the designation ulcus rodens, which Darier2 described as a special lesion in both clinical and structural aspects.
From the first studies of its histogenesis up to the present time, the tendency has been to credit the origin of basal cell carcinomas as having started from the basal cells of the epidermis and cutaneous annexes.
Krompecher (1900)3 noted certain similarities between the basal cells of the epidermis and the cutaneous annexes, and the peripheral cells in the arrangements of parenchymal tumors. Based upon his observations, which showed their origin to be within these structures, he named it basal cell epithelioma in 1903.
Lever (1948)1 thought that the basal cell carcinoma tumor was of embryonic origin derived from structures linked to the cells of the primary epithelial germ, therefore he denominated it a nevoid tumor or organoid hamartoma.
However, Abulafia,1 based on 12 years of observations, showed the existence of a histological rather than a cytological continuity of the epitheliomatous growths within the epidermis and cutaneous annexes. He also reported that there was organoid annexal and architectural differentiation, with hyperplasia in the melanocytes and a high degree of embryonic inductive activity similar to that of the pilar follicle in the anagen phase. In view of this, he suggested the term fetal adnexal epitheliomas.
The development of stroma in its constitution and interaction with basal cell carcinomas was noted by Pinkus in 1962 and in 1967.2 At that time, he showed that this involved organized mesodermic tissue, without, however, accompanying the parenchymal development. Despite the local invasion, he considered that these tumors were not totally malignant. Later, however, he observed some metastases.
The objective of the present work was to clarify the clinical and histopathological behavior of basal cell carcinomas, especially in the dermatopathology services of the Pernambuco region. This area is subject to a high incidence and consequent ready availability of biological material. Furthermore, this work offers an important contribution in view of the lack of regional bibliographical references on the subject. Statistical analysis was used to verify the existence or nonexistence of significant differences and associations in the variables under research.
MATERIAL AND METHODS
The clinical and the anatomopathological aspects of 704 cases of basal cell carcinomas that occurred between 1991 and 1996 were studied. Of these, the study material of 189 cases was provided by the Dermatopathology Laboratory of the Dermatology Clinic of the Hospital das Clinicas, Federal University of Pernambuco (HC-UFPE) and a further 515 by a private laboratory of dermatopathology in Recife. These were cases involving primary tumors that had not been submitted to any prior therapeutics but had been removed by complete surgical excision. Some individuals presented more than one tumor, accounting for the total of only 623 patients. The cases were divided into two groups, the first (Group 1) included the patients of the Dermatology Clinic, HC-UFPE, and the second (Group 2), those of the private laboratory.
In the clinical study, data collected from records of each laboratory were considered (gender, age, origin and patients' color; duration of the disease and the topography of the lesions).
The anatomopathological study was an evaluation of the macro and microscopic morphological aspects. The morphological macroscopic data were extracted from patient files, registering the form, color and measurements of the tumors. The morphological microscopic data was gathered by a revision of the histological preparations of each tumor, and from a diagnosis by optical microscopy of epidermal, parenchymal aspects, stromal alterations and tumor extension. The histological preparations, when necessary, were submitted to depigmentation by potassium permanganate and, for the study of fibrosis, to Masson's trichrome stain.4
To measure tumoral extension, a millimetric reference lens of MCM 1 1 100 MF 33F B KR - 207 21mm was used in the ocular lens, in conjunction with a 4/0.12 objective lens gauged with an Olympus OB-M-1/100 micrometric objective lens.
The histopathological aspects were evaluated by the author and then rechecked by a pathologist on the basis of predetermined parameters. In this manner, the histological pattern was established only according to the arrangements of the tumor cells, and the cellular type in each tumor, relative to the predominant aspects.
The palisade and spaces of parenchymal-stromal (Figure 1) retraction were observed and classified according to their presence and amount of involvement, into one third (slight degree); two thirds (moderate degree) or three thirds (accentuated degree) of the tumor.
Pigment with focal distribution in the parenchyma or in the stroma (Figure 2) was evaluated, for area and quantity, into slight (rare and scarce), moderate (some and more condensed) and accentuated (several, but considerably condensed).
Fibroplasia was interpreted as slight (delicate collagen fibers, few fibroblasts, and the parenchyma predominant over the stroma); moderate (collagen fibers more compact, the presence of regular fibroblasts and the stroma tending to be balanced); and accentuated (compacted collagen, rich in fibroblasts, sometimes with sclerotic hyaline, stroma predominant over the parenchyma).
