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Prevalence of Squamous and Basal Cell Carcinomas in African Albino Skin Cancer Lesions: A Systematic Review and Meta-Analysis of Proportion

Prevalence of Squamous and Basal Cell Carcinomas in African Albino Skin Cancer Lesions: A... Hindawi Journal of Skin Cancer Volume 2022, Article ID 5014610, 8 pages https://doi.org/10.1155/2022/5014610 Research Article Prevalence of Squamous and Basal Cell Carcinomas in African Albino Skin Cancer Lesions: A Systematic Review and Meta-Analysis of Proportion Nnaemeka T. Onyishi and Samuel R. Ohayi Histopathology Department, Enugu State University College of Medicine Parklane, Enugu, Nigeria Correspondence should be addressed to Nnaemeka T. Onyishi; tedcoj@gmail.com Received 10 May 2022; Accepted 9 August 2022; Published 30 August 2022 Academic Editor: Arash Kimyai Asadi Copyright © 2022 Nnaemeka T. Onyishi and Samuel R. Ohayi. �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. Context. Keratinocyte carcinomas are the most common malignant condition in Caucasian populations. African albinos have hypomelanized sensitive skin that is quite susceptible to photocarcinogenesis. Of the keratinocyte carcinomas, squamous cell carcinoma (SCC) has been found more frequent in pigmented Africans, while basal cell carcinoma (BCC) predominates in Caucasians. While some studies report a preponderance of SCC over BCC in African albinos, congruent with the situation in pigmented Africans, other reports have found BCCs to be more frequent and consistent with the pattern in Caucasians. Objective. To estimate the prevalence of cutaneous SCC and BCC in all histologically conŠrmed skin cancer lesions in African albinos.�e following Šve databases are as follows: African Journals Online (AJOL), PubMed, Europe PMC, and Google Scholar were searched for relevant articles. Study Selection: included studies were case series and cross-sectional studies of histologically conŠrmed skin cancers in African albinos. Data extraction and synthesis: data extraction and synthesis was informed by the meta-analysis of observational studies in epidemiology guideline. By random e•ect meta-analysis, we calculated the pooled prevalence of SCC and BCC in skin cancer lesions of the African albinos. Result. We abstracted 695 skin cancer lesions from 540 African albinos (275 male and 241 female albinos with sex not stated in 24 subjects). �ere were 419 SCCs and 249 BCCs. By meta-analysis, the pooled prevalence of SCC is 64% (95% CI; 50–77%). �e prevalence for BCC is 31% (95% CI; 19–45%). Conclusion. Overall, squamous cell carcinoma is the predominant type of keratinocyte carcinoma reported in African albinos. SCC is preponderant in case series of surgical excision biopsies while BCC predominates in studies reporting on albino skin surveillance programmes. Caucasians but only 1%–2% in black people [5]. While the 1. Introduction keratinocyte carcinomas and cutaneous melanomas seem- Keratinocyte carcinoma-squamous cell carcinoma (SCC) ingly account for about 40% of all malignant neoplasms in and basal cell carcinoma (BCC) are the most common the US whites [6], a number of hospital studies in Africa malignant neoplasm in fair skinned populations [1]. It was disclose that skin cancers constitute only 5.5%–13% of all estimated that over 5 million nonmelanoma skin cancers diagnosed malignancies [7–9]. existed in the United States and that over 3 million people However, a subpopulation of Africans, the African al- had been treated for nonmelanoma skin cancers in 2012 binos, has elevated risk for skin cancer. Albinos tend to [2]. Also, the incidence rates for SCC and BCC have been develop multiple cutaneous malignancies, at younger age found to be very high in parts of Australia and England and in sun-exposed body sites. �is increased propensity for [1, 3, 4]. cutaneous malignancies derives from genetically inherited In contrast, pigmented Africans have low risk for cu- disorder in skin melanization, which bequeaths the albino taneous malignancies. A comprehensive review estimates with hypomelanized, sun-sensitive skin susceptible to cu- that skin cancer accounts for 20%–30% of all neoplasms in taneous carcinogenesis [10]. 2 Journal of Skin Cancer Studies show that epidemiology and the incidence pro- subgroup in a larger sample of Africans [18]. Excluded were portionofthekeratinocytecarcinomas(SCCandBCC)differ all studies in which the malignant diagnosis was not his- tologically confirmed and all skin cancer cases in albino in Caucasians and pigmented Africans. Caucasians have propensity for multiple keratinocyte carcinomas, which fea- individuals not of African descent or of African descent but ture more at sun-exposed body sites, and with respect to the not reported from Sub-Saharan Africa [18]. incidence proportion, there is a preponderance of BCC over SCC in Caucasians [11]. )e BCC to SCC incidence ratio of 2.3.DataCollection. Dataextractedfromthearticlesinclude about 4:1 had previously been reported, but recent studies author, year of study, country of study, type of study, brief suggest that this ratio narrows significantly with increasing description of study, total number of subjects, no of albinos age[2,11,12].Incontrast,pigmentedAfricansrarelydevelop withskincancer,sexdistributionofalbinoswithskincancer, BCC.Inarecentanalysisof450Africanpatientswithprimary mean and median age of albinos with skin cancer, and cutaneousmalignancyinaNigerianhospital,39hadBCCand histologic types of albino skin cancer. )e process of data 74% (29/39) of these occurred in African albinos [13]. Most extractionwasindependentlyundertakenbythetwoauthors keratinocyte carcinomas in pigmented Africans are SCC and disagreements were resolved by discussion and con- carcinomas, often occurring in non-sun-exposed sites and sensus among the authors [18]. arising from or commonly associated with chronic inflam- matory conditions and scars [14]. )e epidemiology of keratinocyte carcinomas in African 2.4. Quality Assessment of Individual Studies. Methodological albinos mirrors that of the Caucasians in some respect. quality of the included studies was assessed using a modifi- Similar to the Caucasians, keratinocyte carcinomas in Af- cation of Newcastle–Ottawa Scale adapted for case series [19]. rican albinos tend to be multifocal and more at sun-exposed )is tool consists of eight items under four domains. Some of body sites. [13] But, there have been variations in the in- the items are related to reports of adverse drug event and thus cidence proportion of keratinocyte carcinomas reported in are not relevant to determining the validity of studies included African albinos. While some studies [15] report a prepon- in our review. Our quality assessment was based on scores in derance of SCC over BCC, similar to pigmented Africans. the domain of selection, ascertainment, and reporting. Each of Some other studies [16, 17] have found BCC to be more the included study scored one or two points in each of these frequent than SCC in African albinos consistent with the threedomains.Anaggregatescoreof3or4wasconsideredlow situation in Caucasians. With these reported discrepancies quality while a score of 5 or 6 was appraised high quality. inview,weundertookasystematicreviewandmeta-analysis Discordantassessmentswereresolvedbyconsensusamongthe of all existing studies reporting on skin cancers in African authors (Table 1) [18]. albinos aiming to establish the prevalence of the various types of keratinocyte carcinomas (SCC and BCC) among African albinos with skin cancer. 2.5. Statistical Analysis. We used the metafor package of R statisticalsoftwaretocalculatetheprevalenceproportionsof SCCandBCCintheaggregateskincancerburdenofAfrican 2. Methods albinos. African albinos often presented multiple or mul- Methods adapted for this review had been previously de- tifocalskintumors,thus,theproportionofSCCandBCCfor scribed in our first manuscript, which focused on cutaneous each of the included study was calculated using the total melanoma [18]. number of cancer lesions reported in that study as the denominator. )en, using the restricted maximum-likeli- hood estimator of the random effect model, we calculated 2.1.LiteratureSearchandStudySelection. Fourindexingsites, the weighted average proportions for the two keratinocyte considered the preferred hosts of the African biomedical lit- carcinomas after transformation of the raw proportions by erature, were comprehensively searched for eligible publica- the Freeman–Turkey double arcsine method in order to tions. )e sites were African Journals Online (AJOL), Google achieve normality and variance stability [20]. Heterogeneity Scholar,PubMed,andEuropePMC.)esearchwasconducted 2 2 across included studies was assessed using I , τ , and on May 28, 2020, and updated on September 2020. )e da- Cochrane Q test. I values below 25% were considered low tabases were searched iteratively with the following string of heterogeneity; 25–75%, moderate heterogeneity; above 75%, key terms: “skin cancer in African albinos,” “cutaneous ma- high heterogeneity. Cochran p values below 0.1 were con- lignancy in African albinos,” and“skin cancer in Africans.” As sidered significant. Publication bias was assessed by the this is a second of a two-part report, the full-search strategy funnel plot and Egger’s unweighted regression test. used in data acquisition has been detailed in our first publi- cation that focused on melanoma skin cancers [18]. 