Review Article
Clinicopathological Evaluation of Pigmented Skin Lesions: A Retrospective – Analytical Study
Abstract
Background and Objective: We aimed to study various pigmented skin lesions (benign and malignant) and their clinicopathological characteristics to prevent malignant lesions progression and early detection of them from benign ones.
Methods: This descriptive cross-sectional retrospective study was done by census sampling method on all patients referred to the Department of Dermatology with pigmented skin lesions who underwent biopsy between 2010-2020. Patients’ data were extracted from the pathology ward by pre- prepared checklist that included age, sex, pathology report, margins status, and anatomical location. Data were entered into SPSS22 software, and analyzed by Chi-square and ANOVA tests. A P-value less than 0.05 was considered statistically significant.
Result: Totally 1127 patients with a mean age of 46.55 +_ 21.03 were studied. Of these, 46% were male and 54% were female. Benign lesions were 66.7% and malignant lesions were 33.3%. The most common malignant lesions were epithelial tumors (85.6%) and malignant melanoma respectively. The correlation between malignant lesions and Patients’ age was statistically significant (p-value=0.025). Benign lesions were most common in patients between 19 to 39 years old. Head and neck were the most common sites for both malignant and benign pigmented skin lesions. The overall frequency of lesion size was between 0.5 – 0.74 cm. In 84.3% of the lesions, the margins were free from the tumors.
Conclusion: All pigmented skin lesions in elderly persons require investigation to exclude malignancy, especially malignant melanoma.
Keywords: pigmented skin lesions, melanoma, melanocytic nevus, non- melanocytic pigmented lesions
Introduction
Skin is made-up of three layers of the epidermis, dermis and sub-cutis tissues. Due to melanin, blood, external pigments (tattoo), the pigmented skin lesions are brown, black or blue in color, and these lesions are one of the most common samples sent to the pathology departments for diagnosis [1, 2]. These lesions could be seen in both inherited and acquired diseases. Involvement of the skin in acquired diseases may be due to skin diseases or part of the clinical symptoms of systemic diseases. Climatic conditions or ultraviolet rays play an important role in causing skin damages [3]. The prevalence of benign and malignant lesions is different in men and women depending on the type of the lesion [1] In TM Skender-Kalnenas et al study, the role of benign pigmented lesions was investigated as initiators or markers of cutaneous melanoma. The results of this study further supported acquired and dysplastic nevi as precursors of cutaneous melanoma. In addition, lesions diagnosed as simple lentigo and solar lentigo should be considered as possible precursors of melanoma, especially in the elderly [4,5] One of the most lethal types of skin cancer is melanoma, in which 4% of all of skin cancers are involved. The causes of melanoma are still not clear, but one of the reasons is exposure to sunlight [6, 7]. Old age and diabetes are risk factors for increased mortality in this lesion [8]. Benign lesions need regular examination for a long time, especially in younger patients. Although benign lesions have very little potential to progress to melanoma [8, 9], many of these lesions tend to be malignant and metastatic throughout lymphatic network. The treatment methods of malignant lesions include radiotherapy and removal of the tumor with sufficient margins [9,10]. Identification of predisposing factors, planning for disease prevention, accurate diagnosis, rapid treatment of malignant and pre-malignant pigmented skin lesions can increase patient survival [11]. Considering the strong association of pigmented skin lesions with sunlight and dry and extensive sunlight in the Yazd city, easier treatment by early identifying most common lesions in the province and lack of simultaneous study of benign and malignant pigmented lesions, we decided to investigate clinico-pathological characteristics of pigmented skin lesions in the samples sent to the pathology department of Shahid Sadoughi and Shahid Rahnemoun hospitals and offer new strategies for disease prevention, recurrence and treatment.
