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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 40  |  Issue : 1  |  Page : 15-22

Efficacy of dermoscopy in the diagnosis of different basal cell carcinoma subtypes


1 Department of Dermatology and Venereology, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt
2 Department of Pathology, Faculty of Medicine for Boys, Al-Azhar University, Cairo, Egypt
3 Department of Plastic Surgery, Faculty of Medicine for Girls, Al-Azhar University, Cairo, Egypt
4 Resident in Dermatology Departments, Cairo Hospital for Dermatology, Venereology and STIs, (Alhaud Al Marsoud), Cairo, Egypt

Date of Submission23-May-2019
Date of Acceptance14-Aug-2019
Date of Web Publication6-Jan-2020

Correspondence Address:
Abeer M Kamel
Assistant Professor of Dermatology and Venereology, Department of Dermatology and Venereology, Faculty of Medicine for Girls, Al-Azhar University, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ejdv.ejdv_26_19

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  Abstract 


Background Basal cell carcinoma (BCC) accounts for nearly 80% of all nonmelanoma skin cancers and dermoscopy is an important, noninvasive technique that aids in the diagnosis of BCC.
Objectives To evaluate the role of dermoscopy as a tool for diagnosis of BCC and prediction of its histopathological types.
Patients and methods Dermoscopic features of 30 clinically diagnosed BCCs were analyzed before the histopathological findings were evaluated.
Results Dermoscopy was 100% accurate in the diagnosis of BCC and types of BCC predicted by dermoscopy were identical to the results of histopathological examination, both yielding 27 nodular BCCs (90%), one superficial, one morpheaform, and one lesion of the infiltrative type, each representing 3.3% of lesions, but we did not detect any specific dermoscopic findings in the aggressive micronodular subtype.
Conclusions Dermoscopy is accurate in predicting the main histopathological types, but not the aggressive subtypes of BCC, thus it should be considered a routine but not a sole investigation for BCC.

Keywords: basal cell carcinoma, dermoscopy, diagnosis


How to cite this article:
El-Sayed SK, El-Sayed GDA, Kamel AM, Al-Tramsy AA, Ateia SY. Efficacy of dermoscopy in the diagnosis of different basal cell carcinoma subtypes. Egypt J Dermatol Venerol 2020;40:15-22

How to cite this URL:
El-Sayed SK, El-Sayed GDA, Kamel AM, Al-Tramsy AA, Ateia SY. Efficacy of dermoscopy in the diagnosis of different basal cell carcinoma subtypes. Egypt J Dermatol Venerol [serial online] 2020 [cited 2020 Jan 18];40:15-22. Available from: http://www.ejdv.eg.net/text.asp?2020/40/1/15/275180




  Introduction Top


Basal cell carcinoma (BCC) is the most common skin malignancy in the Caucasian population, accounting for ∼80% of nonmelanoma skin cancers cases. As BCC has different clinical presentations, its differential diagnosis ranges from nevi and skin carcinoma to melanoma. Although the histopathological study is the standard diagnostic procedure, other diagnostic tools are useful and dermoscopy is one of these tools [1]. The major distinctive histopathologic types are nodular, superficial, morpheaform, infiltrative, and metatypical BCC [2].

Common histological features for all types are basaloid cells with a pale cytoplasm surrounding round or oval nuclei. The peripheral cell layers are arranged in a palisading manner and are separated from the surrounding stroma by artificially created clefts. The tumors mainly originate in the epidermis and usually feature peripheral palisading. Key morphological feature includes mucinous stroma and tumor retraction artifact [3]. Infiltrative, morpheaform, micronodular, and metatypical BCC are considered as high-risk histopathological types, while nodular BCC is considered as the low-risk type [4].

The value of dermoscopy in the diagnosis of BCC has been widely emerged in the last few years. Dermoscopy facilitates accurate management of the tumor as dermoscopy can detect tumor characteristics, such as the histopathological subtype, the presence of pigmentation, and the presence of residual lesion or recurrence that help detect the optimum treatment [5].

