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A Profile and Three-Year Follow-Up of Patients with Basal Cell Carcinoma in the Western Cape, South Africa

A Profile and Three-Year Follow-Up of Patients with Basal Cell Carcinoma in the Western Cape,... Hindawi Journal of Skin Cancer Volume 2022, Article ID 8443867, 7 pages https://doi.org/10.1155/2022/8443867 Research Article A Profile and Three-Year Follow-Up of Patients with Basal Cell Carcinoma in the Western Cape, South Africa 1 2 1 3 1 J. C. Gallo , J. W. Schneider , J. de Wet , K. Moxley , H. F. Jordaan , 1 1 W. I. Visser , and B. Tod Division of Dermatology, Department of Medicine, Tygerberg Academic Hospital, Stellenbosch University, Cape Town, South Africa Division of Anatomical Pathology, Department of Pathology, National Health Laboratory Service, Tygerberg Academic Hospital, Stellenbosch University, Cape Town, South Africa Registrar Research Support O­ce, Research Development and Support Division, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa Correspondence should be addressed to J. C. Gallo; justinegallo86@gmail.com Received 7 March 2022; Accepted 21 April 2022; Published 5 May 2022 Academic Editor: Arash Kimyai Asadi Copyright © 2022 J. C. Gallo et al. �is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Basal cell carcinoma (BCC) is an important malignancy in sub-Saharan Africa. �ere is a paucity of data regarding BCC in South Africa. Aims. To describe the clinicopathological features of patients presenting with BCC in a cohort of South African patients. Methods. �is retrospective descriptive study reviewed the medical records of 149 patients with BCC who attended the dermatology clinic at Tygerberg Academic Hospital from September 2015 to August 2016. Demographic and clinical data of those patients with histologically proven BCC were retrieved from clinical records. �e data included the assessment for BCC recurrence after three years (September 2016–August 2019). Results. Of 390 patients, 155 (39.7%) had histologically con—rmed BCCs. Complete medical records were available for 149 of these patients, and most were male (55.7%) and white (85.9%) with a median age of 70 years. Most patients had their BCC lesions for 12 months (43.1%) before diagnosis. BCCs were mostly located on the head and neck area (58.1%). In most patients (72.0%), a diagnostic punch biopsy con—rmed BCC. Plastic surgeons subsequently excised the BCC lesions in 74.0% of these patients. �e most common histological subtype was nodular BCC (74.0%). �e National Comprehensive Cancer Network (NCCN) risk of recurrence was approximately evenly distributed between high- (54.1%) and low-risk groups (45.9%). �e major high-risk feature was the location (36.6%). Histologically con—rmed BCC recurrence occurred in 9 of the 149 patients (3.7%) over three years. Conclusions. BCC represents a high burden of disease in our setting. Compared to existing studies, the BCCs in this study are clinically and histologically similar to international reports. scalp, neck, and face. Destructive invasion by BCC or 1. Introduction therapeutic interventions may cause functional and cosmetic Basal cell carcinoma (BCC) is a type of keratinocyte cancer problems [4, 5]. (KC) that arises from basal epidermal keratinocytes. BCC is BCC management involves consultations by primary the commonest malignancy of the skin and the commonest healthcare physicians or dermatologists, diagnostic biopsies, human malignancy worldwide [1–3]. BCC represents ap- histopathology review, formal surgical excision in the der- proximately 70–80% of all skin carcinomas, making it the matology o£ce, referral for Mohs micrographic surgery (MMS), or referral for plastic and reconstructive surgery most prevalent cancer in many countries [2, 4, 5]. BCC is rarely fatal (mortality rate <0.1%), but localized and, in selected cases, radiation therapy. Patients require tissue invasion may induce considerable morbidity. Most regular follow-up visits to monitor for BCC recurrence or BCC lesions occur on cosmetically sensitive areas such as the the development of new skin cancers. Delayed diagnosis is a 2 Journal of Skin Cancer significant challenge in low- and middle-income countries. 028) [11]. Data about relevant medical history, previous BCC adds a high-cost burden and strain on the health care treatments for BCC, tumour diameter and location, the procedure performed, and any BCC recurrence were re- system [4, 6]. BCC has been extensively studied in Australia, the trieved for each case from records on the TAH Enterprise United States, and Europe. (ese studies confirmed wide Content Management (ECM) system. Histopathology re- variation in BCC incidence, with the highest rates in Aus- sults were obtained from the National Health Laboratory tralia and the lowest rates in parts of Africa [4, 7]. Higher Service database. BCC recurrence was identified by incidence is related to decreasing latitude, intermittent solar reviewing patient records on the ECM from 1 September ultraviolet radiation (UVR) exposure, and more accurate 2016 to 31 August 2019. Recurrence was defined as “possible reporting practices [4]. Little is known regarding BCC in local recurrence” when histologically confirmed BCC arose populations in low- and middle-income countries such as within the scar of a previously excised BCC [12]. (e South Africa (SA). principal investigator (JG) collated the anonymised data in a SA has one of the world’s largest human immunodefi- Microsoft Excel spreadsheet. ciency virus (HIV) epidemics [8]. HIV-infected patients have a 3- to 5-fold increased risk of developing KCs [7, 9, 10]. 2.5. Patient Characteristics. Patient records did not include SA has high levels of solar UVR due to its geographical Fitzpatrick phototypes. (erefore, we used the population location [9]. Furthermore, skin cancer rates in SA have been group as a crude indication of phototype . A hot-deck increasing [9, 10]. Incomplete reporting to the National imputation method was used when the population group Cancer Registry explains the limited data about BCC in SA, was not indicated [11, 13]. Patients were recorded as making it difficult to monitor the national statistics com- immunosuppressed if they had HIV, had a current malig- pared to other countries [10]. (e paucity of clinicopatho- nancy (excluding KC), had a solid organ transplant, or used logical data for BCC in SA justifies research to address this immunosuppressive medication. knowledge gap and to create greater awareness and a better understanding of BCC in SA. Such studies can facilitate educational and prevention campaigns to assist in curbing 2.6.DiagnosisofBCC. Dermatology trainees and consultants the burden of BCC. from the Division of Dermatology at TAH performed bi- opsies and other surgical procedures. In some cases, patients had more than one BCC, requiring multiple biopsies at the 2. Materials and Methods same visit. 