|Year : 2014 | Volume
| Issue : 3 | Page : 98-103
Epidemiologic and pathologic characteristics of basal cell carcinoma in northern Taiwan: Experience from a medical center
Yu-Wen Yeh1, Sheng-Yi Chen2, Bai-Yao Wu3, Hong-Wei Gao4, Chun-Yuan Liu5, Wu-Chien Chien5, Chien-Ping Chiang6
1 Department of Dermatology, Tri-Service General Hospital; Department of Internal Medicine, Tri-Service General Hospital Songshan Branch, National Defense Medical Center, Taipei, Taiwan, Republic of China
2 School of Dentistry; Department of Periodontology, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, Republic of China
3 Department of Dermatology, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, Republic of China
4 Department of Pathology, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, Republic of China
5 School of Public Health, National Defense Medical Center, Taipei, Taiwan, Republic of China
6 Institute of Biochemistry, National Defense Medical Center, Taipei, Taiwan, Republic of China
|Date of Submission||15-Aug-2013|
|Date of Decision||13-Jan-2014|
|Date of Acceptance||20-Jan-2014|
|Date of Web Publication||12-Jun-2014|
Dr. Chien-Ping Chiang
Department of Dermatology, Tri-Service General Hospital, National Defense Medical Center, No. 325, Sec. 2, Cheng-Gong Road, Taipei 11490, Taiwan
Republic of China
Source of Support: None, Conflict of Interest: None
Background: The epidemiologic studies of basal cell carcinoma (BCC) in Taiwan are lacking. Aim: This study aimed to provide the epidemiologic and pathologic information of BCC among the northern Taiwanese population and try to identify the association of patient demographic characteristics with histopathological findings. Materials and Methods: We retrospectively analyzed 103 BCC cases diagnosed between December 1985 and December 2011 at the Tri-Service General Hospital, Taipei, Taiwan. The patients' age and sex, and anatomic distribution, subtype, depth, and pigmentation of the lesions were analyzed. Results: Of the patients, 59 were men and 44 were women (male-to-female ratio, 1.34). The overall mean age was 69.5 ± 12.91 years; with the mean age of the women lower than that of the men (66.9 vs. 71.4 years). The frequency of microscopic pigmentation in BCC was 52.4%. Nodular BCC was more inclined to develop microscopic pigmentation. The BCCs with depths greater than 3.3 mm tended to have no microscopic pigmentation. Superficial BCCs tended to involve the trunk and to occur in people younger than 60 years of age. Conclusions: This updated analysis study of BCC showed the mean age of BCC had a trend to increase in northern Taiwan. The male-to-female ratio in our study was slightly higher than those of other Asian countries. We suggest that excision of BCC without pigmentation could be deeper than pigmented BCC.
Keywords: Basal cell carcinoma, pigmentation, depth, epidemiology, pathology, subtype
|How to cite this article:|
Yeh YW, Chen SY, Wu BY, Gao HW, Liu CY, Chien WC, Chiang CP. Epidemiologic and pathologic characteristics of basal cell carcinoma in northern Taiwan: Experience from a medical center. J Med Sci 2014;34:98-103
|How to cite this URL:|
Yeh YW, Chen SY, Wu BY, Gao HW, Liu CY, Chien WC, Chiang CP. Epidemiologic and pathologic characteristics of basal cell carcinoma in northern Taiwan: Experience from a medical center. J Med Sci [serial online] 2014 [cited 2021 Apr 22];34:98-103. Available from: https://www.jmedscindmc.com/text.asp?2014/34/3/98/134272
| Introduction|| |
Basal cell carcinoma (BCC) is the most common skin cancer among Caucasians, Hispanics, and Asians,  with incidence rates varying according to geographic location. According to the statistics of Taiwanese Government, the incidence of skin cancer has slowly increased since 1983 and skin cancer became the eighth most common form of cancer in Taiwan.  Ultraviolet radiation exposure is the primary etiologic factor for BCC worldwide.  The incidence rate of BCC has recently shown an increasing trend in the older Chinese.  The most common anatomic distribution of BCC tends to be to the head and neck. In the histopathological views of point, nodular BCC is the most frequent pattern, and superficial BCC is most often found on the trunk and limbs. , Infiltrating and superficial BCCs are most likely to recur after the operation because of unclear surgical margin. 