The aim of this study was to evaluate the role of dermoscopy as an easily applied, nontime-consuming and noninvasive tool for the diagnosis of BCC and prediction of its histopathological types.


  Patients and methods Top


This cross-sectional analytic study included 30 patients with different clinical variants of BCC. They were randomly recruited from the Dermatology Outpatient Clinic of Al-Zahraa University Hospital during the period from January 2016 to February 2017.

Informed written consent was obtained from all patients. The approval from the research ethics committee of the Faculty of Medicine for Girls, Al-Azhar University was also obtained.

All eligible patients were subjected to:

  1. Dermoscopic examination:

    • Dermoscopic examination of lesions was done using a handheld dermoscopy (3Gen DermLite DL4; SouthPointe Surgical Supply, Olympus, Coral Spring, Florida, USA) with a 30 mm ×10 lens. Polarized mode with both contact and noncontact techniques was used to visualize dermoscopic findings of BCC in each lesion.


  2. Digital photography of the lesion:

    • Clinical and dermoscopic images were captured using Sony Xperia T2 (Sony, Japan, Tokyo) Mobile camera.


  3. Skin biopsies:

    • Histopathological examination was performed using a sterile 2–4 mm skin punches and biopsy specimens were fixed in 10% buffered formalin, routinely processed and embedded in paraffin and 5-μm thick serial sections were cut and prepared for routine hematoxylin and eosin stain for histopathologic examination by light microscopy (Olympus CX41, USA).


  4. Data management and analysis:

    • Data were collected, revised, coded, and entered to the statistical package for social sciences (IBM SPSS Version. 23). The quantitative data were presented as mean, SD, and ranges when their distribution was found to be parametric and qualitative data were presented as number and percentages.


The comparison between two independent groups with qualitative data was done using χ2 test and/or Fisher’s exact test only when the expected count in any cell is found to be less than 5. The confidence interval was set to 95% and the margin of error accepted was set to 5%. So, the P value was considered significant as the following: P value more than 0.05: nonsignificant, P value less than or equal to 0.05: significant and P value less than 0.01: highly significant.


  Results Top


Clinical evaluation of lesions

This study included 30 patients. Their ages ranged from 35 to 73 years, with a mean±SD age of 60.5±8.2 years, 24 (80%) were men and six (20%) were women. Ten (33.3%) patients were smokers and 16 (53.3%) patients gave a history of sun exposure for long durations. Past history of BCCs was positive in three (10%) patients in the same previous sites. The majority had Fitzpatrick skin phototype III (56.7%), the next prevalent skin phototype was IV (40%), and one (3.3%) patient had skin phototype II. Only one (3.3%) patient had a BCC on a sun-protected site (chest) while the rest of the patients (96.7%) had their lesions on sun-exposed sites (head and neck) ([Table 1]).
Table 1 Clinical evaluation of basal cell carcinoma patients

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On clinical examination, 27 (90%) patients had nodular BCCs, two (6.7%) patients had morpheaform BCCs, and one (3.3%) patient had a BCC of the superficial types ([Table 2]). From all the nodular BCCs only 13 (48.1%) lesions were noduloulcerative and four (14.8%) lesions were of the pigmented subtype. Clinically visible pigmentation was encountered in 23 (76.7%) lesions.
Table 2 Correlations of clinical, dermoscopic, and histopathological types of basal cell carcinoma

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Dermoscopic results

Dermoscopic examination showed that 27 (90%) patients had nodular BCC. One patient had a superficial BCC, one had morpheaform BCC, and another one had a BCC of the infiltrative type, each representing 3.3% of the total number of patients ([Table 2]).

Dermoscopic examination showed pigmentation in 25 (83.3%) lesions, only five (16.7%) lesions were nonpigmented.