3. Result 2.2. Inclusion and Exclusion Criteria. )e included studies 3.1. Study Selection. Database search yielded 575 potentially are case series or cross-sectional studies of skin cancer in relevant records, most of which were irrelevant articles that African albinos. In the included studies, skin cancer lesions were excluded following title and abstract screening. Forty- must have been histologically classified and African albinos six full-text articles were acquired and assessed for eligibility were the overall subject of the study or were identified as a of which 23 fulfilled the inclusion criteria (Figure 1). Journal of Skin Cancer 3 Table 1: Risk of bias assessment tool [19]]. the pooled prevalence was 31% (95CI; 19–41%). Figure 2 is a forest plot showing the individual study prevalence of SCC, A. Selection (Does the patient(s) represent(s) the whole the pooled prevalence, and the heterogeneity statistics. experience of the investigator (center) or is the selection method Individual study prevalence and pooled prevalence of BCC unclear to the extent that other patients with similar presentation are similarly displayed in Figure 3.�ere was high heteroge- may not have been reported?) neity in the prevalence estimates across all the included studies i. Cases were selected over a speciŠed range of period? 2 points (Cochrane Q (df )  195, p  < 0.01). Also, I the ratio of ii. Selection approach unclear? 1 point B. Ascertainment of outcome: (How were the cases ascertained?) between the study variance to the total variance was 89% (95% i. Clinical records? 2 points CI; 85%–96%) just as τ ; another measure of variance between ii. Self-report or other methods? 1point studies was 0.1(95%CI; 0.05–0.2), further highlighting the C. Reporting: heterogeneity of the prevalence estimates across studies. i. Cases described in su¬cient details? 2 points Sensitivity analysis did not signiŠcantly alter the pooled ii. Cases scanty with some missing information? 1point estimate or the heterogeneity statistics. Also, moderator analyses were done using a sample size greater than 20, country of study (Nigeria vs. others), and study specifying 575 Records identified database search multifocal tumour as moderating variables. Observed het- 311 AJOL 226 Google scholar erogeneity was not explained by any of the moderating 38 PubMed 2 variables as R , and �e amount of heterogeneity accounted 0 Cochrane library for by the moderators was 0%. Publication bias: Egger’s test of funnel plot asymmetry was not signiŠcant, z  0.60, p  0.55, suggesting a lack of publication bias in the present review (Figure 4). 575 Records screened in title and abstracts. 4. Discussion 529 Excluded 478 Irrelevant articles 51 Duplicates. African albinos have creamy white skin, sandy yellow hair, and brown hazel eyes, which are the phenotypic conse- 46 Full-text articles assessed for eligibility quence of inherited genetic defects in melanin synthesis and pigmentation of their skin, hair, and ocular tissues [41]. �is 23 Excluded 18 Did not meet the inclusion genetic inheritance and distinctive physical appearance in a criteria. 4 Have incomplete data. population of black pigmented people predisposes the Af- 1 Contained data reported in rican albino to some existential challenges such as social another paper. discrimination, and in some places, physical assault with 23 Studies included in meta-analysis body dismemberment [42, 43]. Healthwise, they uniformly Figure 1: PRISMA ®ow chart of the article selection process. develop visual abnormalities and have elevated risk for photodermatosis and skin cancer [10, 30]. For the African albino, however, skin cancer is a very 3.2. Study Characteristics. Characteristics of the 23 included important health problem. Being deŠcient in the protective studies are shown in Table 2. �e studies were 23 case series melanin pigment and inhabiting a climate of high ambient and cross-sectional studies with the publication year ranging sunshine predisposes African albinos to the photocarcinogenic from 1953 to 2020. Most of the studies were done in Nigeria e•ect of high UV radiation. Epidemiologic studies of skin followed by Tanzania. SpeciŠcally, 10 of the studies cancer in Africans report that, compared with normally [15, 21–29] had only albino skin cancer subjects; 4 studies pigmented Africans, African albinos have higher frequency of [16, 30–32] equally had only albino subjects but reported on keratinocyte cancers, which occur at a signiŠcantly younger skin cancers and other skin diseases; 9 studies [13, 33–40] age, and they develop multiple and/or recurrent lesions which had mixed samples of albinos and nonalbinos. feature more at sun-exposed body sites [25]. �e risk of bias assessment or methodological quality Meta-analysis, originally applied in the synthesizing score for the included studies is presented in Table 3. �e results of clinical trials and determining the e•ects of study quality score ranged from 3 to 6 by the assessment tool treatment interventions, has found escalating use in deriving we used. Twenty-one studies were assessed to be of high precise estimates of disease frequency such as incidence rate quality and 2 were assessed low quality. and prevalence proportions [44]. �e present systematic review synthesized data from 3.3. Synthesis of Results. From the 23 studies, we identiŠed eligible case series and cross-sectional studies of skin cancers 540 African albinos presenting 695 histologically conŠrmed in African albinos and attempted to establish the prevalence skin cancers. �ese were composed of 274 males and 241 proportion of SCC and BCC using the methods of meta- females with sex missing in 24 cases. �ere were 419 SCC analysis. and 249 BCC among the 695 cancer lesions (Table 4). Elaborating on prevalence as a variable, Barendregt et al. By random e•ect meta-analysis, the pooled prevalence of [44] states that disease prevalence is a proportion which is SCC for the 23 studies was 64% (95CI; 50–77%). For BCC, derived by dividing the number of cases of the disease in a 4 Journal of Skin Cancer Table 2: Included studies, country of study, number of albinos, and skin cancer type. Skin cancer type Author; year Country No. of albinos with skin cancer Males Females SCC BCC CM Others Total Shapiro MP; 1953 South Africa 12 9 3 0 0 12 8 4 Datubo–Brown DD; 1991 Nigeria 3 3 0 0 0 3 0 0 Yakubu A; 1993 Nigeria 18 15 3 0 0 18 12 6 Oluwasanmi J; 1969 Nigeria 15 8 6 0 1 15 12 3 Alexander G; 1981 Tanzania 10 21 0 0 0 21 9 1 Lookingbill DP; 1995 Tanzania 10 7 3 0 1 11 5 5 Asuquo ME; 2010 Nigeria 9 5 5 1 0 11 5 4 OparaK O; 2010 Nigeria 20 32 5 0 1 38 10 10 Bangaly T; 2019 Guinea 30 40 0 0 1 41 12 18 Kiprono AS; 2014 Tanzania 86 72 61 1 0 134 41 45 Mabula JB; 2012 Tanzania 64 48 15 1 0 64 38 26 Emadi SE; 2017 Kenya 20 8 15 0 0 23 13 7 Nthumba PM; 2011 Kenya 8 0 8 0 0 8 5 3 Enechukwu AN; 2020 Nigeria 18 9 22 0 9 40 9 9 Awe OO; 2018 Nigeria 22 15 5 2 0 22 11 11 Aluko Olokun; 2015 Nigeria 35 12 16 0 7 35 17 18 Oripelaye MM; 2018 Nigeria 12 8 4 0 0 12 0 0 Asuquo ME; 2013 Nigeria 4 7 0 0 0 7 2 2 Madubuko R; 2018 Nigeria 9 8 1 0 0 9 0 0 Adegbidi H; 2007 Benin Republic 5 1 12 0 0 13 3 2 Saka B; 2020 Togo 33 21 31 0 2 54 17 16 Okafor CO; 2020 Nigeria 86 64 33 0 0 97 38 48 Chidothe IA; 2014 Malawi 7 6 1 0 0 7 6 1 SCC: squamous cell carcinoma; BCC: basal cell carcinoma; CM: cutaneous melanoma. Table 3: Risk of bias assessment score for each of the included study. A B C 1st Author; study year Aggregate score Selection Ascertainment of outcome Reporting 1 Adegbidi H; 2007 2 2 2 6 2 Alexander G; 1981 1 2 2 5 3 Aluko Olokun; 2015 1 1 2 4 4 Asuquo ME; 2013 1 2 2 5 5 Asuquo, ME; 2010 2 2 2 6 6 Awe OO; 2018 2 2 1 5 7 Bangaly T; 2019 2 2 2 6 8 Chidothe IA; 2014 1 2 2 5 9 Datubo–Brown DD; 1991 1 2 1 4 10 Emadi SE; 2017 2 2 2 6 11 Enechukwu AN; 2020 2 2 1 5 12 Kiprono AS; 2014 2 2 2 6 13 Lookingbill DP; 1995 2 2 1 5 14 Mabula JB; 2012 2 2 2 6 15 Madubuko R; 2018 2 2 2 6 16 Nthumba PM; 2011 1 2 2 5 17 Okafor CO; 2O2O 2 2 2 6 18 Oluwasanmi