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Histopathological Characteristics of Cutaneous Melanoma in Isfahan, Iran, from 2013 to 2018

Histopathological Characteristics of Cutaneous Melanoma in Isfahan, Iran, from 2013 to 2018 Hindawi Journal of Skin Cancer Volume 2022, Article ID 4490648, 6 pages https://doi.org/10.1155/2022/4490648 Research Article Histopathological Characteristics of Cutaneous Melanoma in Isfahan, Iran, from 2013 to 2018 1 2 3 4 Zahra Malakoutikhah , Fatemeh Mohaghegh , Siavash Karimi , Parvin Rajabi , and Elham T. Tabatabaei Applied Physiology Research Center, Cardiovascular Research Institute, Isfahan University of Medical Sciences, Isfahan, Iran Department of Dermatology, Skin Diseases and Leishmaniasis Research Center, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran Department of Pathology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran Correspondence should be addressed to Fatemeh Mohaghegh; f.mohaghegh@med.mui.ac.ir Received 13 July 2022; Accepted 2 September 2022; Published 19 September 2022 Academic Editor: Nihal Ahmad Copyright © 2022 Zahra Malakoutikhah 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. Objectives. To investigate the histopathological characteristics of cutaneous melanoma in Isfahan from 2013 to 2018, according to histopathological subtype, lesions location, Clark level, and Breslow thickness. Methods. A descriptive, retrospective study in reports of Alzahra Hospital and Dr. Rajabi Pathology Laboratory in Isfahan. Results. In total, 45 patients were included in this study. �e most prevalent histopathological subtype was acral lentiginous melanoma (48.89%), followed by lentigo maligna melanoma (17.78%), nodular melanoma (11.11%), and super—cial spreading melanoma (8.89%). Most malignant lesions were on the foot and toes (31.1%) and face (24.4%). Tumor invasion level was mainly at Clark level IV (42.2%). Furthermore, the mean depth of tumor penetration (Breslow thickness) was 3.87 ± 3.35. Conclusions. Our study revealed the characteristics of melanoma in the Iranian population. Our results showed a similar trend with previous studies in the Asian population. Further investigations are needed to elucidate the role of ethnic and environmental risk factors for developing melanoma in dišerent populations. CM is a multifactorial disease, having a heterogeneous 1. Introduction presentation. �e goal of current strategies is to reduce the Although cutaneous melanoma accounts for a small pro- disease burden by improving the understanding of the causal portion of all skin cancers diagnosed each year, it is one of factors and their relationships [2]. the most malignant forms of skin cancer, representing up to Cutaneous melanoma varies signi—cantly in genomic 80% of all deaths from skin cancers. Cutaneous melanoma pro—le, clinical manifestations, incidence, and mortality (CM) is also one of the few cancers that are on the rise depending on ethnicity, country of residence, degree of sun globally. It is estimated that melanoma incidence has doubled exposure, and socioeconomic status. �us, the characteris- in the last 20 years, becoming a signi—cant health concern tics of cutaneous melanoma show apparent dišerences worldwide [1]. among various countries and nationalities [3]. Moreover, the development of dišerent subtypes of melanoma is not CM originates from genetically altered and activated melanocytes in the basal epidermis that are producing explained by a single evolutionary pathway. melanin, the material that protects us against radiation Melanoma’s clinical presentation and dermatoscopic exposure and DNA alteration. features depend on the histopathological type of cancer and 2 Journal of Skin Cancer the anatomic location of lesions [4]. )ere are