2.1. Study Design. (is retrospective descriptive study in- (e National Comprehensive Cancer Network (NCCN) cluded patients with histologically proven BCC who BCC guidelines define criteria for high recurrence risk to attended the dermatology clinic at Tygerberg Academic include specific tumour locations and sizes, ill-defined Hospital (TAH) between 1 September 2015 and 31 August clinical borders, recurrences, tumours arising in radiotherapy 2016. (e study included a three-year follow-up of patients fields, aggressive histological growth patterns, perineural (until 31 August 2019) to assess for BCC recurrence. involvement, and patient immunosuppression [14]. A pathologist (JWS) and JG retrieved and reviewed histopathology sections of cases where the histopathology 2.2. Study Setting. TAH is a publicly funded academic reports did not include adequate information regarding tertiary level hospital in Cape Town (Western Cape prov- diagnosis, histological growth pattern, or perineural in- ince, SA) with a large drainage area from primary and volvement. JWS reviewed all BCC specimens and categorized secondary health care facilities. TAH serves a population of them according to the 4th edition World Health Organisa- low- to middle-income status. (e dermatology clinic is tion (WHO) classification guideline for tumours [15]. operated by consultant dermatologists, registrar dermatol- ogists, and nurses. (e unit is medically focused, where 2.7. Data Analysis. Continuous variables were summarised excisions and cautery and electrodesiccation (C&E) of low- risk tumours are performed. High-risk and surgically as median with interquartile range (IQR) for non-normal data. Categorical variables were summarised as frequencies challenging tumours are referred to the Division of Plastic and Reconstructive Surgery at TAH for excision. and percentages. 2.8. Ethical Considerations. (e study was approved by the 2.3. Study Sample. During the study period, 696 biopsies Stellenbosch University Health Research Ethics Committee from 390 patients were performed on clinically suspected (SUHREC) (HREC/REF: S19/04/070). All data were ano- skin cancer [11]. We included patients older than 18 years nymised to ensure the confidentiality of participants’ per- with histologically confirmed BCC. Patients with incomplete sonal information. medical records and those lost to follow-up were excluded. (e final sample size for data collection was therefore 149. 3. Results 2.4. Data Collection. Demographic data were obtained as Of 390 patients biopsied for clinically suspected KC, a total secondary data from a previous study (HREC/REF: U16/10/ of 155 had a confirmed diagnosis of BCC (39.7%). Six Journal of Skin Cancer 3 Table 1: Demographic and clinical characteristics of patients with patients with incomplete medical records were excluded. BCC (N � 149). Fifty-six patients (36.1%) presented with multiple BCCs. Demographic and clinical characteristics of 149 patients Variable Frequency, n Percentage, % meeting inclusion criteria are summarised in Table 1. (e Gender median age (interquartile range, IQR) was 70 (61–78) years. Male 83 55.7 In the mixed ancestry group (n � 18), 13 patients Female 66 44.3 (72.2%) had high-risk features. In contrast, the white Population group population group (n � 128) had high-risk features in 67 ∗ White 128 85.9 patients (52.3%). (ere were a 2.8 (95% CI: 0.97 to 7.86) odds Mixed ancestry 18 12.1 of having a higher risk profile in the mixed ancestry group . Black African 1 0.7 However, this finding was not statistically significant. (e Indian/Asian 1 0.7 Not known 1 0.7 single black African patient was at high-risk due to im- munosuppression from HIV infection and had oculocuta- Risk factors Chronic sun exposure 8 5.4 neous albinism (OCA) and, therefore, presumably lightly Immunosuppression 5 3.4 pigmented skin. (e Indian/Asian patient had a high-risk Site of prior radiation 3 2.0 feature due to the BCC occurring in a high-risk location. Oculocutaneous albinism (OCA) 1 0.7 Risk factors for BCC were poorly documented. In 48 Immunosuppression and OCA 1 0.7 cases with this information, the commonest risk factor was Immunosuppression and previous chronic sun exposure (n � 8), of which 6 cases were occu- psoralen ultraviolet 1 0.7 pational. Sun exposure was only captured if it was reported a (PUVA) therapy in the patient’s clinical notes. (e histological assessment None 29 19.5 confirmed the presence of solar elastosis in 161 cases Not known 101 67.8 (65.4%), an absence thereof in 9 cases (3.7%), and “unable to Previous history of skin cancer assess” in 76 cases (31.0%). Where solar elastosis could be Unspecified KC 43 28.9 histologically assessed, it was found in 94.7% of cases. (us, Basal cell carcinoma 24 16.1 it appears that chronic sun exposure was significantly Squamous cell carcinoma 4 2.7 underreported. Cutaneous melanoma 3 2.0 KC and cutaneous melanoma 8 5.4 Immunosuppression was reported in only 7 patients who KC and other skin cancers 2 1.3 collectively had 17 biopsies performed. Two patients were None 11 7.4 HIV-positive, of whom one had previous PUVA treatment, Not known 54 36.2 and the other had OCA. One patient took methotrexate therapy for psoriasis. (ree patients had cancer elsewhere and one was a renal transplant recipient on immunosup- presented in Table 3. One patient was referred to an oph- pressive medication. thalmologist for excision of a lesion close to the eyelid margin A total of 246 BCCs were diagnosed amongst 149 pa- (n � 1). Two patients, one with a high-risk basosquamous tients and the tumour characteristics are summarised in lesion and the other with a squamous cell carcinoma else- Table 2. Combined high-risk histological subtypes, including where, were referred to a multidisciplinary skin cancer clinic. micronodular, morpheaform, and basosquamous subtypes, Excision by a plastic and reconstructive surgeon resulted in 6 amounted to 24 cases (9.8%). From the pigmented BCC recurrences (of 182 cases treated, 3.3%). One patient in the group (n � 22), 8 cases were considered as high-risk BCCs, “other treatments” group had nodal metastases. (is lesion with the most common high-risk feature being increased was a high-risk basosquamous carcinoma referred to the lesion size (n � 6). Closer examination of the pigmented BCC multidisciplinary skin cancer clinic for surgical nodal group (n � 22) in the current study revealed that 15 arose in ∗ clearance. white patients and the remainder (n � 7) from other Recurrence was clinically suspected in 24 cases, although phototypes (Indian/Asian and mixed ancestry ). Of biopsies it was histologically proven in only 9 cases (3.7%) over the from presumably more pigmented phototypes (all skin types three-year follow-up period. Most recurrences occurred excluding white patients ), a third were pigmented