Inflammatory infiltration was considered in terms of focal and diffuse distribution. Focal distribution was classified as: slight (rare focuses with few inflammatory cells); moderate (several focuses with a number of regular inflammatory cells) and accentuated (numerous focuses, sometimes confluent, or extensive). In the diffuse distribution, occupying the peri- and intra-parenchymal stroma, the same degrees of intensity mentioned above were applied.
Quantification of the tumor extension was based on the histoprognostic methods for malignant melanomas (Clark and Breslow), with invasion levels considered dermal (papillary with one, two, or three thirds reticular); hypodermic and muscular. The depth of tumor thickness was measured starting from the epidermal basal layer, but in ulcerated lesions, starting from a neighboring area presenting a complete epithelium.
The significance level adopted in statistical tests was 5%. The software used for statistical calculations was Statistical Analysis System (SAS / STAT).5
Of the 704 tumors studied, 189 (26.8%) were in Group 1, and 515 (73.2%), Group 2. Table 1 presents the distribution of the cases according to year and group, showing demonstrating an irregular frequency that has increased in the last few years.
In the distribution of patients according to the number of tumors, it was significant that the majority had only one tumor (89.2%). As for gender, females constituted 55.7% of the total, and males 44.3%, this did not show a significant difference (c2 = 0.198 and P = 0.657).
Regarding patients' age (Graph 1), this ranged from 18 to 90 years, with a predominance between 55 and 72 years (42.6%). In Group 1, the mean age was 60.57 years, and the standard deviation, 13.77 against Group 2, 56.45 years and 15.52, respectively. Mann-Whitney test indicated a significant difference (Z = 2.32 and P = 0.00199).
Table 2 shows the patients' distribution according to their regional origin: Recife, Greater Recife (both coastal) and inland cities, the majority being inhabitants of inland areas (55.3%). Of those living along the coast, Group 2 contributed a larger percentile (18.75%).
Most of the patients had leukoderma (78.4%), though there was a higher frequency in Group 2 (81.7%) than in Group 1 (70.2%), revealing a significant difference (c2 = 8.99 and P = 0.0031).
The duration of the lesions varied from one month to 40 years for all the patients, with a mean of 2.49 years, and a standard deviation of 3.81, indicating high variability, according to the coefficient of variation (C.V. = 153.01%). For Group 1, the mean was 2.75 years, the standard deviation, 4.68, and C.V., 170.18%. In Group 2, t was 2.29 years, 2.98 and 130.13%, respectively. In about 54.1% of the cases registered, the course of the disease was one year, and, in 20.7%, two years.
Considerable similarity can be observed between Groups 1 and 2. As for coloration of the tumors, the pigmented (47.4%) and the whitish (45.8%) were the most representative.
In the longitudinal dimension, the median values differ by 0.10mm in favor of Group 1, with reasonable to high variability, indicating a significant difference between the two groups (Z=2.0511 and P = 0.0403). In the transversal measurement, the variability was also from reasonable to elevated and strongly significant between the groups, as shown by the results of the Mann-Whitney test (Z=3.0100 and P = 0.0026), while in Group 1 the mean (0.65) and median (0.6) was higher than Group 2 (0.61 and 0.5, respectively).
There was a notable similarity in tumoral behavior in both groups. For which reason, some analyses were performed simultaneously.
Table 3 presents results of the histological patterns found in all of the tumors, of various types, classified according to the consulted literature. Thus only the main pattern in each tumor was considered, of these the adenoid (28.3%) and the compact (27.4%) were the most frequently observed.
In the relationship between the histological pattern and the type of cell, it was possible to show the predominance of basaloid cells in the six analyzed patterns. At the same time, in the reticulated, trichoepithelioid and superficial specimens there was also, significantly, the presence of fusiform cells (32.4%, 25.5% and 8.1%); in the adenoid, clear cells (17.1%); compact, transitional cells (15.5%); and pseudocystic, squamous cells (10.8%).
Palisade cells were present in 90.5% of the tumors, occurring more in Group 1 (44.4%) than in Group 2 (39%), with accentuated intensity (94.7% and 88.9%, respectively). Relating the histological pattern to the palisade, the result showed a very low significance probability P of the Chi-square test of independence or association (c2 = 39.323 and P = 0.001).
The spaces of parenchymal-stromal retraction (cracks) were frequently found (93.2%) in the total group, predominantly in areas of accentuated intensity (37.6% and 47.4%). In relation to the histological pattern, the reticulated pattern stood out because it showed moderate (35.3%) and slight (29.4%) intensities, suggesting a very significant association (c2 = 45.492 and P <0.0001).