Many reports have been published regarding cases of BCC in western countries; however, data from Asian countries included Taiwan are scares. Thus far, only one study on BCC among Taiwanese is available on PubMed, but with an extremely unbalanced sex ratio as 2.82.  In that study, the authors reviewed 384 BCC cases in 30 years and found that superficial BCC was often occurred in younger patients and preferentially occurred on the trunk, which were consistent with previous Caucasian reports. Another smaller Taiwanese study of BCC published in 1994 reviewed 86 patients (88 cases).  It showed the most common subtype was solid pattern, but only 44 specimens were analyzed. Although BCC with pigmentation is more likely to occur among Asians than among Caucasians, only few Asian studies have analyzed the factors associated with microscopic pigmentation in BCC.
Therefore, in this retrospective study, we aimed to provide the further epidemiologic and pathologic information of BCC among the northern Taiwanese population and try to identify the association of patient demographic characteristics with pathologic findings, such as histopathological subtypes and microscopic pigmentation.
| Materials and Methods|| |
All cases of BCC that were histopathologically confirmed in the Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, between December 1985 and December 2011 were recorded. Diagnoses were made by pathologists, based on hematoxylin and eosin staining of specimens, which were reviewed by a dermatopathologist who had International Board Certification in dermatopathology. Our study was approved by the institutional review board of the Tri-Service General Hospital. Data on sex and age distribution of the patients, clinical location, histopathological subtypes, and microscopic characteristics such as invasion depth and pigmentation of lesions were collected. Scattered pigment incontinence was not considered to be BCC positive for microscopic pigmentation. Tumor invasion depth was measured using a microscope with a digital image system. The histopathological subtypes of BCC in this study were classified into nine major patterns: Nodular, superficial, micronodular, infiltrative, keratotic, morpheaform, metatypical, adenoid, and infundibulocystic types.  The data obtained were analyzed using SPSS version 20.0 for Windows (IBM Corp., NY, USA). Quantitative variables were described as mean ± standard deviation values and statistically analyzed using Mann-Whitney test. Categorical variables were expressed as frequencies and they were analyzed using the Chi-square test. The level of statistical significance was considered as P < 0.05.
| Results|| |
Age and sex
A total of 103 pathologically reviewed BCC specimens were obtained from 103 patients between 1985 and 2011. The patients were all Taiwanese, of whom 59 were men and 44 were women (male-to-female ratio, 1.34). The overall mean age was 69.5 ± 12.91 years; the mean age among men was 71.4 ± 12.93 years and that among women was 66.9 ± 12.57 years (P = 0.041). The sex and age distributions are presented in [Figure 1]. The youngest and oldest patients were men, aged 22 and 91 years, respectively. The BCC patients were mostly older than 50 years, with a peak age at detection of BCC of 71-80 years. The peak age at detection of superficial BCC was 51-60 years, which is lower than the peak age at detection of nodular (61-70 years), micronodular (71-80 years), infiltrative (71-80 years), and keratotic BCCs (81-90 years) [Figure 2].
|Figure 1: The age and sex distributions of 103 patients with basal cell carcinomas in Taiwan patients|
Click here to view
|Figure 2: Age distribution of the patients with different basal cell carcinoma histopathological subtypes|
Click here to view
The most common location of the BCCs was the face (81/103, 78.6%), followed by the scalp (10, 9.7%), trunk (5, 4.9%), limbs (5, 4.9%), and pelvis (2, 1.9%). The BCCs on the face were mostly found on the cheek (41.2%), followed by the nose (27.1%), periorbital area (12.9%), lips (7.1%), forehead (4.7%), temporal area (3.5%), ear (2.4%), and chin [1.2%; [Figure 3]].
|Figure 3: Anatomic distribution: (a) Total and (b) facial basal cell carcinomas|
Click here to view
[Table 1] indicates that the most common histological type was nodular BCC (56, 54.4%), followed by superficial (16, 15.5%), micronodular (14, 13.6%), infiltrative (9, 8.7%), and keratotic BCCs (4, 3.9%). The male-to-female ratio of patients with superficial BCC was 0.78, and that of patients with other BCC subtypes was higher than 1.0 as well. The head/neck-to-trunk/limb ratio of the superficial BCC cases was 2.2, whereas that of the other BCC subtypes was close to 10. The mean age of the patients with superficial BCC was within the range of the youngest ages in the top five subtypes. The overall mean invasion depth of the BCCs was 2.56 ± 2.27 mm. In particular, the mean invasion depth of the superficial BCCs was within the range of the shallowest depths in each subtype (0.98 ± 0.925 mm).