J, 1969 2 2 2 6 19 Opara KO; 2010 2 2 2 6 20 Oripelaye MM; 2018 1 2 2 5 21 Saka B; 2020 2 2 2 6 22 Shapiro MP, 1953 2 2 2 6 23 Yakubu A, 1993 2 2 2 6 Aggregate score: 3, 4 (low quality); 5, 6 (high quality). population by the population number. Its value always lies different cancer types. )us, the number of skin cancer between0and1,andsumovermulticategoriesamountsto1 lesions we abstracted (695) was more than the number of [44].Averynotablefeatureofskincancer inAfricanalbinos albinos with skin cancer (540). We determined the preva- is the propensity for multifocal or multiple tumours with an lence or proportion of SCC and BCC in all the histologically individual patient sometimes presenting histologically confirmed skin cancer lesions of African albinos. Journal of Skin Cancer 5 Table 4: Skin cancer type and sex of 540 African albinos with cutaneous malignancy . Variable Frequency Sex Male 275 Female 241 Missing 24 Total 540 Skin cancer type 419 Squamous cell carcinoma 419 Basal cell carcinoma 249 Cutaneous melanoma 5 ∗∗ Others 22 Total 695 ∗ ∗∗ ; Some patients presented multifocal cancers: 9 basosquamous carcinoma, 10 adenoid cystic carcinoma, 1 malignant adnexal tumour, 1 sarcoma, and 1 unspeciŠed histology. Study scc skin cancers Prevalence 95% C.I. ShapiroMP 1953 9 12 0.75 [0.46; 0.96] Datubo−BrownDD 1991 3 3 1.00 [0.50; 1.00] YakubuA 1993 15 18 0.83 [0.62; 0.98] OluwasanmiJ 1969 8 15 0.53 [0.28; 0.78] AlexanderG 1981 21 21 1.00 [0.92; 1.00] LookingbillDP 1995 7 11 0.64 [0.33; 0.90] AsuquoME 2010 5 11 0.45 [0.17; 0.76] OparaKO 2010 32 38 0.84 [0.71; 0.94] BangalyT 2019 40 41 0.98 [0.90; 1.00] KipronoAS 2014 72 134 0.54 [0.45; 0.62] MabulaJB 2012 48 64 0.75 [0.64; 0.85] EmadiSE 2017 8 23 0.35 [0.16; 0.56] NthumbaPM 2011 0 8 0.00 [0.00; 0.20] EnechukwuAN 2020 9 40 0.22 [0.11; 0.37] Awe OO 2018 15 22 0.68 [0.47; 0.86] AlukoOlokun 2015 12 35 0.34 [0.19; 0.51] OripelayeMM 2018 8 12 0.67 [0.37; 0.91] AsuquoME 2013 7 7 1.00 [0.77; 1.00] MadubukoR 2018 8 9 0.89 [0.58; 1.00] AdegbidiH 2007 1 13 0.08 [0.00; 0.30] SakaB 2020 21 54 0.39 [0.26; 0.52] OkaforCO 2020 64 97 0.66 [0.56; 0.75] ChidotheIA2014 6 7 0.86 [0.48; 1.00] 695 0.64 Random effects model [0.50; 0.77] 2 2 2 Heterogeneity: I = 89%,τ = 0.0903,χ = 194.98 (p < 0.01) Prevalence of SCC Figure 2: Forest plot showing the pooled prevalence of squamous cell carcinoma in 23 included studies. �is pooled prevalence of SCC was 64% while that of proportion of SCC among all histologically conŠrmed skin BCC was 31%, and these represents average proportion of cancer lesions in African albinos would be 60.2% (419/695) SCC and BCC in all the studies weighted by the inverse of and that of BCC, 35.8% (249/695). �ese Šgures are quite their sampling variances. Heterogeneity statistics indicate comparable to the pooled prevalence established by meta- a lack of homogeneity in the reported proportions across analyses. all the included studies. �is was not explainable by Marçon et al. [45] in Brazil suggest that the frequency of sensitivity or moderator analysis. Small sample sizes and BCC might be equal to SCC in albinos and that studies variations in study settings could be responsible. In spite reporting more SCC are hospital excision biopsies of ad- of this observed heterogeneity, the estimated prevalence vanced tumours in which SCCs are more likely to pre- Šgures appear valid. �is is because, by crude unweighted dominate, being the more aggressive of the two tumours and often requiring surgical attention. �is view seems to be pooling of the individual study proportions (analogous to the ditched “vote counting” method previously used in supported by the fact that two studies that reported more meta-analysis of clinical trials and interventions), the BCC than SCC in African albinos feature biopsies taken at 6 Journal of Skin Cancer Study bcc skin cancers Prevalence95% C.I. ShapiroMP 1953 3 12 0.25 [0.04; 0.54] Datubo−BrownDD 1991 0 3 0.00 [0.00; 0.50] YakubuA 1993 3 18 0.17 [0.02; 0.38] 0.40 [0.16; 0.66] OluwasanmiJ 1969 6 15 AlexanderG 1981 0 21 0.00 [0.00; 0.08] LookingbillDP 1995 3 11 0.27 [0.04; 0.58] 5 11 0.45 [0.17; 0.76] AsuquoME 2010 OparaKO 2010 5 38 0.13 [0.04; 0.26] BangalyT 2019 0 41 0.00 [0.00; 0.04] KipronoAS 2014 61 134 0.46 [0.37; 0.54] MabulaJB 2012 15 64 0.23 [0.14; 0.35] 23 0.65 [0.44; 0.84] EmadiSE 2017 15 NthumbaPM 2011 8 8 1.00 [0.80; 1.00] EnechukwuAN 2020 22 40 0.55 [0.39; 0.70] Awe OO 2018 5 22 0.23 [0.07; 0.43] AlukoOlokun 2015 16 35 0.46 [0.29; 0.62] [0.09; 0.63] OripelayeMM 2018 4 12 0.33 AsuquoME 2013 0 7 0.00 [0.00; 0.23] MadubukoR 2018 1 9 0.11 [0.00; 0.42] 13 0.92 [0.70; 1.00] AdegbidiH 2007 12 SakaB 2020 31 54 0.57 [0.44; 0.70] OkaforCO 2020 33 97 0.34 [0.25; 0.44] ChidotheIA2014 1 7 0.14 [0.00; 0.52] Random effects model 695 0.31 [0.19; 0.45] 2 2 2 Heterogeneity: I = 88%,τ = 0.0827,χ = 179.09 (p < 0.01) Prevalence of BCC Figure 3: Forest plot showing the pooled prevalence of basal cell carcinoma. publication bias for comparative studies are appropriate for observational studies of the type used in meta-analysis of proportions. �e studies examined in meta-analysis of proportion, being noncomparative, are not subject to con- 0.067 siderations of statistical signiŠcance and the direction of result, which are known to preferentially in®uence publi- cation of clinical trials [19, 46, 47]. Nevertheless, we assessed 0.134 for publication bias using the funnel plot. Egger’s test of funnel plot asymmetry was nonsigniŠcant, suggesting a lack of publication bias in the published studies. 0.2 Our study has some strengths and limitations. First, it is, to the best of our knowledge, the Šrst meta-analysis on skin cancer in African albinos and thus represents the 0.267 largest study of albinos with skin cancer to date. �e study was able to yield data, which bolstered the previously re- 0 0.21 0.72 1 ported epidemiologic trends of skin cancer and statistically Proportion established that the prevalence for SCC and BCC in skin Figure 4: Funnel plot of the included studies. cancer lesions. �e study is limited by the small sample sizes of the available studies and dearth of publications devoted exclusively to the subject of albino skin cancer. In routine dermatological examination and surveillance pro- grammes [16, 17]. addition, because our study is a review, we could not validate the histological types of the skin cancers reported Publication bias has been explained, chie®y, in terms of preferential publication of manuscripts with statistically by the included studies. signiŠcant results to the exclusion of those with nonsig- niŠcant results. But some other study characteristics such as 5. Conclusion funding source, research setting, and prevailing theories at the time of publication have been found to equally in®uence In conclusion, we estimated the prevalence proportion of publication [46]. Even though publication bias could con- SCC and BCC in histologically conŠrmed skin cancer lesions found systematic reviews, it has been questioned if the in African albinos. �e pooled average prevalence propor- traditional methods employed in the assessment of tion of SCC amongst all histologically conŠrmed skin cancer Standard Error Journal of Skin Cancer 7 [10] E.S.Hong,H.Zeeb,andM.H.Repacholi,“AlbinisminAfrica lesions in African albinos was 64% (95% CI; 50–77%) and as a public health issue,” BMC Public Health, vol. 6, no. 1, the prevalence of BCC was 31% (95% CI; 19–45%). Squa- mouscellcarcinomaisthepredominanttypeofkeratinocyte [11] B.A.RaaschandP.G.Buettner,“Multiplenonmelanomaskin carcinoma reported in African albinos overall. )is pre- cancer in an exposed Australian population,” International dominance of keratinocyte carcinomas in African albinos Journal of Dermatology, vol. 41, no. 10, pp. 652–658, 2002. relates more the with pattern of occurrence in pigmented [12] H. S. Chahal, K. E. Rieger, and K. Y. Sarin, “Incidence ratio of Africans rather than Caucasians. basal cell carcinoma to squamous cell carcinoma equalizes with age,” Journal of the American Academy of Dermatology, vol. 76, no. 2, pp. 353-354, 2017. Data Availability [13] O. C. Okafor and N. T. Onyishi, “Primary cutaneous ma- )e data used to support the findings of this study are in- lignancies in non-albino and albino Africans,” International Journal of Dermatology, vol. 60, no. 2, pp. 222–228, 2021. cluded within the article. [14] P. M. Nthumba, “Marjolin’s ulcers in sub-Saharan Africa,” World Journal of Surgery, vol.34,no.10,pp.2272–2277,2010. Conflicts of Interest [15] J.B.Mabula,P.L.Chalya,M.D.Mchembeetal.