four major types of cutaneous melanoma, including superficial spreading melanoma (SSM), nodular melanoma (NM), Male lentigo maligna melanoma (LMM), and acral lentiginous Female 44% 56% melanoma (ALM). Superficial spreading melanoma is the most common histologic subtype in Caucasian populations. )is subtype is the most likely to be related to a pre-existing nevus. Furthermore, SSM can appear in any anatomic site, but it is more prevalent in men’s back and women’s lower extremities [5]. Nodular melanoma is the second most prevalent subtype, which frequently presents a uniform color or amelanotic hue, symmetric borders, and relatively Female small diameters. )ese benignant features make timely di- Male agnosis difficult, and most NMs are thicker than 2 mm at the Figure 1: Distribution of cutaneous melanoma according to time of diagnosis [6]. Lentigo maligna melanoma is the most gender. prevalent subtype of melanoma on the face, which often occurs in chronically sun-damaged skin of the face and neck of elderly individuals. )is subtype’s precursor is lentigo invasion were determined for each sample and specified in a maligna (LM) or LMM in situ, which grows slowly for years relevant table. Demographic data, including the patient’s and eventually progresses to LMM [7]. Although acral age, gender, and address, were also registered. lentiginous melanoma is the least prevalent subtype among All data were uploaded in SPSS Ver 16 software. Sta- the Caucasian population, it is the most prevalent subtype in tistical analysis was performed using the independent t-test the Asian and dark-skinned population. )is subtype is also and chi-square test (Fisher’s exact test) for categorical values found in glabrous skin, mainly palms, soles, and subungual comparison (P-value <0.05). areas [8]. Dermatoscopical characteristics of melanomas can in- dicate their melanocytic origin, including aggregated brown 3. Results or black globules, pigment networks, and location-related feathers. However, a melanoma may have no clinically and Forty-five patients with a confirmed diagnosis of CM were dermatoscopically specific and well-defined features. Indeed found, of which 44.4% (20 cases) were male, and 55.6% (25 there is no exclusive or typical clinical presentation of cases) were female with a male to female ratio of 0.8 :1 melanoma. Hence, diagnosis of CM continues to be com- [Figure 1]. plicated and challenging for specialists. )e mean age of all patients was 63.31 ± 15.38, with a )e present study aimed to evaluate patients’ histo- range of 32 to 92 years. )e age variable follows the normal pathological features with cutaneous melanoma attending a distribution. )e oldest group was nodular melanoma pa- referral hospital in Isfahan from 2013 to 2018. Hopefully, tients [Table 1]. these findings will help physicians to diagnose melanoma in According to the frequency of different histopathologic this area in a more timely and accurate manner. types, the most common type seen in our study was ALM (48.89%), followed by LLM type (17.78%). Moreover, his- topathologic types’ frequency had no significant differences 2. Materials and Methods between men and women (P � 0.97) and between different It was a retrospective, descriptive study of histopathological age groups (P � 0.86) [Figure 2]. types of CM in Isfahan, from 2013 to 2018, from the records )e mean depth of tumor penetration (Breslow thick- of Alzahra Hospital and Dr. Rajabi Pathology Laboratory. ness) was 3.87± 3.35 mm with a range of 0.8–15 mm in the Slides with a report of cutaneous melanoma were ob- present study. )e tumor penetration depth does not follow tained and re-evaluated by a dermatopathologist. Eligible the normal distribution [Table 2]. samples were those that had the patient’s data