|Table 1: General information on the different BCC histopathological subtypes|
Click here to view
Superficial basal cell carcinoma versus nonsuperficial basal cell carcinoma
The percentage of superficial BCCs was 20.45% (9/44) among the female patients and 11.86% (7/59) among the male patients, indicating a statistically insignificant difference (P = 0.234). The mean age of patients with superficial BCC was 65.9 years, and that of patients with other BCC subtypes was 70.3 years (P = 0.103). [Table 2] shows the clinical characteristics of BCC based on the superficial BCC. In comparison with the nonsuperficial BCCs, the superficial BCCs were found with the tendency to involve the trunk (P = 0.022) and to occur in individuals younger than 60 years of age (P = 0.022) and those with shallower lesions (P < 0.001).
|Table 2: Clinical characteristics of BCC in patients, based on the superficial BCC|
Click here to view
Basal cell carcinoma with pigmentation versus basal cell carcinoma without pigmentation
The overall incidence rate of pigmentation in the BCC cases was 52.4%, the highest being in the nodular BCCs (66.1%), followed by the micronodular (50.0%) and superficial (37.5%) subtypes. Based on the comparison between the pigmented and nonpigmented BCCs, as presented in [Table 3], we found that nodular BCC was prone to develop microscopic pigmentation (P = 0.002). The associations between pigmentation and age, gender or anatomic site were not statistically significant [Table 3]. However by using receiver-operating characteristic curves, we found 3.3 cm as the cut-off point. The possibility of pigmentation in BCCs with depths >3.3 mm was lower than that in BCCs with depths <3.3 mm (P = 0.032). The depth of 3.3 mm was also the 76 th percentile in this study.
|Table 3: Comparison of the characteristics of BCCs in patients, according to pigmentation|
Click here to view
| Discussion|| |
In our study, the mean age of the patients was 69.5 years, which is close to and higher than that reported in recent and earlier Asian studies, respectively [Table 4]. This trend is observed in not only the Chinese population, but also the Japanese population. The mean ages in studies after 2001 were higher than those in earlier studies, probably because of the increasing life span and much better awareness on the importance of sun protection.
|Table 4: General information and histopathological subtypes of BCC in different Asian countries|
Click here to view
In this study, most patients (72.8%, 75/103) were between the ages of 61 and 90 years [Figure 1]. The mean age of female patients with BCC was lower than that of male patients (71.4 vs. 66.9 years, P < 0.05). This may be explained by the fact that a female was more concern about their appearance and sought physicians earlier. The aforementioned results were consistent with previous studies. ,,
In Asians, the male-to-female ratio is often between 0.9 and 1.2 [Table 4], except in one previous study in Taiwan that recorded an extremely high male-to-female ratio of 2.84, which might be due to the predominantly male veteran population in that study.  In our study, the male-to-female ratio was 1.34, which is close to the 1.15 ratio in another study in Taiwan,  but slightly higher than those in other Asian studies, possibly because of the better protection of ultraviolet light among women in Taiwan. The previous Taiwanese series showed male preponderance. , However, BCC cases in Japan, Korea, China, and Singapore had slight female predominance. ,,,,,,, Sex ratio may be influenced by geographical latitude, lifestyle, occupation, and recreational habit.
Basal cell carcinoma has a predilection for exposed areas of the body. The most frequent location of the BCCs in our study was the head region (88.3%), including the face (78.6%) and scalp (9.7%). BCCs in nonhead-neck regions (trunk, limbs, and pelvis) accounted for 12.7% of cases. In most Asian studies, the incidence rate of BCC of the head and neck region ranged from 74% to 88% [Table 4]. In our study, cases of facial BCC involved mainly the cheek, followed by the nose. These results were similar to those of other Asian studies showing that the most common facial location of the BCC was the nose or cheek. ,,,,,,, These findings consisted with the relevance of sun exposure as a risk factor.
The results of the histopathological analyses of BCC subtypes in the different Asian countries are summarized in [Table 4]. In most BCC studies, nodular BCC is the common subtype, followed by superficial subtype on the second or third place. Many studies reported that superficial BCC characteristically differ in terms of anatomic site and age at diagnosis and that its pathogenesis may be relatively distinct from that of other BCC subtypes.  These differences are clearly indicated by the parameters presented in [Table 1], such as mean age, male-to-female ratio, head/neck-to-trunk/limb ratio, and invasion depth.