“Skincancers among Albinos at a University teaching hospital in North- )e authors declare that they have no conflicts of interest. western Tanzania: a retrospective review of 64 cases,” BMC Dermatology, vol. 12, no. 1, pp. 5–180, 2012. [16] N. A. Enechukwu, G. O. Ogun, O. I. Ezejiofor et al., “His- Acknowledgments topathologic patterns of cutaneous malignancies in individ- uals with oculocutaneous albinism in Anambra state, Nigeria: )e authors thank Dr. Nnamani Christian and other staff of a paradigm swing?” Ecancermedicalscience, vol. 14, p. 1013, theHistopathologyDepartmentofESUTTeachingHospital, Parklane, for their contributions to the work. [17] B. Saka, J. N. Teclessou, S. A. Akakpo et al., “A histopatho- logical study of skin lesions in individuals with oculocuta- References neous albinism in Togo in 2019,” Journal of Skin Cancer, vol. 2020, Article ID 2361957, 4 pages, 2020. [1] E. Perera, N. Gnaneswaran, C. Staines, A. K. Win, and [18] N. T. Onyishi and S. R. Ohayi, “Cutaneous melanoma in R. Sinclair, “Incidence and prevalence of non-melanoma skin African albinos: a systematic review,” Journal of Clinical and cancerinAustralia:asystematicreview,” Australasian Journal Diagnostic Research, vol. 15, no. 11, pp. WE01–WE06, 2021. of Dermatology, vol. 56, no. 4, pp. 258–267, 2015. [19] M. H. Murad, S. Sultan, S. Haffar, and F. Bazerbachi, [2] H. W. Rogers, M. A. Weinstock, S. R. Feldman, and “Methodological quality and synthesis of case series and case B. M. Coldiron, “Incidence estimate of nonmelanoma skin reports,” BMJ Evidence-Based Medicine, vol. 23, no. 2, cancer(keratinocytecarcinomas)intheUSpopulation,2012,” pp. 60–63, 2018. JAMADermatol, vol. 151, pp. 06360–11086, 2015. [20] N. Wang, How to Conduct a Meta-Analysis of Proportions in [3] P. G. Buettner and B. A. Raasch, “Incidence rates of skin R: A Comprehensive Tutorial Conducting Meta-Analyses of cancer in Townsville, Australia,” International Journal of Proportions in R, Elsevier, Amsterdam, Netherlands, 2018. Cancer, vol. 78, no. 5, pp. 587–593, 1998. [21] G. A. Alexander and U. K. Henschke, “Advanced skin cancer [4] Z.C.Venables,T.Nijsten,K.F.Wongetal.,“Epidemiologyof inTanzanianalbinos:Preliminaryobservations,” Journal of the basal and cutaneous squamous cell carcinoma in the U.K. National Medical Association, vol. 73, no. 11, pp. 1047–1054, 2013–15: a cohort study,” British Journal of Dermatology, vol. 181, no. 3, pp. 474–482, 2019. [22] M. E. Asuquo, O. O. Otei, J. Omotoso, and E. E. Bassey, [5] H. M. Gloster and K. Neal, “Skin cancer in skin of color,” “Letter: skin cancer in albinos at the university of calabar Journal of the American Academy of Dermatology, vol. 55, teaching hospital, calabar, Nigeria,” Dermatology Online no. 5, pp. 741–760, 2006. Journal, vol. 16, no. 4, p. 14, 2010. [6] O. N. Agbai, K. Buster, M. Sanchez et al., “Skin cancer and [23] K. O. Opara and B. C. Jiburum, “Skin cancers in albinos in a photoprotection in people of color: a review and recom- teaching Hospital in eastern Nigeria - presentation and mendations for physicians and the public,” Journal of the challengesofcare,” World Journal of Surgical Oncology,vol.8, American Academy of Dermatology, vol. 70, no. 4, pp. 748– no. 1, pp. 73–77, 2010. 762, 2014. [24] B. Traore, A. Barry, T. Kourouma, M. Keita, and M. Cisse, [7] G. O. Oseni, P. B. Olaitan, A. O. Komolafe, O. O. Olaofe, “Skin cancers in albinos at surgical oncology unit of donka H. A. M. Akinyemi, and O. A. Suleiman, “Malignant skin nationalhospital(conakry),” Cancer Studies and 2erapeutics, lesions in Oshogbo, Nigeria,” 2e Pan African medical vol. 4, no. 1, pp. 1–5, 2019. journal, vol. 20, pp. 253–256, 2015. [25] S. K. Kiprono, B. M. Chaula, and H. Beltraminelli, “Histo- [8] O. Ochicha, S. T. Edino, A. Z. Mohammed, and A. B. Umar, logical review of skin cancers in African Albinos: a 10-year “Dermatological malignancies in Kano Northern Nigeria: a retrospectivereview,” BMC Cancer,vol.14,no.1,pp.157–164, histopathological review,” Annals of African Medicine, vol. 3, no. 4, pp. 188–191, 2004. [26] O. O. Awe and T. A. Azeke, “Cutaneous cancers in Nigerian [9] P. L. Chalya, J. M. Gilyoma, E. S. Kanumba et al., “Derma- albinos: a review of 22 cases,” Nigerian Journal of Surgery, tological malignancies at a University Teaching Hospital in north-western Tanzania: a retrospective review of 154 cases,” vol. 24, no. 1, pp. 34–38, 2018. [27] M. E. Asuquo, O. O. Otei, I. Bassey, and G. Ebughe, “Ocu- Tanzania Journal of Health Research, vol. 14, no. 1, pp. 9–14, 2012. locutaneous albinism and skin cancer in Calabar,” 8 Journal of Skin Cancer International Journal of Medicine and Medical Sciences,vol.5, [45] C. R. Marçon, J. C. Moraes, M. A. M. de Olivas Ferreira, and C. B. Oliari, “Dermatological and epidemiological profiles of no. 1, pp. 3–5, 2013. [28] B. Saka, S. A. Akakpo, J. N. Teclessou et al., “Skin cancers in patients with albinism in são paulo, Brazil, between 2010 and 2017: a cross-sectional study,” Dermatology, vol. 236, no. 3, peoplewithalbinism inTogoin2019:resultsoftworoundsof national mobile skin care clinics (in review),” BMC Derma- pp. 219–227, 2020. [46] K. M. Coburn and J. L. Vevea, “Publication bias as a function tology, vol. 26, pp. 1–8, 2019. [29] I. A. Chidothe and L. Masamba, “Neoadjuvant chemotherapy of study characteristics,” Psychological Methods, vol. 20, no. 3, pp. 310–330, 2015. in albinos with locally advanced skin cancer at a blantyre [47] P. K. Maulik, M. N. Mascarenhas, C. D. Mathers, T. Dua, and hospital: case series,” Malawi Medical Journal, vol. 26, no. 3, S. Saxena, “Prevalence of intellectual disability: a meta- pp. 97–99, 2014. analysis of population-based studies,” Research in Develop- [30] D. P. Lookingbill, G. L. Lookingbill, and B. Leppard, “Actinic mental Disabilities, vol. 32, no. 2, pp. 419–436, 2011. damage and skin cancer in albinos in northern Tanzania: findings in 164 patients enrolled in an outreach skin care program,” Journal of the American Academy of Dermatology, vol. 32, no. 4, pp. 653–658, 1995. [31] S. E. Emadi, A. J. Suleh, F. Babamahmoodi et al., “Common malignant cutaneous conditions among albinos in Kenya,” Medical Journal of the Islamic Republic of Iran, vol. 31, no. 1, pp. 7–12, 2017. [32] M. C. Roli and O. Abel, “Photodermatoses in the Nigerian albino: a study in an urban hospital in southern Nigeria,” Journal of Medicine in the Tropics, vol. 20, no. 1, pp. 68–73, [33] M. P. Shapiro, P. Keen, L. Cohen, and J. F. Murray, “Skin cancer in the South African Bantu,” British Journal of Cancer, vol. 7, no. 1, pp. 45–57, 1953. [34] D. D. Datubo-Brown, “Primary malignant skin tumor in Nigerians,” Journal of the National Medical Association, vol. 83, pp. 345–348, 1991. [35] A. Yakubu and O. A. Mabogunje, “Skin cancer in African albinos,” Acta Oncologica, vol. 32, no. 6, pp. 621-622, 1993. [36] J. O. Oluwasanmi, A. O. Williams, and A. F. Alli, “Superficial cancer in Nigeria,” British Journal of Cancer, vol. 23, no. 4, pp. 714–728, 1969. [37] P. M. Nthumba, P. C. Cavadas, and L. Landin, “Primary cutaneous malignancies in sub-Saharan Africa,” Annals of Plastic Surgery, vol. 66, no. 3, pp. 313–320, 2011. [38] B. Aluko-Olokun and A. A. Olaitan, “Skin cancer risk factor reductioninAfrica:assessmentofuseofantiretroviraltherapy services by human immunodeficiency virus positive albinos,” HIV & AIDS Review, vol. 14, no. 1, pp. 18–21, 2015. [39] M. M. Oripelaye, A. O. Oladele, F. O. Olanrewaju, and O.O.Olaofe,“)eevolvingpatternofprimaryskincancersin ile-ife, Nigeria,” Serbian Journal of Dermatology and Vene- reology, vol. 10, no. 3, pp. 90–95, 2018. [40] H. Adegbidi, H. Yedomon, F. Atadokpede, M.-C. Balley- Pognon, and F. Do Ango-Padonou, “Skin cancers at the national university hospital of cotonou from 1985 to 2004,” International Journal of Dermatology, vol. 46, no. s1, pp. 26–29, 2007. [41] J. G. R. Kromberg, J. Bothwell, S. H. Kidson, P. Manga, R. Kerr, and T. Jenkins, “Types of albinism in the black southern Africa population,” East African Medical Journal, vol. 89, no. 1, pp. 20–27, 2012. [42] J.Taylor,C.Bradbury-Jones,andP.Lund,“Witchcraft-related Abuse and murder of children with albinism in sub-saharan Africa: a conceptual review,” Child Abuse Review, vol. 28, no. 1, pp. 13–26, 2019. [43] M. H. Brilliant, “Albinism in Africa: a medical and social emergency,” International Health, vol. 7, no. 4, pp. 223–225, [44] J.J.Barendregt,S.A.Doi,Y.Y.Lee,R.E.Norman,andT.Vos, “Meta-analysis of prevalence,” Journal of Epidemiology & Community Health, vol. 67, no. 11, pp. 974–978, 2013. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Skin Cancer Hindawi Publishing Corporation

Prevalence of Squamous and Basal Cell Carcinomas in African Albino Skin Cancer Lesions: A Systematic Review and Meta-Analysis of Proportion

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Copyright © 2022 Nnaemeka T. Onyishi and Samuel R. Ohayi. This 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.