BCCs. 12–24 months after the initial event (n � 5). (ere were 8 Ulceration was noted in 54 cases (22.0%). None of our cases cases of local recurrence and 1 case of metastatic spread to showed perineural invasion. draining lymph nodes (the basosquamous carcinoma Figures 1 and 2 depict BCC location in the cohort. BCCs mentioned above). New BCC lesions in locations other than were more common on the left side of the face (n � 47) the index BCC lesion occurred in 83 cases (33.7%). compared to the right side of the face (n � 39) (Figure 2). (e side of the face was not specified in 31 cases, and the remaining 9 cases were in the midline. (e nose was the most 4. Discussion common area of the face involved (n � 43), followed by the cheeks (n � 24). BCC is a common malignancy with significant morbidity Fifty-six (22.8%) patients were treated by double-cycle and health economic implications. A large body of research C&E or formal excision at the dermatology clinic. NCCN risk on BCC is available. However, little local data exist about stratification, final treatment modalities, and recurrences are BCC in the South African context. (e purpose of this 4 Journal of Skin Cancer Table 2: Clinical and pathological data of all incident basal cell Head & neck: 143 carcinomas (N � 246 biopsy samples). Head: 135 Neck: 8 Variable Frequency, n Percentage, % Clinical diameter (mm) <10 28 11.4 Trunk: 43 Anterior: 18 10–19 27 11 Posterior: 25 ≥20 19 7.7 Not stated in clinical notes 172 69.9 Upper limbs: 30 Duration (months) Right: 17 <6 months 67 27.2 Left: 13 6–12 months 51 20.7 >12 months 106 43.1 Genitalia: 1 Participant unsure 9 5.3 Not stated in clinical notes 13 3.7 Lower limbs: 27 Diagnostic procedure Right: 11 Punch biopsy 177 72.0 Left: 14 Double-cycle C&E 45 18.3 Undefined: 2 Excisional biopsy 21 8.5 Incisional biopsy 2 0.8 Shave biopsy 2 0.8 BCC subtype Nodular 182 74.0 Figure 1: Distribution of basal cell carcinoma tumours on the body Pigmented 22 8.9 (n � 244, n � 2 location not stated). Micronodular 21 8.5 Superficial 5 2.0 Morpheaform 2 0.8 High-risk area Left Right Basosquamous 1 0.4 Medium risk area Unable to assess 13 5.3 NCCN risk stratification 4 5 High-risk 133 54.1 Low-risk 113 45.9 Number of high-risk features 4 10 14 1 high-risk feature 107 43.5 5 4 2 high-risk features 22 8.9 3 high-risk features 4 1.6 High-risk features Location 90 36.6 9 3 Size 24 9.8 4 1 2 3 4 3 Aggressive growth pattern 24 9.8 Immunosuppression 17 6.9 Site of prior radiation 5 2.0 Recurrent BCCs 3 1.2 Figure 2: Distribution of basal cell carcinoma tumours on the face (n � 126). (e area in red is the high-risk mask area of the face (n � 87), and the blue area signifies the rest of the face, which is a retrospective descriptive study was to determine the prev- medium risk (n � 39). alence, clinicopathological features, and recurrence of BCC in a cohort of patients presenting with histologically proven BCC at a single institution. given the higher risk profile of the mixed ancestry group compared to the white population group (72.2% versus 52.3% with high-risk features). (e prevalence of this out- 4.1. Demographic Characteristics. (e overall prevalence of come should be reexamined in research statistically powered BCC in patients with clinically suspected skin cancer in this for assessing this outcome, as it has important clinical im- study sample was 39.7%. In keeping with international plications. (is study could not provide causes for the trends, most patients with BCC were male (55.7%) and possible risk-related differences between these two groups, white (85.9%) with a median age of 70 years [2, 16, 17]. and further studies could investigate this question. Data regarding BCC in other population groups in SA are sparse [18, 19]. In the United States, studies show that skin cancer occurs less frequently in darker pigmented skin types 4.2. Risk Factors for the Development of BCC. Although SA [19, 20]. Our study is in keeping with this trend. also has a high rate of year-round solar UVR exposure, the Skin cancer outcomes tend to be worse in patients with population composition is very different from other coun- pigmented skin types [21]. Our findings echo this observation tries in the southern hemisphere with high BCC rates, such Journal of Skin Cancer 5 Table 3: NCCN risk stratification and final treatment modalities for BCC lesions (N � 246). Risk stratification Treatment modality, n (%) Total high- and low-risk (N � 246) High-risk (n � 135) Low-risk (n � 111) ∗∗ ∗∗ Excision by plastic and reconstructive surgery 182 (74.0) 109 (44.3) (3 ) 73 (29.7) (3 ) ∗∗ Double-cycle C&E at dermatology 37 (15.0) 18 (7.3) 19 (7.7) (2 ) Excision at dermatology 19 (7.7) 4 (1.6) 15 (6.1) ∗∗ Other treatments 3 (1.2) 2 (0.8) (1 ) 1 (0.4) Loss to follow-up 5 (2.0) 2 (0.8) 3 (1.2) ∗∗ (n ) represents the number of recurrent cases in a specific treatment modality. as Australia [19]. Solar elastosis was observed in most cases, lesion size at the time of diagnosis, highlighting the diag- suggesting significant sun damage in these patients. Re- nostic delay in these challenging cases. In previous studies, pigmented BCCs have been shown to predominate in darker garding immunosuppression, SA has one of the highest rates of HIV in the world at an estimated 13% prevalence, and pigmented skin types [22, 24]. Pigmented BCCs were more prevalent in pigmented skin types in this cohort. (is is approximately, 7-8 million people were living with HIV in 2020 [8]. Both HIV-positive patients in our study had other clinically relevant as pigmented BCCs may be misdiagnosed as seborrheic keratoses or melanocytic naevi, for example, in risk factors for BCC (OCA and previous PUVA exposure). SA theoretically has a population uniquely predisposed to darker skin types. Dermoscopy can assist in differentiating BCC due to high levels of UVR coupled with a large portion such lesions from BCC [25]. Clinicians should be aware of of the population being immunosuppressed due to HIV. this important differential diagnosis in patients with darker Further studies are required to fully understand this. skin types. 