In nodular BCCs, the most common dermoscopic finding was ulceration, found in 19 (70.4%) lesions followed by blue-gray ovoid nests, found in 18 (66.7%) lesions. Arborizing blood vessels were found in 17 (63%) lesions, blue-gray globules were found in 14 (51.9%) lesions, and maple leaf-like areas were found in 10 (37%) lesions. In-focus dots were encountered in five (18.5%) lesions while short white streaks and spoke wheel-like structures were found in 7.4 and 3.7% of lesions, respectively ([Table 3]) ([Figure 1]).
Table 3 Dermoscopic findings in nodular basal cell carcinomas

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Figure 1 Pigmented nodular basal cell carcinoma. (a) Clinical picture of pigmented nodular basal cell carcinoma. (b) Dermoscopic picture of pigmented nodular basal cell carcinoma. Black arrow: blue-gray ovoid nests, yellow arrow: ulceration (×10 lens). (c) Histopathological picture of pigmented nodular basal cell carcinoma. Blue arrow: masses of basaloid cells, black arrow: peritumoral clefts, white arrow: deposits of melanin, green arrow: area of central necrosis (hematoxylin and eosin, ×40).

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Dermoscopic findings encountered in the superficial BCC were blue-gray globules, in-focus dots, maple leaf-like areas, spoke wheel-like structures, concentric globules, and fine telangiectasia ([Figure 2]).
Figure 2 Pigmented superficial basal cell carcinoma. (a) Clinical picture of pigmented superficial basal cell carcinoma. (b) Dermoscopic picture of pigmented superficial basal cell carcinoma. Blue arrow: blue-gray globules, white and yellow circles: maple leaf-like areas, red circle: concentric globules (×10 lens). (c) Histopathological picture of pigmented superficial basal cell carcinoma. White arrow: melanin deposition within the masses of basaloid cells, black arrow: palisading of nuclei of basaloid cells (hematoxylin and eosin, ×40).

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In morpheaform BCC, dermoscopic findings were arborizing blood vessels, ulceration, and a whitish background ([Figure 3]).
Figure 3 Morpheaform basal cell carcinoma. (a) Clinical picture of morpheaform basal cell carcinoma. (b) Dermoscopic picture of morpheaform basal cell carcinoma. Red arrow: arborizing blood vessels, yellow arrow: ulceration, green arrow: whitish background (×10 lens). (c) Histopathological picture of morpheaform basal cell carcinoma. Blue arrow: masses of basaloid cells, Black arrow: Peritumoral cleft, Yellow arrow: fibrous stoma rich in collagen bundles (hematoxylin and eosin, ×40).

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Dermoscopic findings found in the infiltrative BCC were arborizing blood vessels, blue-gray ovoid nests, in-focus dots, white-red structureless areas, and fine telangiectasia ([Figure 4]).
Figure 4 Infiltrative basal cell carcinoma. (a) Clinical pictures of infiltrative basal cell carcinoma. (b) Dermoscopic pictures of infiltrative basal cell carcinoma. Red arrow: fine arborizing vessel, yellow arrow: ulceration, yellow circles: in-focus dots. (×10 lens). (c) Histopathological picture of infiltrative basal cell carcinoma. Blue arrow: masses of basaloid cells with jagged irregular outlines, black arrow: peritumoral clefts, yellow arrow: fibrous stoma (hematoxylin and eosin, ×100).

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Histopathological results

On histopathological examination, 27 (90%) patients had nodular BCCs. One patient had superficial BCC, one had morpheaform BCC, and another one had a BCC of the infiltrative type, each representing 3.3% of the total number of patients ([Table 2]). Pigmentations were detected in 25 (83.3%) lesions.

Two (7.4%) lesions of the nodular BCCs showed adenoid differentiation and one (3.7%) lesion was of the micronodular subtype ([Figure 5]).
Figure 5 Histopathological picture of micronodular basal cell carcinoma. Blue arrow: small masses of basaloid cells, green arrow): superficial nonspecific inflammatory infiltrate (hematoxylin and eosin, ×40).