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10.1155/2022/5014610
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Hindawi Journal of Skin Cancer Volume 2022, Article ID 5014610, 8 pages https://doi.org/10.1155/2022/5014610 Research Article Prevalence of Squamous and Basal Cell Carcinomas in African Albino Skin Cancer Lesions: A Systematic Review and Meta-Analysis of Proportion Nnaemeka T. Onyishi and Samuel R. Ohayi Histopathology Department, Enugu State University College of Medicine Parklane, Enugu, Nigeria Correspondence should be addressed to Nnaemeka T. Onyishi; tedcoj@gmail.com Received 10 May 2022; Accepted 9 August 2022; Published 30 August 2022 Academic Editor: Arash Kimyai Asadi Copyright © 2022 Nnaemeka T. Onyishi and Samuel R. Ohayi. �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. Context. Keratinocyte carcinomas are the most common malignant condition in Caucasian populations. African albinos have hypomelanized sensitive skin that is quite susceptible to photocarcinogenesis. Of the keratinocyte carcinomas, squamous cell carcinoma (SCC) has been found more frequent in pigmented Africans, while basal cell carcinoma (BCC) predominates in Caucasians. While some studies report a preponderance of SCC over BCC in African albinos, congruent with the situation in pigmented Africans, other reports have found BCCs to be more frequent and consistent with the pattern in Caucasians. Objective. To estimate the prevalence of cutaneous SCC and BCC in all histologically conŠrmed skin cancer lesions in African albinos.�e following Šve databases are as follows: African Journals Online (AJOL), PubMed, Europe PMC, and Google Scholar were searched for relevant articles. Study Selection: included studies were case series and cross-sectional studies of histologically conŠrmed skin cancers in African albinos. Data extraction and synthesis: data extraction and synthesis was informed by the meta-analysis of observational studies in epidemiology guideline. By random e•ect meta-analysis, we calculated the pooled prevalence of SCC and BCC in skin cancer lesions of the African albinos. Result. We abstracted 695 skin cancer lesions from 540 African albinos (275 male and 241 female albinos with sex not stated in 24 subjects). �ere were 419 SCCs and 249 BCCs. By meta-analysis, the pooled prevalence of SCC is 64% (95% CI; 50–77%). �e prevalence for BCC is 31% (95% CI; 19–45%). Conclusion. Overall, squamous cell carcinoma is the predominant type of keratinocyte carcinoma reported in African albinos. SCC is preponderant in case series of surgical excision biopsies while BCC predominates in studies reporting on albino skin surveillance programmes. Caucasians but only 1%–2% in black people [5]. While the 1. Introduction keratinocyte carcinomas and cutaneous melanomas seem- Keratinocyte carcinoma-squamous cell carcinoma (SCC) ingly account for about 40% of all malignant neoplasms in and basal cell carcinoma (BCC) are the most common the US whites [6], a number of hospital studies in Africa malignant neoplasm in fair skinned populations [1]. It was disclose that skin cancers constitute only 5.5%–13% of all estimated that over 5 million nonmelanoma skin cancers diagnosed malignancies [7–9]. existed in the United States and that over 3 million people However, a subpopulation of Africans, the African al- had been treated for nonmelanoma skin cancers in 2012 binos, has elevated risk for skin cancer. Albinos tend to [2]. Also, the incidence rates for SCC and BCC have been develop multiple cutaneous malignancies, at younger age found to be very high in parts of Australia and England and in sun-exposed body sites. �is increased propensity for [1, 3, 4]. cutaneous malignancies derives from genetically inherited In contrast, pigmented Africans have low risk for cu- disorder in skin melanization, which bequeaths the albino taneous malignancies. A comprehensive review estimates with hypomelanized, sun-sensitive skin susceptible to cu- that skin cancer accounts for 20%–30% of all neoplasms in taneous carcinogenesis [10]. 2 Journal of Skin Cancer Studies show that epidemiology and the incidence pro- subgroup in a larger sample of Africans [18]. Excluded were portionofthekeratinocytecarcinomas(SCCandBCC)differ all studies in which the malignant diagnosis was not his- tologically confirmed and all skin cancer cases in albino in Caucasians and pigmented Africans. Caucasians have propensity for multiple keratinocyte carcinomas, which fea- individuals not of African descent or of African descent but ture more at sun-exposed body sites, and with respect to the not reported from Sub-Saharan Africa [18]. incidence proportion, there is a preponderance of BCC over SCC in Caucasians [11]. )e BCC to SCC incidence ratio of 2.3.DataCollection. Dataextractedfromthearticlesinclude about 4:1 had previously been reported, but recent studies author, year of study, country of study, type of study, brief suggest that this ratio narrows significantly with increasing description of study, total number of subjects, no of albinos age[2,11,12].Incontrast,pigmentedAfricansrarelydevelop withskincancer,sexdistributionofalbinoswithskincancer, BCC.Inarecentanalysisof450Africanpatientswithprimary mean and median age of albinos with skin cancer, and cutaneousmalignancyinaNigerianhospital,39hadBCCand histologic types of albino skin cancer. )e process of data 74% (29/39) of these occurred in African albinos [13]. Most extractionwasindependentlyundertakenbythetwoauthors keratinocyte carcinomas in pigmented Africans are SCC and disagreements were resolved by discussion and con- carcinomas, often occurring in non-sun-exposed sites and sensus among the authors [18]. arising from or commonly associated with chronic inflam- matory conditions and scars [14]. )e epidemiology of keratinocyte carcinomas in African 2.4. Quality Assessment of Individual Studies. Methodological albinos mirrors that of the Caucasians in some respect. quality of the included studies was assessed using a modifi- Similar to the Caucasians, keratinocyte carcinomas in Af- cation of Newcastle–Ottawa Scale adapted for case series [19]. rican albinos tend to be multifocal and more at sun-exposed )is tool consists of eight items under four domains. Some of body sites. [13] But, there have been variations in the in- the items are related to reports of adverse drug event and thus cidence proportion of keratinocyte carcinomas reported in are not relevant to determining the validity of studies included African albinos. While some studies [15] report a prepon- in our review. Our quality assessment was based on scores in derance of SCC over BCC, similar to pigmented Africans. the domain of selection, ascertainment, and reporting. Each of Some other studies [16, 17] have found BCC to be more the included study scored one or two points in each of these frequent than SCC in African albinos consistent with the threedomains.Anaggregatescoreof3or4wasconsideredlow situation in Caucasians. With these reported discrepancies quality while a score of 5 or 6 was appraised high quality. inview,weundertookasystematicreviewandmeta-analysis Discordantassessmentswereresolvedbyconsensusamongthe of all existing studies reporting on skin cancers in African authors (Table 1) [18]. albinos aiming to establish the prevalence of the various types of keratinocyte carcinomas (SCC and BCC) among African albinos with skin cancer. 2.5. Statistical Analysis. We used the metafor package of R statisticalsoftwaretocalculatetheprevalenceproportionsof SCCandBCCintheaggregateskincancerburdenofAfrican 2. Methods albinos. African albinos often presented multiple or mul- Methods adapted for this review had been previously de- tifocalskintumors,thus,theproportionofSCCandBCCfor scribed in our first manuscript, which focused on cutaneous each of the included study was calculated using the total melanoma [18]. number of cancer lesions reported in that study as the denominator. )en, using the restricted maximum-likeli- hood estimator of the random effect model, we calculated 2.1.LiteratureSearchandStudySelection. Fourindexingsites, the weighted average proportions for the two keratinocyte considered the preferred hosts of the African biomedical lit- carcinomas after transformation of the raw proportions by erature, were comprehensively searched for eligible publica- the Freeman–Turkey double arcsine method in order to tions. )e sites were African Journals Online (AJOL), Google achieve normality and variance stability [20]. Heterogeneity Scholar,PubMed,andEuropePMC.)esearchwasconducted 2 2 across included studies was assessed using I , τ , and on May 28, 2020, and updated on September 2020. )e da- Cochrane Q test. I values below 25% were considered low tabases were searched iteratively with the following string of heterogeneity; 25–75%, moderate heterogeneity; above 75%, key terms: “skin cancer in African albinos,” “cutaneous ma- high heterogeneity. Cochran p values below 0.1 were con- lignancy in African albinos,” and“skin cancer in Africans.” As sidered significant. Publication bias was assessed by the this is a second of a two-part report, the full-search strategy funnel plot and Egger’s unweighted regression test. used in data acquisition has been detailed in our first publi- cation that focused on melanoma skin cancers [18]. 