Pigment in the parenchyma appeared in only 20.3% of the tumors with slight intensity (11.1%); in the stroma, in 22.1%, also with slight intensity, mainly in Group 1 (32.3%). The association of the histological pattern with the pigment in the parenchyma and/or stroma was seen more in the trichoepithelioid pattern and especially in those with accentuated intensity.
In both groups fibroplasia was present in 95% of the cases, being predominant in areas of slight intensity (39.9%) mainly associated with the reticulated pattern (29.4%). There is a very strong significance in this association (c2 = 85.030 and P <0.0001).
In measuring the extension of the tumors, it was found that Group 2 reached a vertical growth of 0.05 to 0.45mm (38.5%) and Group 1, 0.46 to 0.85mm (39.3%). The median for the patients as a whole was 0.49mm; in Group 1, 0.71mm and in Group 2, 0.49mm, demonstrating a significant difference between the two groups (Z = 8.043 and P <0.0001). In the analysis of the levels of involvement of the tumors, most tumors (31.4%) involved two thirds of the reticular dermis.
In the study of the relationship between the histological pattern and the level of dermal and hypodermic involvement (Table 4), the pseudocystic pattern stands out (48.7%) having a greater depth, involving three thirds of the reticular layer and revealing a very significant association (c2 = 354.413 and P <0.001). However, in the comparison of vertical growth with fibroplasia (Table 5), the greater the tumors' depth, the more accentuated was the fibroplasia, according to the level of significance adopted (c2 = 9.674 and P = 0.022).
In relating disease duration to the measurements of tumoral growth, using the Pearson® coefficient of correlation, none were significantly above zero.
Inflammatory Infiltrate in the total group more frequently showed a focal distribution and slight intensity (38.8%), however, it was seen that when the distribution was diffused, the predominant intensity was moderate (16.5%).
Of the epidermal alterations, such as the tumor covering, atrophy was the most frequently observed in both groups (71.6%).
Basal cell carcinomas are the most frequent cutaneous malignant tumors. Every year the incidence of these tumors is increasing, mainly in countries located in the low latitudes or with strong solar radiation.6-10 Although there are records that show that some appear as a consequence of other less frequent factors.11,12
The findings in the 704 cases of basal cell carcinomas registered in the two services coincide with those in national and international literature regarding factors of irregular frequency, age group and increase in incidence in recent years.7,10,13 Although it has been mentioned above that several tumors may belong to the same patient, most patients presented only a single lesion. These observations are similar to those of Kikuchi and col.,14 who studying 243 Japanese patients with basal cell carcinomas, reported multiple lesions in only four patients.
In spite of the majority being of the female gender, the difference was not significant, corroborating the results obtained in other populations (Asian, African, Mexican and Spanish).14,15,16
The tumor is more frequently found to occur between the third and fifth decades of life,17 although, in this work, the youngest patients had been registered at the age of 18 years and the oldest at 90 years of age, this being similar to that reported in other work.9,18 Some authors consider such extreme ages to be less frequent.14,15
Goldberg19 demonstrated that, when individuals submit themselves to solar exposure at around 20 years of age, a carcinogenic process begins that results in a delayed manifestation eventually seen in the period from about 40 to 60 years of age, thus explaining the source of the tardive cumulative effects.
In evaluating the relative importance of the coastal lifestyle, it was found that it was not a significant factor for greater incidence of basal cell carcinomas, but attention was called to the continuous solar exposure of those who do not live on the coast 20,6 but that habitually spend much of their lives out-of-doors.13
The disease duration of the tumors presented great variation, from one month to 40 years. Genetic studies justify this length of time, showing replication of DNA with a prolonged phase of synthesis. Clinically, the tumor takes years to double its size due to the small percentile of active proliferative tumoral cells.21
In this analysis, the main locations of the tumors were: head (73%), anterior (9.9%) and posterior (9%) areas of the trunk, superior (5.5%) and inferior (1.7%) members. In the head, they were mainly on the scalp (6.2%) and forehead (10.1%), orbital (6.3%), auricular (2.1%), mastoid (1.8%), zygomatic (18.5), nasal (21.2%), buccal (2.6%), mental (1.2%) and cervical (3.8%) areas. Such results are similar those reported by Grosshans.22
As for unusual locations, there is a report of a case in in the urogenital (vulvar) area, similar to that found at Harvard University.23 Also there was one in a gluteal location, an area that was not mentioned in reports in the consulted literature. It is important to call attention to the reports of tumors in areas not limited to the face.6