The peak age at detection of the superficial BCCs in our study was 51-60 years, which is lower than that for the other BCC types [Figure 2]. Our study demonstrated that superficial BCC had a shallower invasion depth than other BCC subtypes and tends to involve the trunk and occur in people younger than 60 years of age [Table 2]. The results were comparable with those of previous studies. ,,
Basal cell carcinoma containing pigment is more frequently found in people with color. Pigmented BCC was easily misdiagnosed as benign seborrheic keratosis or malignant melanoma clinically. This pigmented variant was found to have a tendency of complete excisions. It may be the result of clearer margin made by the pigment.  BCC with pigmentation or not did not found the relationship with clinical outcome if treated properly. Three Asian studies reported incidence rates of pigmented BCC ranging from 69.1% to 69.4%, ,, which were higher than that in our study (52.4%). One of these studies indicated that of BCC cases with microscopic pigmentation, 17.9% manifested pigmentation only in the tumor nest periphery.  Therefore, this incidence rate of pigmentation of these studies would be similar to that of our study if the cases with mild pigmentary incontinence were excluded.
Maloney et al. have reported that pigmented BCC was more frequently excised with a negative tumor margin and had a similar rank in the incidence rate of pigmentation as the mixed micronodular/nodular (12.4%), nodular (7.7%), and superficial BCCs (7.2%).  Aoyagi and Nouri demonstrated that pigmented BCCs required smaller surgical margins than nonpigmented types.  However, no study has surveyed the correlation between microscopic invasion depth and incidence of pigmentation in BCC. [Table 3] shows that Nodular BCC was also more prone to develop microscopic pigmentation than the other BCC subtypes (P = 0.002). The prevalence rates of pigmentation were lower in BCC with depths >3.3 mm (76 th percentile) than in those with depths <3.3 mm (P = 0.032). This association may be due to the warning effect of pigmented skin lesions, which leads patients to visit a clinic earlier than those with nonpigmented BCCs. Excision of BCC without pigmentation should be deeper according our finding in this study.
However, this study was limited by the retrospective nature, selection bias and relatively small number of cases. It was a data from a single medical center and may not represent the accurate result of whole Taiwanese population. As we were focus on demographic and histopathologic information, the types of surgical procedures and treatment choices were not included in this study. In this research, the main reason why the uvivariate analysis was used as the method for statistics is due to the small sample size. Further investigations are required to provide more information with an adequate number of cases, such as multi-center studies.
In summary, our studies revealed that the mean ages of BCC had a trend to increase in northern Taiwan. The male-to-female ratio of BCC in Taiwan was slightly higher than other Asian courtiers. The present study demonstrates an association between BCC subtype, invasion depth, and microscopic pigmentation as well as more detail information of epidemiologic and histopathologic patterns within Taiwan population. We recommend that excision of BCC without pigmentation could be deeper than pigmented BCC.
| Acknowledgments|| |
This work was supported by grants from Songshan Armed Forces General Hospital, No. 10004 and National Defense Medical Center (NDMC-100-M083), Taipei, Taiwan, Republic of China.
| Disclosure|| |
All authors declare no competing financial interests.
| References|| |
|1.||Rubin AI, Chen EH, Ratner D. Basal-cell carcinoma. N Engl J Med 2005;353:2262-9. |
|2.||Cancer Registry Annual Report, 2010; 2013. Available from: http://www.hpa.gov.tw/BHPNet/Web/Stat/StatisticsShow.aspx?No=201305060001. |
|3.||Gallagher RP, Hill GB, Bajdik CD, Fincham S, Coldman AJ, McLean DI, et al. Sunlight exposure, pigmentary factors, and risk of nonmelanocytic skin cancer. I. Basal cell carcinoma. Arch Dermatol 1995;131:157-63. |
|4.||Sng J, Koh D, Siong WC, Choo TB. Skin cancer trends among Asians living in Singapore from 1968 to 2006. J Am Acad Dermatol 2009;61:426-32. |