4.3. Duration of BCC Prior to Diagnosis. Delayed BCC di- 4.5. National Comprehensive Cancer Network (NCCN) Risk agnosis has been linked to recurrence and metastatic risk Stratification. Our cohort was stratified utilizing the NCCN [22]. Most of the patients in this study presented to the risk for recurrence stratification, defining a large proportion dermatology clinic having had BCC for more than of patients as high-risk for recurrence (n � 133, 54.0%), 12 months. Simultaneously, most cases involved conspic- mostly due to BCC location. A low recurrence rate was observed; however, limitations in the methodology mean uous areas such as the face, and there was a high proportion of large, locally advanced lesions at presentation (18.7% were that this has probably been underreported. larger than 10 mm). (is suggests a lack of awareness about the clinical signs of BCC. (ere is a need to educate patients 4.6. BCC Treatment. (e goal of BCC treatment is a cure and health-care workers to identify BCC and seek profes- with maximum preservation of function, cosmesis, and low sional medical care promptly, thereby improving surgical complication rates [3, 26, 27]. (e NCCN guidelines for the outcomes and limiting disfigurement due to larger tumours surgical treatment of BCC recommend that low-risk BCCs [2, 22]. less than 2 cm in diameter be excised with a 4 mm clinical margin. MMS is the gold standard treatment for high-risk 4.4. Histology of BCC. (ere are several described histo- BCCs as it offers the highest cure rate [27–29]. A study logical subtypes of BCC [15, 23]. (e World Health Orga- evaluating MMS for BCC treatment in SA echoed inter- nisation (WHO) classifies the various BCC subtypes national data and showed that MMS offers the highest cure according to their different growth patterns [15]. Nodular, rates with a low recurrence rate (0.1%) [29]. MMS is not a superficial, and pigmented BCC subtypes are generally treatment option at TAH. considered less aggressive, whereas micronodular, mor- Double-cycle C&E produced good results for our cohort, with seemingly low recurrence rates. C&E is indicated for pheaform, basosquamous, and infiltrating subtypes are more aggressive. Recent research has highlighted a different trend the treatment of small, low-risk nonfacial BCCs and patients who are not surgical candidates [26]. Although not rec- for the involvement of lateral or deep margins according to different histological subtypes [23]. Lateral involvement is ommended by international guidelines, C&E can be con- more frequent for the morpheaform subtype whereas the sidered in low-resource settings for the treatment of high- deep margin is more involved in the nodular subtype [23]. In risk BCCs, since it is a convenient and cost-effective pro- this study, the most common BCC subtype was nodular cedure. (is occurs in carefully selected patients at TAH. (74.0%), in line with international literature [2, 23]. (e BCC recurrence in high-risk areas treated with C&E is re- more aggressive histological subtypes (n � 24, 9.8%) are ported to be significantly higher compared to surgical al- deemed high-risk for recurrence using the NCCN guidelines ternatives (6.9% versus 3.8% respectively) [30, 31]. High-risk [14]. BCCs treated with C&E require more rigorous follow-up for recurrence, which could result in an increased demand on Pigmented BCCs are considered a less aggressive his- tological subtype [24]. (ere was a high proportion of other resources and loss to follow-up. Training primary and secondary healthcare workers to high-risk features among pigmented BCCs in this cohort. (e most common high-risk feature was increased clinical diagnose and treat low-risk BCCs with C&E could offer 6 Journal of Skin Cancer better treatment outcomes than long delays in referral to a context. Furthermore, early surgical management of BCCs tertiary dermatology centre. Surgical training of dermatol- will improve patients’ outcomes and reduce the risk of future ogy trainees to excise high-risk BCCs would necessitate complications. fewer referrals to plastic and reconstructive surgery. Further studies are required to assess the need for an adapted BCC Data Availability risk stratification in resource-limited environments and more accurately evaluate the success of double-cycle C&E in Data can be available on request. (e requesting party can selected high-risk lesions. contact the corresponding author. Additional Points 4.7. BCC Recurrence. Possible recurrence was observed in 9 patients (3.7%). Six patients with recurrent BCC were ini- Variations in the epidemiology and clinical features of BCC tially treated for their primary BCC by surgical excision, and significantly correlate with patients’ Fitzpatrick phototypes, the majority occurred 12–24 months after the initial event. justifying the inclusion of this data [21]. While the pop- (ese results are in keeping with international trends of BCC ulation group (a social construct) is not reliably correlated recurrence rates [3, 22]. However, patients were only fol- with the phototype, it is used in this study as a crude proxy. lowed up over three years, and cases could have recurred after this time or been lost to follow-up. A randomised Ethical Approval control trial with a 10-year follow-up period found that over 50% of BCC recurrences occur after five years [30]. (e study was approved by the Stellenbosch University (erefore, the three-year follow-up period in this study Health Research Ethics Committee (SUHREC). could lead to a misleadingly low recurrence rate. Conflicts of Interest 4.8. Study Limitations. A limitation of this retrospective (e authors declare that they have no competing interests. study is that our data depended on the accuracy of the clinical records. (e small size of the study was also a limitation and further research including a larger cohort of Acknowledgments patients with BCC is required to profile this group of patients (e authors acknowledge medical student Minette Steyn in our setting more accurately. NCCN risk factors for re- from the University of Stellenbosch for assistance with data currence such as tumour size and clinical borders could not collection. (e authors thank Professor Carl Lombard and be comprehensively studied due to incomplete data in the Faheema Kimmie from the Division of Epidemiology and majority of clinical records. (e use of population group as a Biostatistics at the University of Stellenbosch for their as- proxy for Fitzpatrick phototype means that our findings in ∗ sistance with data analysis. (e authors also thank Robyn this respect must be viewed with circumspection . In most Schaffner for the figure design. Finally, the authors are cases, only tumour tissue obtained by curettage or punch grateful to the dermatology clinic nursing staff for assisting biopsy was available to assess histological BCC subtypes and with the biopsy registry. perineural invasion. Limited amounts of tumour tissue may not be representative of the entire BCC, potentially com- References promising conclusions about BCC subtypes and recurrence. (e recurrence assessment was limited by the retrospective [1] Work Group, Invited Reviewers, J. Y. S. Kim et al., study design, short follow-up period, incomplete clinical “Guidelines of care for the management of basal cell carci- records, and patients being lost to follow-up. Missed re- noma,” Journal of the American Academy of Dermatology, currences might distort the recurrence rate after double- vol. 78, no. 3, pp. 540–559, 2018. cycle C&E. Prospective research with a longer follow-up [2] M. C. Cameron, E. Lee, B. P. 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A Profile and Three-Year Follow-Up of Patients with Basal Cell Carcinoma in the Western Cape, South Africa