As in the clinical forms, the histological forms also presented variations,11,24,25 most of which were in the small tumors, coinciding with the information in the literature.26 Few tumors present a single histological pattern.27 The definition adopted here was based only on the form of presentation of these arrangements, considering that stromal alterations should not be included in the nomenclature of basal cell carcinomas, but that these alterations provide data relevant to a conclusive diagnosis of tumoral behavior. While remaining in accordance with these parameters, it should be noted that some authors exclude from the literature several histological patterns of basal cell carcinomas that are included here; these are, however, based on the consulted literature. For example, the Pinkus type which has a reticulated pattern was considered special according to the observations of Grinspan & Abulafia.28
The variation in histological patterns was justified by Petersen in 1902, Madsen in 1941 and Foot in 1947.29 Using a three-dimensional study of basal cell carcinomas they showed the impossibility of an exact image - in that what one sees is only an approximation of the true histological pattern. Others consider that there are architectural modifications taking place resulting from the development and deepening, and that these hinder the imaging in the histological sections.18,29,30,31 This being the case, the superficial pattern seen presented a highly varied architecture, everything from compact, adenoid, reticulated and trichoepithelioid arrangements, with single or multiple growths connected to the epidermis.29,32,33
The cellular variations were grouped into five types, these were seen to be in a complex arrangement in each tumor and rarely presented as pure.1,27,34,35,36
There was agreement with the literature in reference to the palisade, as a constant characteristic of basal cell carcinomas. On the other hand, its absence and the variation of intensity found in the reticulated pattern (23.5%) were not considered in the literature consulted.25,27,37
The spaces of parenchymal-stromal retraction were always very much in evidence, seeming to corroborate the observations of Miller.21 This apparently indicates that they result from desmosome alterations and a decrease in collagen from the collagenase synthesis.
Some tumors presented more squamous cells as an epidermoid differentiation, which is an important factor in their aggressive behavior38 and their greater growth at depth,31,32,33,37 Most of the time (31.4%), they did not exceed 1mm, in spite of the fact that tumors present more intense fibroplasia if they penetrate deeper.37,39,40
The inflammatory infiltration, besides the lymphocytic elements, was occasionally composed of plasm cells and mast cells, mainly in ulcerated areas representing the local immunity.40,41 It has been demonstrated that the presence of the mast cells participates in the synthesis of glycosaminoglycan in the fibroblastic proliferation and in the tumoral aggressiveness.21,40
Although the present work was performed with a separation into two socially different groups, the social inequalities did not produce sufficient significant data to allow specific conclusions to be applied to each group.
1 - Basal cell
carcinomas are occurring with greater and abnormal frequency mainly in the last
few years. There is a slight bias in the female gender. The age group having
the greatest probability is from 55 to 72 years, pointing to the growing emergence
in a younger population.
2 - In tropical areas, living on the coast in itself is not a significant factor for higher registrations of incidence of basal cell carcinomas, but rather continuous solar exposure arising from peoples' life styles.
3 - They are tumors that develop slowly in the first two years. Their size does not depend on the disease duration.
4 - The most common locations were the head (nasal and zygomatic) and (though with few registrations) superior and inferior members.
1 - The nomenclature
of these histological patterns should be based only on the arrangements of the
parenchymal cells, thus making the language more uniform. The patterns researched
were: adenoid, compact, plexiform, pseudocystic, reticulated, trichoepithelioid,
Pinkus fibroepithelial and superficial. The superficial has similar arrangements
to several other patterns, showing it to be but a stage of their development.
Of them, the most frequent were the adenoid and the compact.
2 - Basaloid cells, as prototypes of basal cell carcinomas, were found more often, followed by the fusiform, transitional, clear and squamous; squamous cells were seen more in the pseudocystic pattern, and fusiform in the reticulated pattern. These are considered to be the more aggressive tumors.
3 - Palisade cells were always very present with accentuated intensity, but generally seen more in the compact and reticulated patterns.
4 - The spaces of parenchymal-stromal retraction and the melanin pigment (parenchyma and stroma), in any distribution, were more frequent in the trichoepithelioid pattern.
5 - Most of the tumors had little deep growth, but the cellular type of the tumoral parenchyma and fibroplasia interfered in that growth.
6 - The inflammatory infiltrate of basal cell carcinomas was usually focal and of mild intensity, and rarely diffuse.
7 - The histological behavior of the tumors was similar in both groups from the public and private dermatopathological services.
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Aurilene Monteiro Bandeira
Rua Padre Roma, 688 - apto. 2002
Recife - PE 52060-060
Tel: +55(81) 3267-6155 / 9975-7764
Fax: +55(81) 3327-1396
Received in March, 16th of 2000.
Approved by the Consultive Council and accepted for publication in August, 22th of 2002.
* Work done for Masters thesis in Anatomic Pathology, Federal University of Pernambuco.