3. Result 2.2. Inclusion and Exclusion Criteria. )e included studies 3.1. Study Selection. Database search yielded 575 potentially are case series or cross-sectional studies of skin cancer in relevant records, most of which were irrelevant articles that African albinos. In the included studies, skin cancer lesions were excluded following title and abstract screening. Forty- must have been histologically classified and African albinos six full-text articles were acquired and assessed for eligibility were the overall subject of the study or were identified as a of which 23 fulfilled the inclusion criteria (Figure 1). Journal of Skin Cancer 3 Table 1: Risk of bias assessment tool [19]]. the pooled prevalence was 31% (95CI; 19–41%). Figure 2 is a forest plot showing the individual study prevalence of SCC, A. Selection (Does the patient(s) represent(s) the whole the pooled prevalence, and the heterogeneity statistics. experience of the investigator (center) or is the selection method Individual study prevalence and pooled prevalence of BCC unclear to the extent that other patients with similar presentation are similarly displayed in Figure 3.�ere was high heteroge- may not have been reported?) neity in the prevalence estimates across all the included studies i. Cases were selected over a speciŠed range of period? 2 points (Cochrane Q (df )  195, p  < 0.01). Also, I the ratio of ii. Selection approach unclear? 1 point B. Ascertainment of outcome: (How were the cases ascertained?) between the study variance to the total variance was 89% (95% i. Clinical records? 2 points CI; 85%–96%) just as τ ; another measure of variance between ii. Self-report or other methods? 1point studies was 0.1(95%CI; 0.05–0.2), further highlighting the C. Reporting: heterogeneity of the prevalence estimates across studies. i. Cases described in su¬cient details? 2 points Sensitivity analysis did not signiŠcantly alter the pooled ii. Cases scanty with some missing information? 1point estimate or the heterogeneity statistics. Also, moderator analyses were done using a sample size greater than 20, country of study (Nigeria vs. others), and study specifying 575 Records identified database search multifocal tumour as moderating variables. Observed het- 311 AJOL 226 Google scholar erogeneity was not explained by any of the moderating 38 PubMed 2 variables as R , and �e amount of heterogeneity accounted 0 Cochrane library for by the moderators was 0%. Publication bias: Egger’s test of funnel plot asymmetry was not signiŠcant, z  0.60, p  0.55, suggesting a lack of publication bias in the present review (Figure 4). 575 Records screened in title and abstracts. 4. Discussion 529 Excluded 478 Irrelevant articles 51 Duplicates. African albinos have creamy white skin, sandy yellow hair, and brown hazel eyes, which are the phenotypic conse- 46 Full-text articles assessed for eligibility quence of inherited genetic defects in melanin synthesis and pigmentation of their skin, hair, and ocular tissues [41]. �is 23 Excluded 18 Did not meet the inclusion genetic inheritance and distinctive physical appearance in a criteria. 4 Have incomplete data. population of black pigmented people predisposes the Af- 1 Contained data reported in rican albino to some existential challenges such as social another paper. discrimination, and in some places, physical assault with 23 Studies included in meta-analysis body dismemberment [42, 43]. Healthwise, they uniformly Figure 1: PRISMA ®ow chart of the article selection process. develop visual abnormalities and have elevated risk for photodermatosis and skin cancer [10, 30]. For the African albino, however, skin cancer is a very 3.2. Study Characteristics. Characteristics of the 23 included important health problem. Being deŠcient in the protective studies are shown in Table 2. �e studies were 23 case series melanin pigment and inhabiting a climate of high ambient and cross-sectional studies with the publication year ranging sunshine predisposes African albinos to the photocarcinogenic from 1953 to 2020. Most of the studies were done in Nigeria e•ect of high UV radiation. Epidemiologic studies of skin followed by Tanzania. SpeciŠcally, 10 of the studies cancer in Africans report that, compared with normally [15, 21–29] had only albino skin cancer subjects; 4 studies pigmented Africans, African albinos have higher frequency of [16, 30–32] equally had only albino subjects but reported on keratinocyte cancers, which occur at a signiŠcantly younger skin cancers and other skin diseases; 9 studies [13, 33–40] age, and they develop multiple and/or recurrent lesions which had mixed samples of albinos and nonalbinos. feature more at sun-exposed body sites [25]. �e risk of bias assessment or methodological quality Meta-analysis, originally applied in the synthesizing score for the included studies is presented in Table 3. �e results of clinical trials and determining the e•ects of study quality score ranged from 3 to 6 by the assessment tool treatment interventions, has found escalating use in deriving we used. Twenty-one studies were assessed to be of high precise estimates of disease frequency such as incidence rate quality and 2 were assessed low quality. and prevalence proportions [44]. �e present systematic review synthesized data from 3.3. Synthesis of Results. From the 23 studies, we identiŠed eligible case series and cross-sectional studies of skin cancers 540 African albinos presenting 695 histologically conŠrmed in African albinos and attempted to establish the prevalence skin cancers. �ese were composed of 274 males and 241 proportion of SCC and BCC using the methods of meta- females with sex missing in 24 cases. �ere were 419 SCC analysis. and 249 BCC among the 695 cancer lesions (Table 4). Elaborating on prevalence as a variable, Barendregt et al. By random e•ect meta-analysis, the pooled prevalence of [44] states that disease prevalence is a proportion which is SCC for the 23 studies was 64% (95CI; 50–77%). For BCC, derived by dividing the number of cases of the disease in a 4 Journal of Skin Cancer Table 2: Included studies, country of study, number of albinos, and skin cancer type. Skin cancer type Author; year Country No. of albinos with skin cancer Males Females SCC BCC CM Others Total Shapiro MP; 1953 South Africa 12 9 3 0 0 12 8 4 Datubo–Brown DD; 1991 Nigeria 3 3 0 0 0 3 0 0 Yakubu A; 1993 Nigeria 18 15 3 0 0 18 12 6 Oluwasanmi J; 1969 Nigeria 15 8 6 0 1 15 12 3 Alexander G; 1981 Tanzania 10 21 0 0 0 21 9 1 Lookingbill DP; 1995 Tanzania 10 7 3 0 1 11 5 5 Asuquo ME; 2010 Nigeria 9 5 5 1 0 11 5 4 OparaK O; 2010 Nigeria 20 32 5 0 1 38 10 10 Bangaly T; 2019 Guinea 30 40 0 0 1 41 12 18 Kiprono AS; 2014 Tanzania 86 72 61 1 0 134 41 45 Mabula JB; 2012 Tanzania 64 48 15 1 0 64 38 26 Emadi SE; 2017 Kenya 20 8 15 0 0 23 13 7 Nthumba PM; 2011 Kenya 8 0 8 0 0 8 5 3 Enechukwu AN; 2020 Nigeria 18 9 22 0 9 40 9 9 Awe OO; 2018 Nigeria 22 15 5 2 0 22 11 11 Aluko Olokun; 2015 Nigeria 35 12 16 0 7 35 17 18 Oripelaye MM; 2018 Nigeria 12 8 4 0 0 12 0 0 Asuquo ME; 2013 Nigeria 4 7 0 0 0 7 2 2 Madubuko R; 2018 Nigeria 9 8 1 0 0 9 0 0 Adegbidi H; 2007 Benin Republic 5 1 12 0 0 13 3 2 Saka B; 2020 Togo 33 21 31 0 2 54 17 16 Okafor CO; 2020 Nigeria 86 64 33 0 0 97 38 48 Chidothe IA; 2014 Malawi 7 6 1 0 0 7 6 1 SCC: squamous cell carcinoma; BCC: basal cell carcinoma; CM: cutaneous melanoma. Table 3: Risk of bias assessment score for each of the included study. A B C 1st Author; study year Aggregate score Selection Ascertainment of outcome Reporting 1 Adegbidi H; 2007 2 2 2 6 2 Alexander G; 1981 1 2 2 5 3 Aluko Olokun; 2015 1 1 2 4 4 Asuquo ME; 2013 1 2 2 5 5 Asuquo, ME; 2010 2 2 2 6 6 Awe OO; 2018 2 2 1 5 7 Bangaly T; 2019 2 2 2 6 8 Chidothe IA; 2014 1 2 2 5 9 Datubo–Brown DD; 1991 1 2 1 4 10 Emadi SE; 2017 2 2 2 6 11 Enechukwu AN; 2020 2 2 1 5 12 Kiprono AS; 2014 2 2 2 6 13 Lookingbill DP; 1995 2 2 1 5 14 Mabula JB; 2012 2 2 2 6 15 Madubuko R; 2018 2 2 2 6 16 Nthumba PM; 2011 1 2 2 5 17 Okafor