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Hindawi Journal of Skin Cancer Volume 2022, Article ID 8443867, 7 pages https://doi.org/10.1155/2022/8443867 Research Article A Profile and Three-Year Follow-Up of Patients with Basal Cell Carcinoma in the Western Cape, South Africa 1 2 1 3 1 J. C. Gallo , J. W. Schneider , J. de Wet , K. Moxley , H. F. Jordaan , 1 1 W. I. Visser , and B. Tod Division of Dermatology, Department of Medicine, Tygerberg Academic Hospital, Stellenbosch University, Cape Town, South Africa Division of Anatomical Pathology, Department of Pathology, National Health Laboratory Service, Tygerberg Academic Hospital, Stellenbosch University, Cape Town, South Africa Registrar Research Support O­ce, Research Development and Support Division, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa Correspondence should be addressed to J. C. Gallo; justinegallo86@gmail.com Received 7 March 2022; Accepted 21 April 2022; Published 5 May 2022 Academic Editor: Arash Kimyai Asadi Copyright © 2022 J. C. Gallo et al. �is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Basal cell carcinoma (BCC) is an important malignancy in sub-Saharan Africa. �ere is a paucity of data regarding BCC in South Africa. Aims. To describe the clinicopathological features of patients presenting with BCC in a cohort of South African patients. Methods. �is retrospective descriptive study reviewed the medical records of 149 patients with BCC who attended the dermatology clinic at Tygerberg Academic Hospital from September 2015 to August 2016. Demographic and clinical data of those patients with histologically proven BCC were retrieved from clinical records. �e data included the assessment for BCC recurrence after three years (September 2016–August 2019). Results. Of 390 patients, 155 (39.7%) had histologically con—rmed BCCs. Complete medical records were available for 149 of these patients, and most were male (55.7%) and white (85.9%) with a median age of 70 years. Most patients had their BCC lesions for 12 months (43.1%) before diagnosis. BCCs were mostly located on the head and neck area (58.1%). In most patients (72.0%), a diagnostic punch biopsy con—rmed BCC. Plastic surgeons subsequently excised the BCC lesions in 74.0% of these patients. �e most common histological subtype was nodular BCC (74.0%). �e National Comprehensive Cancer Network (NCCN) risk of recurrence was approximately evenly distributed between high- (54.1%) and low-risk groups (45.9%). �e major high-risk feature was the location (36.6%). Histologically con—rmed BCC recurrence occurred in 9 of the 149 patients (3.7%) over three years. Conclusions. BCC represents a high burden of disease in our setting. Compared to existing studies, the BCCs in this study are clinically and histologically similar to international reports. scalp, neck, and face. Destructive invasion by BCC or 1. Introduction therapeutic interventions may cause functional and cosmetic Basal cell carcinoma (BCC) is a type of keratinocyte cancer problems [4, 5]. (KC) that arises from basal epidermal keratinocytes. BCC is BCC management involves consultations by primary the commonest malignancy of the skin and the commonest healthcare physicians or dermatologists, diagnostic biopsies, human malignancy worldwide [1–3]. BCC represents ap- histopathology review, formal surgical excision in the der- proximately 70–80% of all skin carcinomas, making it the matology o£ce, referral for Mohs micrographic surgery (MMS), or referral for plastic and reconstructive surgery most prevalent cancer in many countries [2, 4, 5]. BCC is rarely fatal (mortality rate <0.1%), but localized and, in selected cases, radiation therapy. Patients require tissue invasion may induce considerable morbidity. Most regular follow-up visits to monitor for BCC recurrence or BCC lesions occur on cosmetically sensitive areas such as the the development of new skin cancers. Delayed diagnosis is a 2 Journal of Skin Cancer significant challenge in low- and middle-income countries. 028) [11]. Data about relevant medical history, previous BCC adds a high-cost burden and strain on the health care treatments for BCC, tumour diameter and location, the procedure performed, and any BCC recurrence were re- system [4, 6]. BCC has been extensively studied in Australia, the trieved for each case from records on the TAH Enterprise United States, and Europe. (ese studies confirmed wide Content Management (ECM) system. Histopathology re- variation in BCC incidence, with the highest rates in Aus- sults were obtained from the National Health Laboratory tralia and the lowest rates in parts of Africa [4, 7]. Higher Service database. BCC recurrence was identified by incidence is related to decreasing latitude, intermittent solar reviewing patient records on the ECM from 1 September ultraviolet radiation (UVR) exposure, and more accurate 2016 to 31 August 2019. Recurrence was defined as “possible reporting practices [4]. Little is known regarding BCC in local recurrence” when histologically confirmed BCC arose populations in low- and middle-income countries such as within the scar of a previously excised BCC [12]. (e South Africa (SA). principal investigator (JG) collated the anonymised data in a SA has one of the world’s largest human immunodefi- Microsoft Excel spreadsheet. ciency virus (HIV) epidemics [8]. HIV-infected patients have a 3- to 5-fold increased risk of developing KCs [7, 9, 10]. 2.5. Patient Characteristics. Patient records did not include SA has high levels of solar UVR due to its geographical Fitzpatrick phototypes. (erefore, we used the population location [9]. Furthermore, skin cancer rates in SA have been group as a crude indication of phototype . A hot-deck increasing [9, 10]. Incomplete reporting to the National imputation method was used when the population group Cancer Registry explains the limited data about BCC in SA, was not indicated [11, 13]. Patients were recorded as making it difficult to monitor the national statistics com- immunosuppressed if they had HIV, had a current malig- pared to other countries [10]. (e paucity of clinicopatho- nancy (excluding KC), had a solid organ transplant, or used logical data for BCC in SA justifies research to address this immunosuppressive medication. knowledge gap and to create greater awareness and a better understanding of BCC in SA. Such studies can facilitate educational and prevention campaigns to assist in curbing 2.6.DiagnosisofBCC. Dermatology trainees and consultants the burden of BCC. from the Division of Dermatology at TAH performed bi- opsies and other surgical procedures. In some cases, patients had more than one BCC, requiring multiple biopsies at the 2. Materials and Methods same visit. 