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Correlations

Types of BCC predicted by dermoscopy were identical to the results of histopathological examination, both yielding 27 (90%) nodular BCCs, one superficial, one morpheaform, and one lesion of the infiltrative subtype, each representing 3.3% of lesions, unlike classifying lesions based on clinical evaluation which described 27 (90%) nodular lesions, one (3.3%) superficial, and two (6.7%) morpheaform BCCs with no significant difference (P=0.959) ([Table 2]). By clinical examination, pigmentation was detected in 23 (76.7%) lesions, while dermoscopic and histopathological examination showed pigmentation in 25 (83.3%) lesions.

By dermoscopic examination, the two nodular lesions showing adenoid differentiation showed arborizing blood vessels and blue-gray ovoid nests (100%), while ulceration, short white streaks, and blue-gray globules were each found in only one (50%) lesion. The micronodular BCC showed arborizing vessels and blue-gray globules.


  Discussion Top


This study included 30 patients. Their ages ranged from 35 to 73 years, with a mean±SD age of 60.5±8.2 years; men were 24 (80%) and women were six (20%). Our results were consistent with Muzic et al. [6] which showed that the mean age of BCC patients was 63.4 years with a higher incidence in men (50.2%).

For dermoscopic diagnosis of BCC we used the dermoscopic model proposed by Menzies et al. [7] based on the absence of a pigment network and the presence of at least one of six positive morphologic features including ulceration not associated with a recent history of trauma, multiple blue-gray globules, leaf-like areas, large blue-gray ovoid nests, spoke wheel-like structures, and arborizing telangiectasia. Also, we used the findings of nonclassic BCCs, added by Altamura et al. [8] including short-fine telangiectasia, multiple small erosions, in-focus dots, concentric structures, and shiny white-pink areas.

In our study, the most common dermoscopic feature in all BCCs was ulceration (70%) followed by arborizing blood vessels and blue-gray ovoid nests, each found in 19 (63.3%) lesions. In contrast with our results, a study by Altamura et al. [8] concluded that the most common dermoscopic findings were the arborizing vessels, identified in 57.1% of BCCs, large blue-gray ovoid nests (47.5%), and ulceration (39.2%). This contrast is most probably due to the presence of pigmentation in 83.3% of our lesions, which to some extent conceal the vascular structures. Dermoscopic ulceration is consistent with the high percentage of clinically ulcerated lesions and loss of parts of the epidermis in histopathology. On the other hand, our findings were in line with a study by Suppa et al. [9], who found that BCCs presenting with dermoscopic ulceration were the same lesions in which they detected clinical ulceration and the frequency of vascular pattern significantly decreased with increasing degree of pigmentation: from 90.6% in nonpigmented and scarcely pigmented BCCs to 56.5% in heavily pigmented BCCs.

We had only one lesion of the superficial type and the dermoscopic findings encountered in it were blue-gray globules, in-focus dots, maple leaf-like areas, spoke wheel-like structures, concentric globules, and fine telangiectasia. In the same context, according to Giacomel and Zalaudek [10] the most characteristic features of BCC were seen in pigmented variants and include concentric structures, spoke wheel areas, and maple leaf-like areas. They also concluded that detection of blue-gray ovoid nests signifies the presence of dermal pigmented basaloid nests, and excludes the superficial nature of the tumor. We could not confirm blue-gray ovoid nests as negative predictors of superficial BCC as we only had one lesion of the superficial type, while Papageorgiou et al. [11] consider superficial fine telangiectasia and white shiny blotches/strands as additional BCC predictors.

The dermoscopic findings that we encountered in the morpheaform BCC were arborizing blood vessels, ulceration, and a whitish background, while in the infiltrative BCC we found arborizing vessels, blue-gray ovoid nests, in-focus dots, white-red structureless areas, and fine telangiectasia.