Material and Methods
This cross- sectional retrospective study was approved by the ethics committee of Shahid Sadoughi University of Medical Sciences, Yazd, Iran (IR.SSU.MEDICINE.REC.1398. 170). All patients with clinical diagnosis of benign and malignant pigmented skin lesions that underwent skin biopsy and referred to Shahid Sadoughi and Shahid Rahnemoon General hospitals were entered into the study. Sampling was performed by the census method. All patients with pigmented skin lesions were included in the study and those whose slides or paraffin blocks were absent, or who was unwilling to cooperate for the completion of the clinical information were excluded. Then, a questionnaire was designed based on age, sex, pathology report, anatomical location and thickness of the lesion. Collected data were entered into the SPSS software version 22 and were analyzed by Chi-square, t-test and ANOVA tests. P value less than 0.05 was considered statistically significance.
Results
Totally 1127 patient’s data were studied. The mean age at the time of diagnosis was 46.55 ± 21.03, minimum and maximum ages were 1 and 96 years, respectively. Of them 518 were male (46%) and 609 were female (54 %). The t-test results showed a significant difference between the average age of diagnosis between men and women, such that the average age of men was higher than the average age of women (p-value<0.001) at the time of diagnosis. Finally, 752 patients (66.7%) with benign lesions and 375 (33.3%) with malignant lesions were reported. The average of patients’ age with malignant lesions were significantly higher than the average of patients’ age with benign lesions (p-value<0.001). The most anatomical site of involvement was head and neck (76.1%). In 84.3% of the pigmented lesions the margins were free from tumoral cells. The average of patients’ age with involved margins were significantly higher than the average of patients’ age with free margins (P-value<0.001). The absence of ulceration was reported in 93.5% of the pigmented lesions. Significant difference between the average of patients’ age with and without ulceration was reported (P-value<0.018). The frequency of benign lesions was significantly higher in women with 465 patients and malignant lesions in men with 231 patients (P-value<0.001). The frequency of benign and malignant lesions was significantly highest in the head and neck area (P-value<0.001). According to Chi-square test, the probability of margins involvement (p-value <0.001) and concomitant presence of ulceration were significantly highest in malignant lesions (P-value<0.001).
Findings of benign pigmented skin lesions
In terms of benign lesions, 61.8% were females and 38.2% were males. The most frequent age group was 19 to 39 years, with 312 cases (41. 5%). The most common site of involvement was head and neck with 530 patients (70.5%) and the lowest frequency were in the upper extremities with 40 patients (5.3%). The highest frequency of benign lesions thickness was in the range of 0.25 to 0.74 cm with 276 cases (36.7%) and the lowest frequency was in ≥ 1 cm in 28 cases (3.7%). Also, the margins were free from the tumor for 700 cases (93.1%) and for 52 cases (6.9%) the margins were involved.724 cases (96.3%) did not have concomitant presence of ulceration with pigmented lesions. Based on Chi-square test, various types of benign lesions were significantly related to age in this study. Thus, benign tumors at the age of ≥ 60 years have the highest frequency (P-value<0.001). Also, congenital nevus and benign tumors were significantly higher in men, acquired melanocytic nevus, inflammatory and vascular lesions were significantly higher in women (P-value<0.001). According to Fisher’s exact test, all types of benign lesions were significantly higher in the head and neck (P-value<0.001).