2.1. Study Design. (is retrospective descriptive study in- (e National Comprehensive Cancer Network (NCCN) cluded patients with histologically proven BCC who BCC guidelines define criteria for high recurrence risk to attended the dermatology clinic at Tygerberg Academic include specific tumour locations and sizes, ill-defined Hospital (TAH) between 1 September 2015 and 31 August clinical borders, recurrences, tumours arising in radiotherapy 2016. (e study included a three-year follow-up of patients fields, aggressive histological growth patterns, perineural (until 31 August 2019) to assess for BCC recurrence. involvement, and patient immunosuppression [14]. A pathologist (JWS) and JG retrieved and reviewed histopathology sections of cases where the histopathology 2.2. Study Setting. TAH is a publicly funded academic reports did not include adequate information regarding tertiary level hospital in Cape Town (Western Cape prov- diagnosis, histological growth pattern, or perineural in- ince, SA) with a large drainage area from primary and volvement. JWS reviewed all BCC specimens and categorized secondary health care facilities. TAH serves a population of them according to the 4th edition World Health Organisa- low- to middle-income status. (e dermatology clinic is tion (WHO) classification guideline for tumours [15]. operated by consultant dermatologists, registrar dermatol- ogists, and nurses. (e unit is medically focused, where 2.7. Data Analysis. Continuous variables were summarised excisions and cautery and electrodesiccation (C&E) of low- risk tumours are performed. High-risk and surgically as median with interquartile range (IQR) for non-normal data. Categorical variables were summarised as frequencies challenging tumours are referred to the Division of Plastic and Reconstructive Surgery at TAH for excision. and percentages. 2.8. Ethical Considerations. (e study was approved by the 2.3. Study Sample. During the study period, 696 biopsies Stellenbosch University Health Research Ethics Committee from 390 patients were performed on clinically suspected (SUHREC) (HREC/REF: S19/04/070). All data were ano- skin cancer [11]. We included patients older than 18 years nymised to ensure the confidentiality of participants’ per- with histologically confirmed BCC. Patients with incomplete sonal information. medical records and those lost to follow-up were excluded. (e final sample size for data collection was therefore 149. 3. Results 2.4. Data Collection. Demographic data were obtained as Of 390 patients biopsied for clinically suspected KC, a total secondary data from a previous study (HREC/REF: U16/10/ of 155 had a confirmed diagnosis of BCC (39.7%). Six Journal of Skin Cancer 3 Table 1: Demographic and clinical characteristics of patients with patients with incomplete medical records were excluded. BCC (N � 149). Fifty-six patients (36.1%) presented with multiple BCCs. Demographic and clinical characteristics of 149 patients Variable Frequency, n Percentage, % meeting inclusion criteria are summarised in Table 1. (e Gender median age (interquartile range, IQR) was 70 (61–78) years. Male 83 55.7 In the mixed ancestry group (n � 18), 13 patients Female 66 44.3 (72.2%) had high-risk features. In contrast, the white Population group population group (n � 128) had high-risk features in 67 ∗ White 128 85.9 patients (52.3%). (ere were a 2.8 (95% CI: 0.97 to 7.86) odds Mixed ancestry 18 12.1 of having a higher risk profile in the mixed ancestry group . Black African 1 0.7 However, this finding was not statistically significant. (e Indian/Asian 1 0.7 Not known 1 0.7 single black African patient was at high-risk due to im- munosuppression from HIV infection and had oculocuta- Risk factors Chronic sun exposure 8 5.4 neous albinism (OCA) and, therefore, presumably lightly Immunosuppression 5 3.4 pigmented skin. (e Indian/Asian patient had a high-risk Site of prior radiation 3 2.0 feature due to the BCC occurring in a high-risk location. Oculocutaneous albinism (OCA) 1 0.7 Risk factors for BCC were poorly documented. In 48 Immunosuppression and OCA 1 0.7 cases with this information, the commonest risk factor was Immunosuppression and previous chronic sun exposure (n � 8), of which 6 cases were occu- psoralen ultraviolet 1 0.7 pational. Sun exposure was only captured if it was reported a (PUVA) therapy in the patient’s clinical notes. (e histological assessment None 29 19.5 confirmed the presence of solar elastosis in 161 cases Not known 101 67.8 (65.4%), an absence thereof in 9 cases (3.7%), and “unable to Previous history of skin cancer assess” in 76 cases (31.0%). Where solar elastosis could be Unspecified KC 43 28.9 histologically assessed, it was found in 94.7% of cases. (us, Basal cell carcinoma 24 16.1 it appears that chronic sun exposure was significantly Squamous cell carcinoma 4 2.7 underreported. Cutaneous melanoma 3 2.0 KC and cutaneous melanoma 8 5.4 Immunosuppression was reported in only 7 patients who KC and other skin cancers 2 1.3 collectively had 17 biopsies performed. Two patients were None 11 7.4 HIV-positive, of whom one had previous PUVA treatment, Not known 54 36.2 and the other had OCA. One patient took methotrexate therapy for psoriasis. (ree patients had cancer elsewhere and one was a renal transplant recipient on immunosup- presented in Table 3. One patient was referred to an oph- pressive medication. thalmologist for excision of a lesion close to the eyelid margin A total of 246 BCCs were diagnosed amongst 149 pa- (n � 1). Two patients, one with a high-risk basosquamous tients and the tumour characteristics are summarised in lesion and the other with a squamous cell carcinoma else- Table 2. Combined high-risk histological subtypes, including where, were referred to a multidisciplinary skin cancer clinic. micronodular, morpheaform, and basosquamous subtypes, Excision by a plastic and reconstructive surgeon resulted in 6 amounted to 24 cases (9.8%). From the pigmented BCC recurrences (of 182 cases treated, 3.3%). One patient in the group (n � 22), 8 cases were considered as high-risk BCCs, “other treatments” group had nodal metastases. (is lesion with the most common high-risk feature being increased was a high-risk basosquamous carcinoma referred to the lesion size (n � 6). Closer examination of the pigmented BCC multidisciplinary skin cancer clinic for surgical nodal group (n � 22) in the current study revealed that 15 arose in ∗ clearance. white patients and the remainder (n � 7) from other Recurrence was clinically suspected in 24 cases, although phototypes (Indian/Asian and mixed ancestry ). Of biopsies it was histologically proven in only 9 cases (3.7%) over the from presumably more pigmented phototypes (all skin types three-year follow-up period. Most recurrences occurred excluding white patients ), a third were pigmented BCCs. 12–24 months after the initial event (n � 5). (ere were 8 Ulceration was noted