Similarly, Zalaudek et al. [12] stated that infiltrative and scleroderma form (morpheaform) BCC also display branching vessels under dermoscopy. However, they are usually finer, more scattered, and show fewer branches compared with the classic vessels of nodular BCC. In addition, and in contrast to the global translucent pinkish color of nodular BCC, infiltrative BCC often exhibits white-red structureless areas, while the underlying fibrosis of scleroderma form BCC results in a dermoscopic whitish background.

Dermoscopic examination of our study cases showed pigmentation in 25 (83.3%) lesions, only five (16.7%) lesions were nonpigmented. This may be attributed to the darker skin phototypes prevalent in our Egyptian patients. Also, Takenouchi [13] stated that more than 80% of BCC in Japanese patients are pigmented and dermoscopic features are derived from the presence of melanin. Dermoscopic features are particularly affected by aggregates of melanophages in the tumor parenchyma. Hyperplastic melanocytes at the tumor margins may also play a role [14]. In contrast to our results, a study by Tan et al. [15] reported that in Caucasians, pigmented tumors account for less than 10% of all BCCs.

On histopathological examination and according to the histologic growth pattern classification, we found that 27 (90%) patients had nodular BCCs, one patient had superficial BCC, one had morpheaform BCC, and another one had a BCC of the infiltrative type, each representing 3.3% of the total number of patients and one (4.7%) lesion of the nodular BCCs was of the micronodular subtype.

Nodular BCC was the most common type among our cases. Soyer et al. [16] stated that nodular BCC is the most common clinical type, accounting for 50–79% of all BCCs. This wide range is influenced to a certain extent by the assignment or exclusion of similar growth types [17]. Furthermore, keeping with our findings, Mackiewicz-Wysocka et al. [18] stated that nodular BCC is the most common histopathologic BCC. Our histopathological results confirmed 100% accuracy of dermoscopy in diagnosing BCC, this is in line with the results of the study by Akay and Erdem [19] in which dermoscopy maintained 95.3% preoperative diagnostic accuracy rate for BCC.

The histopathological examination also confirmed that dermoscopy achieved a high level of precision predicting the histopathological types of BCC. However, dermoscopy was not able to detect the micronodular subtype. To our knowledge, there is no specific dermoscopic pattern to diagnose this aggressive subtype of nodular BCC.

The dermoscopic examination did not show any specific findings in the micronodular lesion as it showed arborizing vessels and blue-gray globules. Similarly, in a study by Lallas et al. [20] arborizing vessels, blue-gray globules and ulceration were the most common findings encountered in micronodular BCCs.

Remarkably, in our study pigmentation was clinically detected in 23 (76.7%) lesions, while dermoscopic and histopathological examination enabled us to detect pigmentation in 25 (83.3%) lesions.

In line with our results, a study by Lallas et al. [21] showed that 30% of BCCs clinically assessed as nonpigmented display dermoscopic pigmentation. This is explained by the fact that when only scarce foci of pigmentation are present, they might be insufficient to result in clinically evident pigmentation. Dermoscopy efficiently enhances clinicians’ ability to avoid the pitfall of misdiagnosing a pigmented BCC and applying an ineffective therapy and improving their selection of the tumors to be treated with photodynamic therapy [22].


  Conclusion Top


Histopathological examination proved dermoscopy to be 100% accurate in the diagnosis of BCC. Although prediction by even clinical diagnosis is pretty high in BCC, dermoscopy enabled us to detect pigmentation in clinically nonpigmented lesions and achieved a high level of precision predicting the main histopathological types of BCC. However, it was not sufficient for the prediction of the aggressive subtypes and we were not able to detect any specific findings in the micronodular lesion by dermoscopy. Limitations of this study include the small number and therefore larger scale studies are needed to prove these findings.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Verduzco‐Martinez AP, Quinones‐Venegas R, Guevara-Gutierrez E, Tlacuilo-Parra A. Correlation of dermoscopic findings with histopathologic variants of basal cell carcinoma. Int J Dermatol 2013; 52:718–721.  Back to cited text no. 1
    