CO; 2O2O 2 2 2 6 18 Oluwasanmi J, 1969 2 2 2 6 19 Opara KO; 2010 2 2 2 6 20 Oripelaye MM; 2018 1 2 2 5 21 Saka B; 2020 2 2 2 6 22 Shapiro MP, 1953 2 2 2 6 23 Yakubu A, 1993 2 2 2 6 Aggregate score: 3, 4 (low quality); 5, 6 (high quality). population by the population number. Its value always lies different cancer types. )us, the number of skin cancer between0and1,andsumovermulticategoriesamountsto1 lesions we abstracted (695) was more than the number of [44].Averynotablefeatureofskincancer inAfricanalbinos albinos with skin cancer (540). We determined the preva- is the propensity for multifocal or multiple tumours with an lence or proportion of SCC and BCC in all the histologically individual patient sometimes presenting histologically confirmed skin cancer lesions of African albinos. Journal of Skin Cancer 5 Table 4: Skin cancer type and sex of 540 African albinos with cutaneous malignancy . Variable Frequency Sex Male 275 Female 241 Missing 24 Total 540 Skin cancer type 419 Squamous cell carcinoma 419 Basal cell carcinoma 249 Cutaneous melanoma 5 ∗∗ Others 22 Total 695 ∗ ∗∗ ; Some patients presented multifocal cancers: 9 basosquamous carcinoma, 10 adenoid cystic carcinoma, 1 malignant adnexal tumour, 1 sarcoma, and 1 unspeciŠed histology. Study scc skin cancers Prevalence 95% C.I. ShapiroMP 1953 9 12 0.75 [0.46; 0.96] Datubo−BrownDD 1991 3 3 1.00 [0.50; 1.00] YakubuA 1993 15 18 0.83 [0.62; 0.98] OluwasanmiJ 1969 8 15 0.53 [0.28; 0.78] AlexanderG 1981 21 21 1.00 [0.92; 1.00] LookingbillDP 1995 7 11 0.64 [0.33; 0.90] AsuquoME 2010 5 11 0.45 [0.17; 0.76] OparaKO 2010 32 38 0.84 [0.71; 0.94] BangalyT 2019 40 41 0.98 [0.90; 1.00] KipronoAS 2014 72 134 0.54 [0.45; 0.62] MabulaJB 2012 48 64 0.75 [0.64; 0.85] EmadiSE 2017 8 23 0.35 [0.16; 0.56] NthumbaPM 2011 0 8 0.00 [0.00; 0.20] EnechukwuAN 2020 9 40 0.22 [0.11; 0.37] Awe OO 2018 15 22 0.68 [0.47; 0.86] AlukoOlokun 2015 12 35 0.34 [0.19; 0.51] OripelayeMM 2018 8 12 0.67 [0.37; 0.91] AsuquoME 2013 7 7 1.00 [0.77; 1.00] MadubukoR 2018 8 9 0.89 [0.58; 1.00] AdegbidiH 2007 1 13 0.08 [0.00; 0.30] SakaB 2020 21 54 0.39 [0.26; 0.52] OkaforCO 2020 64 97 0.66 [0.56; 0.75] ChidotheIA2014 6 7 0.86 [0.48; 1.00] 695 0.64 Random effects model [0.50; 0.77] 2 2 2 Heterogeneity: I = 89%,τ = 0.0903,χ = 194.98 (p < 0.01) Prevalence of SCC Figure 2: Forest plot showing the pooled prevalence of squamous cell carcinoma in 23 included studies. �is pooled prevalence of SCC was 64% while that of proportion of SCC among all histologically conŠrmed skin BCC was 31%, and these represents average proportion of cancer lesions in African albinos would be 60.2% (419/695) SCC and BCC in all the studies weighted by the inverse of and that of BCC, 35.8% (249/695). �ese Šgures are quite their sampling variances. Heterogeneity statistics indicate comparable to the pooled prevalence established by meta- a lack of homogeneity in the reported proportions across analyses. all the included studies. �is was not explainable by Marçon et al. [45] in Brazil suggest that the frequency of sensitivity or moderator analysis. Small sample sizes and BCC might be equal to SCC in albinos and that studies variations in study settings could be responsible. In spite reporting more SCC are hospital excision biopsies of ad- of this observed heterogeneity, the estimated prevalence vanced tumours in which SCCs are more likely to pre- Šgures appear valid. �is is because, by crude unweighted dominate, being the more aggressive of the two tumours and often requiring surgical attention. �is view seems to be pooling of the individual study proportions (analogous to the ditched “vote counting” method previously used in supported by the fact that two studies that reported more meta-analysis of clinical trials and interventions), the BCC than SCC in African albinos feature biopsies taken at 6 Journal of Skin Cancer Study bcc skin cancers Prevalence95% C.I. ShapiroMP 1953 3 12 0.25 [0.04; 0.54] Datubo−BrownDD 1991 0 3 0.00 [0.00; 0.50] YakubuA 1993 3 18 0.17 [0.02; 0.38] 0.40 [0.16; 0.66] OluwasanmiJ 1969 6 15 AlexanderG 1981 0 21 0.00 [0.00; 0.08] LookingbillDP 1995 3 11 0.27 [0.04; 0.58] 5 11 0.45 [0.17; 0.76] AsuquoME 2010 OparaKO 2010 5 38 0.13 [0.04; 0.26] BangalyT 2019 0 41 0.00 [0.00; 0.04] KipronoAS 2014 61 134 0.46 [0.37; 0.54] MabulaJB 2012 15 64 0.23 [0.14; 0.35] 23 0.65 [0.44; 0.84] EmadiSE 2017 15 NthumbaPM 2011 8 8 1.00 [0.80; 1.00] EnechukwuAN 2020 22 40 0.55 [0.39; 0.70] Awe OO 2018 5 22 0.23 [0.07; 0.43] AlukoOlokun 2015 16 35 0.46 [0.29; 0.62] [0.09; 0.63] OripelayeMM 2018 4 12 0.33 AsuquoME 2013 0 7 0.00 [0.00; 0.23] MadubukoR 2018 1 9 0.11 [0.00; 0.42] 13 0.92 [0.70; 1.00] AdegbidiH 2007 12 SakaB 2020 31 54 0.57 [0.44; 0.70] OkaforCO 2020 33 97 0.34 [0.25; 0.44] ChidotheIA2014 1 7 0.14 [0.00; 0.52] Random effects model 695 0.31 [0.19; 0.45] 2 2 2 Heterogeneity: I = 88%,τ = 0.0827,χ = 179.09 (p < 0.01) Prevalence of BCC Figure 3: Forest plot showing the pooled prevalence of basal cell carcinoma. publication bias for comparative studies are appropriate for observational studies of the type used in meta-analysis of proportions. �e studies examined in meta-analysis of proportion, being noncomparative, are not subject to con- 0.067 siderations of statistical signiŠcance and the direction of result, which are known to preferentially in®uence publi- cation of clinical trials [19, 46, 47]. Nevertheless, we assessed 0.134 for publication bias using the funnel plot. Egger’s test of funnel plot asymmetry was nonsigniŠcant, suggesting a lack of publication bias in the published studies. 0.2 Our study has some strengths and limitations. First, it is, to the best of our knowledge, the Šrst meta-analysis on skin cancer in African albinos and thus represents the 0.267 largest study of albinos with skin cancer to date. �e study was able to yield data, which bolstered the previously re- 0 0.21 0.72 1 ported epidemiologic trends of skin cancer and statistically Proportion established that the prevalence for SCC and BCC in skin Figure 4: Funnel plot of the included studies. cancer lesions. �e study is limited by the small sample sizes of the available studies and dearth of publications devoted exclusively to the subject of albino skin cancer. In routine dermatological examination and surveillance pro- grammes [16, 17]. addition, because our study is a review, we could not validate the histological types of the skin cancers reported Publication bias has been explained, chie®y, in terms of preferential publication of manuscripts with statistically by the included studies. signiŠcant results to the exclusion of those with nonsig- niŠcant results. But some other study characteristics such as 5. Conclusion funding source, research setting, and prevailing theories at the time of publication have been found to equally in®uence In conclusion, we estimated the prevalence proportion of publication [46]. Even though publication bias could con- SCC and BCC in histologically conŠrmed skin cancer lesions found systematic reviews, it has been questioned if the in African albinos. �e pooled average prevalence propor- traditional methods employed in the assessment of tion of SCC amongst all histologically conŠrmed skin cancer Standard Error Journal of Skin Cancer 7 [10] E.S.Hong,H.Zeeb,andM.H.Repacholi,“AlbinisminAfrica lesions in African albinos was 64% (95% CI; 50–77%) and as a public health issue,” BMC Public Health, vol. 6, no. 1, the prevalence of BCC was 31% (95% CI; 19–45%). Squa- mouscellcarcinomaisthepredominanttypeofkeratinocyte [11] B.A.RaaschandP.G.Buettner,“Multiplenonmelanomaskin carcinoma reported in African albinos overall. )is pre- cancer in an exposed Australian population,” International dominance of keratinocyte carcinomas in African albinos Journal of Dermatology, vol. 41, no. 10, pp. 652–658, 2002. relates more the with pattern of occurrence in pigmented [12] H. S. Chahal, K. E. Rieger, and K. Y. Sarin, “Incidence ratio of Africans rather than Caucasians. basal cell carcinoma to squamous cell carcinoma equalizes with age,” Journal of the American Academy of Dermatology, vol. 76, no. 2, pp. 353-354, 2017. Data Availability [13] O. C. Okafor and N. T. Onyishi, “Primary cutaneous ma- )e data used to support the findings of this study are in- lignancies in non-albino and albino Africans,” International Journal of Dermatology, vol. 60, no. 2, pp. 222–228, 2021. cluded within the article. [14] P. M. Nthumba, “Marjolin’s ulcers in sub-Saharan Africa,” World Journal of Surgery, vol.34,no.10,pp.2272–2277,2010. Conflicts of Interest [15] J.B.Mabula,P.L.Chalya,M.D.Mchembeetal.