Table 1: Frequency distribution of benign pigmented skin lesions based on sex, age, anatomical Sites
Acquired melanocytic nevus | Congenital nevus | Benign tumors | Inflammatory lesions | Vascular lesions | Total | ||
---|---|---|---|---|---|---|---|
Sex | Male | 146 31.5% | 40 54.8% | 71 50.7% | 26 42.6% | 4 28.6% | 287 38.2% |
Female | 318 68.5% | 33 45.2% | 69 49.3% | 35 57.4% | 10 71.4% | 465 61.8% |
|
Age | ≤ 18 Years | 64 13.8% | 26 35.6% | 5 3.6% | 8 13.1% | 1 7.1% | 104 13.8% |
19-39 | 216 46.5% | 38 52.1% | 27 19.3% | 26 42.6% | 5 35.7% | 312 41.5% |
|
40-59 | 133 28.7% | 7 9.6% | 46 32.8% | 19 31.1% | 6 42.9% | 211 28.1% |
|
> 60 | 51 11.0% | 2 2.7% | 62 44.3% | 8 13.1% | 2 14.3% | 125 16.6% |
|
Anatomical site | Head and neck | 360 77.6% | 57 78.1% | 84 60.0% | 21 34.4% | 8 57.1% | 530 70.5% |
Trunk | 47 10.1% | 9 12.3% | 34 24.3% | 14 23.0% | 1 7.1% | 105 14.0% |
|
Upper extremities | 20 4.3% | 3 4.1% | 8 5.7% | 8 13.1% | 1 7.1% | 40 5.3% |
|
Lower extremities | 37 8.0% | 4 5.5% | 14 10.0% | 18 29.5% | 4 28.6% | 77 10.2% |
|
Total | ---- | 464 100.0% | 73 100.0% | 140 100.0% | 61 100.0% | 14 100.0% | 752 100.0% |
Also, thickness of 0.5 to 0.74 was significantly frequent in acquired melanocytic nevus, benign tumors, inflammatory and vascular lesions and 0.25 to 0.49 cm was significantly frequent in congenital nevus and inflammatory lesions (P-value<0.001). Ulceration was significantly frequent in vascular (benign) lesions (P-value<0.001). In this study, acquired melanocytic nevus include: 86% intradermal nevus, 8% compound nevus, 1% junctional nevus, 3% blue nevus, 1% spitz nevus, and 1% simple lentigo nevus. Intradermal nevus with 86% was the most frequent among acquired melanocytic nevus. This lesion was more common in the age group of 19 to 39 (48.11%) and in women (70.79%). The most common anatomic site involved in the study for intradermal nevi was head and neck (81.61%). Pigmented Seborrheic keratosis was the most common lesion among benign tumors with 71%. This lesion was more common in men (53.53%). Ages ≥60 had a significantly higher frequency with 51.52%. The most common anatomical site for the lesion was head and neck (66.7%).
Findings of malignant lesions
Out of 375 cases with malignant lesions, epithelial tumors were the most frequent type (85.6%). The highest frequency of these lesions was in the age of ≥60 years with 245 cases (65. 3%), and the lowest frequency of group’ ages was at <_ 18 years with 2.4% (9 patients). Anatomical site was head and neck in for 328 patients (87.5%), trunk in 15 patients (4%), upper extremities in 8 patients (2.1%) and lower extremities with 24 patients (6.4%). The highest frequency of thickness for malignant lesions were in the range of 0.25 to 0.49 cm in 128 cases (34.1%) and the lowest was 1≥ cm in 22 cases (5.9%). Surgical margins in 250 cases (66.7%) were free from the tumors. Ulceration with malignant lesions was reported in 330cases (88%). According to the Fisher’s exact test significantly malignant tumors were higher in patients ≥60 years old (P-value=0.025). Also, no significant correlation was observed between type of malignant lesions and gender (P-value = 0.371). Melanoma, epithelial tumors in the head and neck and vascular tumors in the lower extremities were significantly highest according to Chi-square test (P-value<0.001). According to Fisher’s exact test, the highest frequency of melanoma was observed in thickness of 0.49-0.25 and 0.74-0.5 each with 15 cases and also the highest frequency of epithelial tumors was observed with the thickness of 0.49-0.25 (P-value=0.023). Ulceration of malignant lesions were significantly more common in malignant epithelial tumors (P-value=0.001).