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Costache M, Georgescu TA, Oproiu AA, Castache D, Naie A, Sajin M et al. Emerging concepts and latest advances regarding the etiopathogenesis, morphology and immunophenotype of basal cell carcinoma. Rom J Morphol Embryol 2018; 59:427–433.  Back to cited text no. 3
    
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Muzic JG, Schmitt AR, Wright AC, Alniemi DT, Zubair AS, Olazagasti Louurido JM et al. Incidence and trends of basal cell carcinoma and cutaneous squamous cell carcinoma: A population-based study in Olmsted County, Minnesota, 2000 to 2010. Mayo Clin Proc 2017; 92:890–898.  Back to cited text no. 6
    
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Menzies SW, Westerhoff K, Rabinovitz H, Kopf AW, McCarthy WH, Katz B. Surface microscopy of pigmented basal cell carcinoma. Arch Dermatol 2000; 136:1012–1016.  Back to cited text no. 7
    
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Altamura D, Menzies SW, Argenziano G, Zalaudek I, Soyer HP, Sera F et al. Dermatoscopy of basal cell carcinoma: morphologic variability of global and local features and accuracy of diagnosis. J Am Acad Dermatol 2010; 62:67–75.  Back to cited text no. 8
    
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Suppa M, Micantonio T, Di Stefani A, Soyer HP, Chimenti S, Fargnoli MC et al. Dermoscopic variability of basal cell carcinoma according to clinical type and anatomic location. J Eur Acad Dermatol Venereol 2015; 29:1732–1741.  Back to cited text no. 9
    
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Giacomel J, Zalaudek I. Dermoscopy of superficial basal cell carcinoma. Dermatol Surg 2005; 31:1710–1713.  Back to cited text no. 10
    
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Papageorgiou C, Apalla Z, Variaah G, Matiaki FC, Sortiriou E, Vakirlis E et al. Accuracy of dermoscopic criteria for the differentiation between superficial basal cell carcinoma and Bowen’s disease. J Eur Acad Dermatol Venereol 2018; 32:1914–1919.  Back to cited text no. 11
    
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Takenouchi T. Key points in dermoscopic diagnosis of basal cell carcinoma and seborrheic keratosis in Japanese. J Dermatol 2011; 38:59–65.  Back to cited text no. 13
    
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Soyer HP, Rigel DS, McMeniman E. Actinic keratosis, basal cell carcinoma and squamous cell carcinoma. In: Bolognia JL, Schaffer JV, Cerroni L, eds. Dermatology. 4th ed. Philadelphia: Elsevier Saunders; 2017; 1872–1893.  Back to cited text no. 16
    
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Akay BN, Erdem C. The evaluation of dermoscopic findings in basal cell carcinoma. J Turk Acad Dermatol 2010; 4:1–7.  Back to cited text no. 19
    
20.
Lallas A, Tzellos T, Kyrgidis A, Apalla Z, Zalaudek I, Karatolias A et al. Accuracy of dermoscopic criteria for discriminating superficial from other subtypes of basal cell carcinoma. J Am Acad Dermatol 2014c; 7:303–311.  Back to cited text no. 20
    
21.
Lallas A, Apalla Z, Ioannides D, Argenziano G, Castagenetti F, Moscarella E et al. Dermoscopy in the diagnosis and management of basal cell carcinoma. Future Oncol 2015; 11:2975–2984.  Back to cited text no. 21
    
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Arits AH, Mosterd K, Essers BA, Spoorenberg E, Sommer A, DeRooij MJ et al. Photodynamic therapy versus topical imiquimod versus topical fluorouracil for treatment of superficial basal-cell carcinoma: a single blind, non-inferiority, randomised controlled trial. Lancet Oncol 2013; 7:647–654.  Back to cited text no. 22
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

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