“Skincancers among Albinos at a University teaching hospital in North- )e authors declare that they have no conflicts of interest. western Tanzania: a retrospective review of 64 cases,” BMC Dermatology, vol. 12, no. 1, pp. 5–180, 2012. [16] N. A. Enechukwu, G. O. Ogun, O. I. Ezejiofor et al., “His- Acknowledgments topathologic patterns of cutaneous malignancies in individ- uals with oculocutaneous albinism in Anambra state, Nigeria: )e authors thank Dr. Nnamani Christian and other staff of a paradigm swing?” Ecancermedicalscience, vol. 14, p. 1013, theHistopathologyDepartmentofESUTTeachingHospital, Parklane, for their contributions to the work. [17] B. Saka, J. N. Teclessou, S. A. Akakpo et al., “A histopatho- logical study of skin lesions in individuals with oculocuta- References neous albinism in Togo in 2019,” Journal of Skin Cancer, vol. 2020, Article ID 2361957, 4 pages, 2020. [1] E. Perera, N. Gnaneswaran, C. Staines, A. K. Win, and [18] N. T. Onyishi and S. R. Ohayi, “Cutaneous melanoma in R. Sinclair, “Incidence and prevalence of non-melanoma skin African albinos: a systematic review,” Journal of Clinical and cancerinAustralia:asystematicreview,” Australasian Journal Diagnostic Research, vol. 15, no. 11, pp. WE01–WE06, 2021. of Dermatology, vol. 56, no. 4, pp. 258–267, 2015. [19] M. H. Murad, S. Sultan, S. Haffar, and F. Bazerbachi, [2] H. W. Rogers, M. A. Weinstock, S. R. Feldman, and “Methodological quality and synthesis of case series and case B. M. Coldiron, “Incidence estimate of nonmelanoma skin reports,” BMJ Evidence-Based Medicine, vol. 23, no. 2, cancer(keratinocytecarcinomas)intheUSpopulation,2012,” pp. 60–63, 2018. JAMADermatol, vol. 151, pp. 06360–11086, 2015. [20] N. Wang, How to Conduct a Meta-Analysis of Proportions in [3] P. G. Buettner and B. A. Raasch, “Incidence rates of skin R: A Comprehensive Tutorial Conducting Meta-Analyses of cancer in Townsville, Australia,” International Journal of Proportions in R, Elsevier, Amsterdam, Netherlands, 2018. Cancer, vol. 78, no. 5, pp. 587–593, 1998. [21] G. A. Alexander and U. K. Henschke, “Advanced skin cancer [4] Z.C.Venables,T.Nijsten,K.F.Wongetal.,“Epidemiologyof inTanzanianalbinos:Preliminaryobservations,” Journal of the basal and cutaneous squamous cell carcinoma in the U.K. National Medical Association, vol. 73, no. 11, pp. 1047–1054, 2013–15: a cohort study,” British Journal of Dermatology, vol. 181, no. 3, pp. 474–482, 2019. [22] M. E. Asuquo, O. O. Otei, J. Omotoso, and E. E. Bassey, [5] H. M. Gloster and K. Neal, “Skin cancer in skin of color,” “Letter: skin cancer in albinos at the university of calabar Journal of the American Academy of Dermatology, vol. 55, teaching hospital, calabar, Nigeria,” Dermatology Online no. 5, pp. 741–760, 2006. Journal, vol. 16, no. 4, p. 14, 2010. [6] O. N. Agbai, K. Buster, M. Sanchez et al., “Skin cancer and [23] K. O. Opara and B. C. Jiburum, “Skin cancers in albinos in a photoprotection in people of color: a review and recom- teaching Hospital in eastern Nigeria - presentation and mendations for physicians and the public,” Journal of the challengesofcare,” World Journal of Surgical Oncology,vol.8, American Academy of Dermatology, vol. 70, no. 4, pp. 748– no. 1, pp. 73–77, 2010. 762, 2014. [24] B. Traore, A. Barry, T. Kourouma, M. Keita, and M. Cisse, [7] G. O. Oseni, P. B. Olaitan, A. O. Komolafe, O. O. Olaofe, “Skin cancers in albinos at surgical oncology unit of donka H. A. M. Akinyemi, and O. A. Suleiman, “Malignant skin nationalhospital(conakry),” Cancer Studies and 2erapeutics, lesions in Oshogbo, Nigeria,” 2e Pan African medical vol. 4, no. 1, pp. 1–5, 2019. journal, vol. 20, pp. 253–256, 2015. [25] S. K. Kiprono, B. M. Chaula, and H. Beltraminelli, “Histo- [8] O. Ochicha, S. T. Edino, A. Z. Mohammed, and A. B. Umar, logical review of skin cancers in African Albinos: a 10-year “Dermatological malignancies in Kano Northern Nigeria: a retrospectivereview,” BMC Cancer,vol.14,no.1,pp.157–164, histopathological review,” Annals of African Medicine, vol. 3, no. 4, pp. 188–191, 2004. [26] O. O. Awe and T. A. Azeke, “Cutaneous cancers in Nigerian [9] P. L. Chalya, J. M. Gilyoma, E. S. Kanumba et al., “Derma- albinos: a review of 22 cases,” Nigerian Journal of Surgery, tological malignancies at a University Teaching Hospital in north-western Tanzania: a retrospective review of 154 cases,” vol. 24, no. 1, pp. 34–38, 2018. [27] M. E. Asuquo, O. O. Otei, I. Bassey, and G. Ebughe, “Ocu- Tanzania Journal of Health Research, vol. 14, no. 1, pp. 9–14, 2012. locutaneous albinism and skin cancer in Calabar,” 8 Journal of Skin Cancer International Journal of Medicine and Medical Sciences,vol.5, [45] C. R. Marçon, J. C. Moraes, M. A. M. de Olivas Ferreira, and C. B. Oliari, “Dermatological and epidemiological profiles of no. 1, pp. 3–5, 2013. [28] B. Saka, S. A. Akakpo, J. N. Teclessou et al., “Skin cancers in patients with albinism in são paulo, Brazil, between 2010 and 2017: a cross-sectional study,” Dermatology, vol. 236, no. 3, peoplewithalbinism inTogoin2019:resultsoftworoundsof national mobile skin care clinics (in review),” BMC Derma- pp. 219–227, 2020. [46] K. M. Coburn and J. L. Vevea, “Publication bias as a function tology, vol. 26, pp. 1–8, 2019. [29] I. A. Chidothe and L. Masamba, “Neoadjuvant chemotherapy of study characteristics,” Psychological Methods, vol. 20, no. 3, pp. 310–330, 2015. in albinos with locally advanced skin cancer at a blantyre [47] P. K. Maulik, M. N. Mascarenhas, C. D. Mathers, T. Dua, and hospital: case series,” Malawi Medical Journal, vol. 26, no. 3, S. Saxena, “Prevalence of intellectual disability: a meta- pp. 97–99, 2014. analysis of population-based studies,” Research in Develop- [30] D. P. Lookingbill, G. L. Lookingbill, and B. Leppard, “Actinic mental Disabilities, vol. 32, no. 2, pp. 419–436, 2011. damage and skin cancer in albinos in northern Tanzania: findings in 164 patients enrolled in an outreach skin care program,” Journal of the American Academy of Dermatology, vol. 32, no. 4, pp. 653–658, 1995. [31] S. E. Emadi, A. J. Suleh, F. Babamahmoodi et al., “Common malignant cutaneous conditions among albinos in Kenya,” Medical Journal of the Islamic Republic of Iran, vol. 31, no. 1, pp. 7–12, 2017. [32] M. C. Roli and O. Abel, “Photodermatoses in the Nigerian albino: a study in an urban hospital in southern Nigeria,” Journal of Medicine in the Tropics, vol. 20, no. 1, pp. 68–73, [33] M. P. Shapiro, P. Keen, L. Cohen, and J. F. Murray, “Skin cancer in the South African Bantu,” British Journal of Cancer, vol. 7, no. 1, pp. 45–57, 1953. [34] D. D. Datubo-Brown, “Primary malignant skin tumor in Nigerians,” Journal of the National Medical Association, vol. 83, pp. 345–348, 1991. [35] A. Yakubu and O. A. Mabogunje, “Skin cancer in African albinos,” Acta Oncologica, vol. 32, no. 6, pp. 621-622, 1993. [36] J. O. Oluwasanmi, A. O. Williams, and A. F. Alli, “Superficial cancer in Nigeria,” British Journal of Cancer, vol. 23, no. 4, pp. 714–728, 1969. [37] P. M. Nthumba, P. C. Cavadas, and L. Landin, “Primary cutaneous malignancies in sub-Saharan Africa,” Annals of Plastic Surgery, vol. 66, no. 3, pp. 313–320, 2011. [38] B. Aluko-Olokun and A. A. Olaitan, “Skin cancer risk factor reductioninAfrica:assessmentofuseofantiretroviraltherapy services by human immunodeficiency virus positive albinos,” HIV & AIDS Review, vol. 14, no. 1, pp. 18–21, 2015. [39] M. M. Oripelaye, A. O. Oladele, F. O. Olanrewaju, and O.O.Olaofe,“)eevolvingpatternofprimaryskincancersin ile-ife, Nigeria,” Serbian Journal of Dermatology and Vene- reology, vol. 10, no. 3, pp. 90–95, 2018. [40] H. Adegbidi, H. Yedomon, F. Atadokpede, M.-C. Balley- Pognon, and F. Do Ango-Padonou, “Skin cancers at the national university hospital of cotonou from 1985 to 2004,” International Journal of Dermatology, vol. 46, no. s1, pp. 26–29, 2007. [41] J. G. R. Kromberg, J. Bothwell, S. H. Kidson, P. Manga, R. Kerr, and T. Jenkins, “Types of albinism in the black southern Africa population,” East African Medical Journal, vol. 89, no. 1, pp. 20–27, 2012. [42] J.Taylor,C.Bradbury-Jones,andP.Lund,“Witchcraft-related Abuse and murder of children with albinism in sub-saharan Africa: a conceptual review,” Child Abuse Review, vol. 28, no. 1, pp. 13–26, 2019. [43] M. H. Brilliant, “Albinism in Africa: a medical and social emergency,” International Health, vol. 7, no. 4, pp. 223–225, [44] J.J.Barendregt,S.A.Doi,Y.Y.Lee,R.E.Norman,andT.Vos, “Meta-analysis of prevalence,” Journal of Epidemiology & Community Health, vol. 67, no. 11, pp. 974–978, 2013.

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Journal of Skin CancerHindawi Publishing Corporation

Published: Aug 30, 2022

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