Table 2: Frequency distribution of malignant pigmented skin lesions based on patients’ sex, age, anatomical site, thickness and ulceration
Melanoma | Vascular tumors | Epithelial tumors | Total | ||
---|---|---|---|---|---|
Sex | Male | 29 56.9% | 3 100.0% | 199 62.0% | 231 61.6% |
Female | 22 43.1% | 0 0.0% | 122 38.0% | 144 38.4% |
|
Age(years) | ≤ 18 | 4 7.8% | 0 0.0% | 5 1.6% | 9 2.4% |
39 – 19 | 5 9.8% | 0 0.0% | 14 4.4% | 19 5.1% |
|
59 – 40 | 17 33.3% | 1 33.3% | 84 26.2% | 102 27.2% |
|
≥ 60 | 25 49.0% | 2 66.7% | 218 67.9% | 245 65.3% |
|
Anatomical site | Head and neck | 22 43.1% | 0 0.0% | 306 95.3% | 328 87.5% |
Trunk | 8 15.7% | 0 0.0% | 7 2.2% | 15 4.0% |
|
Upper extremities | 4 7.8% | 1 33.3% | 3 0.9% | 8 2.1% |
|
Lower extremities | 17 33.3% | 2 66.7% | 5 1.6% | 24 6.4% |
|
Thickness | ≤0.25 | 5 9.8% | 1 33.3% | 67 20.9% | 73 19.5% |
0.25 - 0.49 | 15 29.4% | 1 33.3% | 112 34.9% | 128 34.1% |
|
0.50 - 0.74 | 15 29.4% | 1 33.3% | 102 31.8% | 118 31.5% |
|
0.75 – 1 | 8 15.7% | 0 0.0% | 26 8.1% | 34 9.1% |
|
≥1 | 8 15.7% | 0 0.0% | 14 4.4% | 22 5.9% |
|
Ulceration | With | 3 5.9% | 3 100.0% | 39 12.1% | 45 12.0% |
Without | 48 94.1% | 0 0.0% | 282 87.9% | 330 88.0% |
|
Total | --- | 51 100.0% | 3 100.0% | 321 100.0% | 375 100.0% |
Discussion
This study was performed on 1127 patients with benign and malignant pigmented skin lesions with a mean age of 46.55±21.03, including 46% males and 54% females. Benign pigmented lesions had the highest frequency. In a similar study by Reza Nemati Ahmadabad on 46 patients with 62 acral pigmented skin lesions ranging in age from 2.5 to 75 years with a mean age of 35.53 years, with 44% men and 56% women, pigmented lesions had the highest frequency. But in other similar studies, malignant lesions were more common than benign lesions. This difference is justified since prevalence of malignant pigmented lesions were higher in men than women and the predominant group was men in these studies [4, 9, 14-16]. More involvement of women than men in benign pigmented skin lesions was observed in this study, which is consistent with the statistics of reference books and similar previous studies [9]. In our study, intradermal nevus with 85.56% were the most frequent subgroup in acquired melanocytic nevus, this lesion was mostly seen in the age group of 19 to 39 years and the predominant group were women. The most common anatomical site for intradermal nevus was the head and neck. In a similar study by Magda Martinkaz, the most common melanocyte nevi were intradermal nevus (44%) with 45% involvement of trunk and 35% involvement of head and neck, probably because these anatomical sites were more exposed to direct sunlight. But in other similar studies, intradermal nevus was not the most common lesion [4, 5, 17] Sixteen cases of blue nevus were found in our study and were categorized into the acquired melanocyte nevus group, and it was more common in women with the average age of 37. These lesions were observed in the lower extremities and often in the age group of 19 to 39. In previous studies, the most common anatomical site was reported to be the head and neck, which is one of the most common sites mentioned for this lesion in reference books. Also, women were more frequently affected than men, but the average age of the patients were higher than our study and reference books, and unfortunately, we did not find a justification for this higher average age [18-20]. In our study, 4 cases of Spitz pigment were seen, 2 females and 2 males. In the anatomical site of the head and neck, trunk, upper and lower limbs with an average thickness of 0.42 cm were reported. In other similar studies, women were more frequently affected than men. The most common anatomical site was reported to be the lower extremities. In our study, unlike previous studies, determining the frequency distribution in age group and anatomical location could not be investigated due to the small number of patients [21, 22]. In this study, congenital nevi accounted for 9.7% of cases, and were often seen in men. The highest frequency of this lesions was in the age group of 19 to 39 years and in the head and neck. In a similar study by Murat Orhan, in the Turkish Department of Dermatology, 2913 patients with pigmented lesions in the age range of 1 month to 63 years were studied. 239 patients (8.2%) with congenital nevus and average age of 20.76±13.76 were reported. 