in 54 cases (22.0%). None of our cases cases of local recurrence and 1 case of metastatic spread to showed perineural invasion. draining lymph nodes (the basosquamous carcinoma Figures 1 and 2 depict BCC location in the cohort. BCCs mentioned above). New BCC lesions in locations other than were more common on the left side of the face (n � 47) the index BCC lesion occurred in 83 cases (33.7%). compared to the right side of the face (n � 39) (Figure 2). (e side of the face was not specified in 31 cases, and the remaining 9 cases were in the midline. (e nose was the most 4. Discussion common area of the face involved (n � 43), followed by the cheeks (n � 24). BCC is a common malignancy with significant morbidity Fifty-six (22.8%) patients were treated by double-cycle and health economic implications. A large body of research C&E or formal excision at the dermatology clinic. NCCN risk on BCC is available. However, little local data exist about stratification, final treatment modalities, and recurrences are BCC in the South African context. (e purpose of this 4 Journal of Skin Cancer Table 2: Clinical and pathological data of all incident basal cell Head & neck: 143 carcinomas (N � 246 biopsy samples). Head: 135 Neck: 8 Variable Frequency, n Percentage, % Clinical diameter (mm) <10 28 11.4 Trunk: 43 Anterior: 18 10–19 27 11 Posterior: 25 ≥20 19 7.7 Not stated in clinical notes 172 69.9 Upper limbs: 30 Duration (months) Right: 17 <6 months 67 27.2 Left: 13 6–12 months 51 20.7 >12 months 106 43.1 Genitalia: 1 Participant unsure 9 5.3 Not stated in clinical notes 13 3.7 Lower limbs: 27 Diagnostic procedure Right: 11 Punch biopsy 177 72.0 Left: 14 Double-cycle C&E 45 18.3 Undefined: 2 Excisional biopsy 21 8.5 Incisional biopsy 2 0.8 Shave biopsy 2 0.8 BCC subtype Nodular 182 74.0 Figure 1: Distribution of basal cell carcinoma tumours on the body Pigmented 22 8.9 (n � 244, n � 2 location not stated). Micronodular 21 8.5 Superficial 5 2.0 Morpheaform 2 0.8 High-risk area Left Right Basosquamous 1 0.4 Medium risk area Unable to assess 13 5.3 NCCN risk stratification 4 5 High-risk 133 54.1 Low-risk 113 45.9 Number of high-risk features 4 10 14 1 high-risk feature 107 43.5 5 4 2 high-risk features 22 8.9 3 high-risk features 4 1.6 High-risk features Location 90 36.6 9 3 Size 24 9.8 4 1 2 3 4 3 Aggressive growth pattern 24 9.8 Immunosuppression 17 6.9 Site of prior radiation 5 2.0 Recurrent BCCs 3 1.2 Figure 2: Distribution of basal cell carcinoma tumours on the face (n � 126). (e area in red is the high-risk mask area of the face (n � 87), and the blue area signifies the rest of the face, which is a retrospective descriptive study was to determine the prev- medium risk (n � 39). alence, clinicopathological features, and recurrence of BCC in a cohort of patients presenting with histologically proven BCC at a single institution. given the higher risk profile of the mixed ancestry group compared to the white population group (72.2% versus 52.3% with high-risk features). (e prevalence of this out- 4.1. Demographic Characteristics. (e overall prevalence of come should be reexamined in research statistically powered BCC in patients with clinically suspected skin cancer in this for assessing this outcome, as it has important clinical im- study sample was 39.7%. In keeping with international plications. (is study could not provide causes for the trends, most patients with BCC were male (55.7%) and possible risk-related differences between these two groups, white (85.9%) with a median age of 70 years [2, 16, 17]. and further studies could investigate this question. Data regarding BCC in other population groups in SA are sparse [18, 19]. In the United States, studies show that skin cancer occurs less frequently in darker pigmented skin types 4.2. Risk Factors for the Development of BCC. Although SA [19, 20]. Our study is in keeping with this trend. also has a high rate of year-round solar UVR exposure, the Skin cancer outcomes tend to be worse in patients with population composition is very different from other coun- pigmented skin types [21]. Our findings echo this observation tries in the southern hemisphere with high BCC rates, such Journal of Skin Cancer 5 Table 3: NCCN risk stratification and final treatment modalities for BCC lesions (N � 246). Risk stratification Treatment modality, n (%) Total high- and low-risk (N � 246) High-risk (n � 135) Low-risk (n � 111) ∗∗ ∗∗ Excision by plastic and reconstructive surgery 182 (74.0) 109 (44.3) (3 ) 73 (29.7) (3 ) ∗∗ Double-cycle C&E at dermatology 37 (15.0) 18 (7.3) 19 (7.7) (2 ) Excision at dermatology 19 (7.7) 4 (1.6) 15 (6.1) ∗∗ Other treatments 3 (1.2) 2 (0.8) (1 ) 1 (0.4) Loss to follow-up 5 (2.0) 2 (0.8) 3 (1.2) ∗∗ (n ) represents the number of recurrent cases in a specific treatment modality. as Australia [19]. Solar elastosis was observed in most cases, lesion size at the time of diagnosis, highlighting the diag- suggesting significant sun damage in these patients. Re- nostic delay in these challenging cases. In previous studies, pigmented BCCs have been shown to predominate in darker garding immunosuppression, SA has one of the highest rates of HIV in the world at an estimated 13% prevalence, and pigmented skin types [22, 24]. Pigmented BCCs were more prevalent in pigmented skin types in this cohort. (is is approximately, 7-8 million people were living with HIV in 2020 [8]. Both HIV-positive patients in our study had other clinically relevant as pigmented BCCs may be misdiagnosed as seborrheic keratoses or melanocytic naevi, for example, in risk factors for BCC (OCA and previous PUVA exposure). SA theoretically has a population uniquely predisposed to darker skin types. Dermoscopy can assist in differentiating BCC due to high levels of UVR coupled with a large portion such lesions from BCC [25]. Clinicians should be aware of of the population being immunosuppressed due to HIV. this important differential diagnosis in patients with darker Further studies are required to fully understand this. skin types. 