|5.||Scrivener Y, Grosshans E, Cribier B. Variations of basal cell carcinomas according to gender, age, location and histopathological subtype. Br J Dermatol 2002;147:41-7. |
|6.||Betti R, Inselvini E, Carducci M, Crosti C. Age and site prevalence of histologic subtypes of basal cell carcinomas. Int J Dermatol 1995;34:174-6. |
|7.||Sexton M, Jones DB, Maloney ME. Histologic pattern analysis of basal cell carcinoma. Study of a series of 1039 consecutive neoplasms. J Am Acad Dermatol 1990;23:1118-26. |
|8.||Chen CC, Chen CL. Clinical and histopathologic findings of superficial basal cell carcinoma: A comparison with other basal cell carcinoma subtypes. J Chin Med Assoc 2006;69:364-71. |
|9.||Tu ME LY, Chen HC, Su HY. Basal cell carcinoma - A clinicopathological analysis of 86 cases. Dermatol Sin 1994;12:183-92. |
|10.||McKee P, Calonje E, SG. Pathology of the Skin, with Clinical Correlations. 3 rd ed. Philadelphia, PA: Mosby; 2005. p. 1167-84. |
|11.||Chang JM, Gao XM. Clinical and histopathological characteristics of basal cell carcinoma in Chinese patients. Chin Med J (Engl) 2013;126:211-4. |
|12.||Raasch BA, Buettner PG, Garbe C. Basal cell carcinoma: histological classification and body-site distribution. Br J Dermatol 2006;155:401-7. |
|13.||Zhang B, Wang N, He W. Clinicopathologic analysis of 60 cases of basal cell carcinoma. Chin Med Sci J 1993;8:121-2. |
|14.||Kikuchi A, Shimizu H, Nishikawa T. Clinical histopathological characteristics of basal cell carcinoma in Japanese patients. Arch Dermatol 1996;132:320-4. |
|15.||Cho S, Kim MH, Whang KK, Hahm JH. Clinical and histopathological characteristics of basal cell carcinoma in Korean patients. J Dermatol 1999;26:494-501. |
|16.||Takenouchi T, Nomoto S, Ito M. Factors influencing the linear depth of invasion of primary basal cell carcinoma. Dermatol Surg 2001;27:393-6. |
|17.||Goh BK, Ang P, Wu YJ, Goh CL. Characteristics of basal cell carcinoma amongst Asians in Singapore and a comparison between completely and incompletely excised tumors. Int J Dermatol 2006;45:561-4. |
|18.||Yap FB. Clinical characteristics of basal cell carcinoma in a tertiary hospital in Sarawak, Malaysia. Int J Dermatol 2010;49:176-9. |
|19.||Goto M, Kai Y, Arakawa S, Oishi M, Ishikawa K, Anzai S, et al. Analysis of 256 cases of basal cell carcinoma after either one-step or two-step surgery in a Japanese institution. J Dermatol 2012;39:68-71. |
|20.||McCormack CJ, Kelly JW, Dorevitch AP. Differences in age and body site distribution of the histological subtypes of basal cell carcinoma. A possible indicator of differing causes. Arch Dermatol 1997;133:593-6. |
|21.||Maloney ME, Jones DB, Sexton FM. Pigmented basal cell carcinoma: investigation of 70 cases. J Am Acad Dermatol 1992;27:74-8. |
|22.||Aoyagi S, Nouri K. Difference between pigmented and nonpigmented basal cell carcinoma treated with Mohs micrographic surgery. Dermatol Surg 2006;32:1375-9. |
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4]
|This article has been cited by|
||Real-life data on basal cell carcinoma treatment: Insights on cliniciansę therapeutic choices from an institutional hospital registry
| ||Sofia-Magdalini Manoli,Andreas Moutsoudis,Chryssoula Papageorgiou,Konstantinos Lallas,Haris-Marios Rigas,Eirini Kyrmanidou,Ilias Papadimitriou,Eleni Paschou,Ioannis Spyridis,Theodosia Gkentsidi,Elena Sotiriou,Efstratios Vakirlis,Demetrios Ioannidis,Zoe Apalla,Aimilios Lallas |
| ||Dermatologic Therapy. 2020; |
|[Pubmed] | [DOI]|
||Evaluation of the appropriate surgical margin for pigmented basal cell carcinoma according to the risk factors for recurrence: a single-institute retrospective study in Japan
| ||Y. Nakamura,K. Tanese,I. Hirai,K. Kameyama,Y. Kawakami,M. Amagai,T. Funakoshi |
| ||Journal of the European Academy of Dermatology and Venereology. 2018; |
|[Pubmed] | [DOI]|
||Targeting the VEGF-C/VEGFR3 axis suppresses Slug-mediated cancer metastasis and stemness via inhibition of KRAS/YAP1 signaling
| ||Yu-Wen Yeh,Ching-Chia Cheng,Shu-Ting Yang,Chi-Feng Tseng,Ting-Yu Chang,Sin-Ying Tsai,Earl Fu,Chien-Ping Chiang,Li-Chuan Liao,Pei-Wen Tsai,Yung-Luen Yu,Jen-Liang Su |
| ||Oncotarget. 2017; 8(3): 5603 |
|[Pubmed] | [DOI]|
||Treatment of Pigmented Basal Cell Carcinoma with 3?mm Surgical Margin in Asians
| ||Shang-Hung Lin,Yu-Wen Cheng,Yi-Chien Yang,Ji-Chen Ho,Chih-Hung Lee |
| ||BioMed Research International. 2016; 2016: 1 |
|[Pubmed] | [DOI]|