52.3% of cases were women. The most common anatomical sites were the upper extremities, followed by the head, neck, trunk and lower extremities. In a study by Leyli Changchien et al. on 77 patients with congenital nevus in the age range of 1 month to 70 years and the mean age of 26 years, similar to our study, men (53%) were more likely affected than women [23, 24]. Congenital nevi were quite benign, but the giant nevi had become the melanoma with the likelihood of 5 to 10%, and nervous system involvement was important. In case of encountering this lesion, it’s better to take appropriate and timely treatment [25]. Among benign tumors in this study, pigmented seborrheic keratosis had the highest frequency. This lesion was more common in men and in the age group of ≥60. The most common anatomical site for this lesion was the head and neck. Excisional biopsy was performed for these lesions. In a previous study, similar to our study, this lesion was reported to be more highly frequent in the age group of >60 and the most common anatomical site was in the head and neck. But unlike our study, women were more frequently affected than men [26]. In this study, malignant pigmented skin lesions were more common in men, which was consistent with other studies. That’s because men with outdoor jobs were more exposed to sunlight, which is one of the important risk factors for skin cancer [9]. In this study, melanoma was most common in the age group of >60, which was consistent with previous studies on melanoma and indicates age is a risk factor for melanoma [5, 8, 22, 27-29]. In our study, melanoma was more common in men. The most common anatomical sites were reported to be the head and neck and then the lower extremities. Lesion thickness between 0.25 to 0.74 cm were the most common. In previous studies, men were more frequently affected. The most common lesion thickness was similar to our study. The most common site of involvement was the lower extremity, and in our study too, it was one of the most common affected sites. However, in the study of Biangu Wu Soo in the Department of Dermatology of Korea, women (50.9%) had a higher frequency than men in terms of involvement [5, 6, 8, 22, 27]. In this study, there was a low prevalence of concurrent ulceration with melanoma, which is similar to the study of Eishan Sheen (29.1%). Ulcerations are one of the poor prognostic factors in melanoma [6]. The most common Clark level in our study was Clark level III. In the E-Ritter study, Clark levels 3 and 4 were also dominant. But in study of Christian-Alexander Clanses in the department of dermatology Australia, Clark level 2 (43.3%) and in the study of the Yom Jung Kim, Clark level 1 (30.3%) were dominant. This was probably due to better health and economic conditions of these regions. Also, patients with melanoma have fewer doctor visits in my area, as a result the diagnosis of the disease is given in more advanced stages [5, 22, 27]. The most prevalent melanoma subgroup in our study was acral lentiginous melanoma. Superficial spreading melanoma with 14.63% ranked second and lentigo malignant melanoma had the lowest frequency. In the study of Jang Yum Kim in the Department of Dermatology of Korea on 261 patients with cutaneous melanoma similar to our study, the acral lentiginous melanoma (44.1%) and superficial spreading melanoma (7.3%) and lentigo maligna melanoma had the highest frequency, respectively. In the E-Reiter study, 12% of melanomas did not have a specific subgroup, and the most common subgroups were superficial spreading melanoma (48%) and nodular melanoma, respectively [22, 27]. In our study, the 84.3% of margins of pigmented skin lesions were free from the tumors. It was almost similar to the study by Anna Gracia Robasco on 70 patients with melanocyte and non-melanocyte acral nevus, in which 94.3% of margins were free from lesions. This is probably because due to the clinical similarity of benign and malignant pigmented lesions, surgeons preferably remove the lesions completely with a free margin to avoid misdiagnosis of the malignant lesions as well as to reduce the recurrence of the lesion [30].
Conclusion
Since most pigmented skin lesions in the elderly have the potential for malignancy, so early diagnosis and appropriate treatment should be done to increase life expectancy in these patients.
Acknowledgments:
We would like to thank the professors of pathology at Shahid Sadoughi University of Medical Sciences in Yazd.
Potential conflicts of interest:
The authors declare no conflicts of interest.
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