4.3. Duration of BCC Prior to Diagnosis. Delayed BCC di- 4.5. National Comprehensive Cancer Network (NCCN) Risk agnosis has been linked to recurrence and metastatic risk Stratification. Our cohort was stratified utilizing the NCCN [22]. Most of the patients in this study presented to the risk for recurrence stratification, defining a large proportion dermatology clinic having had BCC for more than of patients as high-risk for recurrence (n � 133, 54.0%), 12 months. Simultaneously, most cases involved conspic- mostly due to BCC location. A low recurrence rate was observed; however, limitations in the methodology mean uous areas such as the face, and there was a high proportion of large, locally advanced lesions at presentation (18.7% were that this has probably been underreported. larger than 10 mm). (is suggests a lack of awareness about the clinical signs of BCC. (ere is a need to educate patients 4.6. BCC Treatment. (e goal of BCC treatment is a cure and health-care workers to identify BCC and seek profes- with maximum preservation of function, cosmesis, and low sional medical care promptly, thereby improving surgical complication rates [3, 26, 27]. (e NCCN guidelines for the outcomes and limiting disfigurement due to larger tumours surgical treatment of BCC recommend that low-risk BCCs [2, 22]. less than 2 cm in diameter be excised with a 4 mm clinical margin. MMS is the gold standard treatment for high-risk 4.4. Histology of BCC. (ere are several described histo- BCCs as it offers the highest cure rate [27–29]. A study logical subtypes of BCC [15, 23]. (e World Health Orga- evaluating MMS for BCC treatment in SA echoed inter- nisation (WHO) classifies the various BCC subtypes national data and showed that MMS offers the highest cure according to their different growth patterns [15]. Nodular, rates with a low recurrence rate (0.1%) [29]. MMS is not a superficial, and pigmented BCC subtypes are generally treatment option at TAH. considered less aggressive, whereas micronodular, mor- Double-cycle C&E produced good results for our cohort, with seemingly low recurrence rates. C&E is indicated for pheaform, basosquamous, and infiltrating subtypes are more aggressive. Recent research has highlighted a different trend the treatment of small, low-risk nonfacial BCCs and patients who are not surgical candidates [26]. Although not rec- for the involvement of lateral or deep margins according to different histological subtypes [23]. Lateral involvement is ommended by international guidelines, C&E can be con- more frequent for the morpheaform subtype whereas the sidered in low-resource settings for the treatment of high- deep margin is more involved in the nodular subtype [23]. In risk BCCs, since it is a convenient and cost-effective pro- this study, the most common BCC subtype was nodular cedure. (is occurs in carefully selected patients at TAH. (74.0%), in line with international literature [2, 23]. (e BCC recurrence in high-risk areas treated with C&E is re- more aggressive histological subtypes (n � 24, 9.8%) are ported to be significantly higher compared to surgical al- deemed high-risk for recurrence using the NCCN guidelines ternatives (6.9% versus 3.8% respectively) [30, 31]. High-risk [14]. BCCs treated with C&E require more rigorous follow-up for recurrence, which could result in an increased demand on Pigmented BCCs are considered a less aggressive his- tological subtype [24]. (ere was a high proportion of other resources and loss to follow-up. Training primary and secondary healthcare workers to high-risk features among pigmented BCCs in this cohort. (e most common high-risk feature was increased clinical diagnose and treat low-risk BCCs with C&E could offer 6 Journal of Skin Cancer better treatment outcomes than long delays in referral to a context. Furthermore, early surgical management of BCCs tertiary dermatology centre. Surgical training of dermatol- will improve patients’ outcomes and reduce the risk of future ogy trainees to excise high-risk BCCs would necessitate complications. fewer referrals to plastic and reconstructive surgery. Further studies are required to assess the need for an adapted BCC Data Availability risk stratification in resource-limited environments and more accurately evaluate the success of double-cycle C&E in Data can be available on request. (e requesting party can selected high-risk lesions. contact the corresponding author. Additional Points 4.7. BCC Recurrence. Possible recurrence was observed in 9 patients (3.7%). Six patients with recurrent BCC were ini- Variations in the epidemiology and clinical features of BCC tially treated for their primary BCC by surgical excision, and significantly correlate with patients’ Fitzpatrick phototypes, the majority occurred 12–24 months after the initial event. justifying the inclusion of this data [21]. While the pop- (ese results are in keeping with international trends of BCC ulation group (a social construct) is not reliably correlated recurrence rates [3, 22]. However, patients were only fol- with the phototype, it is used in this study as a crude proxy. lowed up over three years, and cases could have recurred after this time or been lost to follow-up. A randomised Ethical Approval control trial with a 10-year follow-up period found that over 50% of BCC recurrences occur after five years [30]. (e study was approved by the Stellenbosch University (erefore, the three-year follow-up period in this study Health Research Ethics Committee (SUHREC). could lead to a misleadingly low recurrence rate. Conflicts of Interest 4.8. Study Limitations. A limitation of this retrospective (e authors declare that they have no competing interests. study is that our data depended on the accuracy of the clinical records. (e small size of the study was also a limitation and further research including a larger cohort of Acknowledgments patients with BCC is required to profile this group of patients (e authors acknowledge medical student Minette Steyn in our setting more accurately. NCCN risk factors for re- from the University of Stellenbosch for assistance with data currence such as tumour size and clinical borders could not collection. (e authors thank Professor Carl Lombard and be comprehensively studied due to incomplete data in the Faheema Kimmie from the Division of Epidemiology and majority of clinical records. (e use of population group as a Biostatistics at the University of Stellenbosch for their as- proxy for Fitzpatrick phototype means that our findings in ∗ sistance with data analysis. (e authors also thank Robyn this respect must be viewed with circumspection . In most Schaffner for the figure design. Finally, the authors are cases, only tumour tissue obtained by curettage or punch grateful to the dermatology clinic nursing staff for assisting biopsy was available to assess histological BCC subtypes and with the biopsy registry. perineural invasion. Limited amounts of tumour tissue may not be representative of the entire BCC, potentially com- References promising conclusions about BCC subtypes and recurrence. (e recurrence assessment was limited by the retrospective [1] Work Group, Invited Reviewers, J. Y. S. Kim et al., study design, short follow-up period, incomplete clinical “Guidelines of care for the management of basal cell carci- records, and patients being lost to follow-up. Missed re- noma,” Journal of the American Academy of Dermatology, currences might distort the recurrence rate after double- vol. 78, no. 3, pp. 540–559, 2018. cycle C&E. Prospective research with a longer follow-up [2] M. C. Cameron, E. Lee, B. P. 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Published: May 5, 2022

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