and the )e highest rate of tumor invasion was to the reticular patient’s pathology sheet. Moreover, the histopathology dermis (Clark IV) and then to the fat layer (Clark V), 42.2% and 22.2%, respectively [Table 2]. )e most common tumor type, Breslow, and Clark must be visible in the studied slides. If, according to the examining dermatopathologist opinion, lesion site was the foot and toes (31.1%), followed by the face (24.4%). )e lesion site’s frequency distribution based on the diagnosis of CM was not definitive, the sample would be excluded from the study. If the anonymous review was age, sex, and Breslow thickness is summarized in Table 3. disagreed with the original report, a secondary anonymous Vascular invasion was seen in eight patients (17.8%), of review by another dermatopathologist was considered as a which 62.5% were seen in ALM type. Furthermore, 19 diagnostic criterion. patients (42.2%) had ulcers. )e highest ulcer rate was in the All samples were reviewed anonymously, without the ALM type (52.63%) and then in NM and LMM types dermatopathologist knowing the first diagnosis of each slide. (15.78%). )e frequency distribution of vascular invasion Histopathological type of cutaneous melanoma, Clark’s and ulceration in the samples based on the depth of tumor invasion level, Breslow thickness, ulcer status, and vascular penetration and the lesion’s location is shown in Table 4. Journal of Skin Cancer 3 Table 1: )e frequency distribution of multiple variables based on histopathologic subtypes of cutaneous melanoma. Histopathologic types of cutaneous melanoma ALM LMM NM SSM Others Number 22 8 5 4 6 Percent 48.89 17.78 11.11 8.89 13.33 Gender (%) Male 10 (45.5) 4 (50) 2 (40) 2 (50) 2 (33.3) Female 12 (54.5) 4 (50) 3 (60) 2 (50) 4 (66.7) Mean age± SD 62.00± 15.25 69.13± 15.18 70.20± 15.02 60.25± 8.88 56.67± 19.61 Clark’s invasion level (%) Level I 1 (4.5) 1 (12.5) — 1 (25.0) — Level II 4 (18.2) 2 (25.0) — 2 (50.0) — Level III 2 (9.1) 1 (12.5) — 1 (25.0) 1 (16.7) Level IV 12 (54.5) 3 (37.5) 3 (60.0) — 1 (16.7) Level V 3 (13.6) 1 (12.5) 2 (40.0) — 4 (66.7) Depth of tumor penetration (Breslow thickness) (%) <1.00 5 (22.7) 3 (37.5) — 3 (75.0) — 1.00–2.00 3 (13.6) 2 (25.0) — 1 (25.0) 1 (16.7) 2.01–4.00 10 (45.5) 1 (12.5) — — — >4.00 4 (18.2) 2 (25.0) 5 (100) — 5 (83.3) Mean± SD 3.11± 2.16 2.48± 2.15 7.90± 4.56 1.10± 0.60 7.03± 3.99 Tumor location (%) Face — 7 (87.5) 2 (40.0) — 2 (33.3) Scalp — 1 (12.5) — — — Trunk — — 1 (20.0) 2 (50.0) 1 (16.7) Arm — — — 2 (50.0) 1 (16.7) Hand 7 (31.8) — — — — Anus — — 1 (20.0) — — Leg 1 (4.5) — 1 (20.0) — 2 (33.3) Foot 14 (63.6) — — — — Moreover, the mean age in men was 65.55± 16.29, and in women was 61.52± 14.70, which was not statistically significant (P � 0.38). show the same trend as previous studies. Notably, the most Others prevalent histopathological subtype was ALM (48.89%), SSM 13% followed by LMM (17.78%), NM (11.11%), and SSM (8.89%) 9% ALM [Figure 2]. As previous studies conducted in Iran’s different NM 49% cities showed, the most common histopathological subtype 11% in our study was ALM. )e prevalence of the ALM subtype LMM in the Kamyab et al.’s study [9] in Tehran was 30%, and in the 18% Handjani et al.’s study [10] in southern Iran was 44.8%. )ese results are consistent with other research studies conducted in the Asian and dark-skinned populations [11, 12]. According to the SEER database, ALM was predominant ALM SSM LMM Others among African–Americans, while the most common histo- NM pathologic subtype in other racial and ethnic groups in the United States was SSM [12, 13]. A large-scale study conducted Figure 2: Distribution of cutaneous melanoma according to his- in the Japanese population reported ALM as the most topathological subtype. prevalent subtype (40.4%). In contrast, the proportion of this subtype in non-Hispanic whites was only 1.5% [14]. Based on these and other valid studies, we can conclude that the ALM is 4. Discussion the most prevalent histopathological subtype in Asian and )e increasing prevalence of cutaneous malignant mela- dark-skinned populations. )us, geographical and racial noma in recent years has attracted the attention of many variations in melanoma’s clinical manifestations have been researchers. Our study revealed the histopathological confirmed. )e high prevalence of ALM might be a significant characteristics of melanoma in patients referred to Alzahra cause of the high mortality rate among these races despite the Hospital and Dr. Rajabi Pathology Laboratory in Isfahan, low incidence rate [3, 15]. According to the SEER study, from 2013 to 2018. Our melanoma patients’ mean age was African–Americans had significantly shorter melanoma- 63.31± 15.38, with a range of 32–92 years. )ese findings specific survival than Caucasians. In African–Americans 4 Journal of Skin Cancer Table 2: Frequency distribution of Breslow thickness and tumor invasion level. Variable Number Percent Depth of tumor penetration (Breslow thickness) <1.00 11 24.4 1.00–2.00 7 15.6 2.01–4.00 11 24.4 >4.00 16 35.6 Total 45 100 Clark’s invasion level Level I: limited to the epidermis 3 6.7 Level II: invasion of the papillary dermis 8 17.8 Level III: filling the papillary dermis to connect the reticular dermis 5 11.1 Level IV: invasion of the reticular dermis 19 42.2 Level V: fat invasion 10 22.2 Total 45 100 Table 3: )e frequency distribution of lesion site based on sex, age, and Breslow thickness. Gender (%) Tumor location Number Percent Mean age± SD Breslow’s thickness Male Female Face 11 24.4 6 (30.0) 5 (20.0) 69.55± 16.80 3.35± 2.47 Scalp 1 2.2 — 1 (4.0) 76.00 6.00 Trunk 4 8.9 3 (15.0) 1 (4.0) 63.50± 7.32 6.15± 6.29 Arm 3 6.7 — 3 (12.0) 59.67± 6.65 3.93± 4.42 Hand 7 15.6 — 7 (28.0) 59.57± 13.37 3.10± 1.27 Anus 1 2.2 — 1 (4.0) 73.00 15.00 Leg 4 8.9 2 (10.0) 2 (8.0) 51.25± 19.36 4.17± 2.07 Foot 14 31.1 9 (45.0) 5 (20.0) 62.86± 16.94 2.98± 2.54 Total 45 100 20 (100) 25 (100) Table 4: )e frequency distribution of vascular invasion and ulceration in the samples based on the lesion’s location and depth of tumor penetration. Vascular invasion (%) Ulceration (%) Variable Yes No Yes No )e whole sample 8 (17.8) 37 (82.2) 19 (42.2) 26 (57.8) Tumor location Face 1 (12.5) 10 (27.0) 6 (31.6) 5 (19.2) Scalp — 1 (2.7) — 1 (3.8) Trunk 1 (12.5) 3 (8.1) 1 (5.3) 3 (11.5) Arm 1 (12.5) 2 (5.4) 1 (5.3) 2 (7.7) Hand 1 (12.5) 6 (16.2) 5 (26.3) 2 (7.7) Anus — 1 (2.7) 1 (5.3) — Leg 1 (12.5) 3 (8.1) 1 (5.3) 3 (11.5) Foot 3 (37.5) 11 (29.7) 4 (21.1) 10 (38.5) Total 8 (100) 37 (100) 19 (100) 26 (100) Depth of tumor penetration (Breslow thickness) <1.00 — 11 (29.7) 1 (5.3) 10 (38.5) 1.00–2.00 — 7 (18.9) 3 (15.8) 4 (15.4) 2.01–4.00 1 (12.5) 10 (27.0) 6 (31.6) 5 (19.2) >4.00 7 (87.5) 9 (24.3) 9 (47.4) 7 (26.9) Total 8 (100) 37 (100) 19 (100) 26 (100) Mean± SD 7.12± 3.18 3.17± 2.98 5.08± 3.51 2.99± 2.98 melanoma patients with NM or ALM subtype, melanoma- In several other studies, the survival of the ALM subtype specific mortality was statically higher, while 5-year survival has also been compared with other subtypes. According to a was statically lower. Interestingly, African–Americans ex- study conducted by Ishihara et al., the survival of ALM was perienced higher melanoma-specific mortality and lower significantly lower than SSM in the Japanese population. survival for NM and ALM than Caucasians [12]. Fujisawa et al. reported no association between ALM and Journal of Skin Cancer 5 12 14 0 0 ALM LMM NM SSM Others ALM LMM NM SSM Others <1.00 2.01 - 4.00 Clark I Clark IV 1.00 - 2.00 >4.00 Clark II Clark V Clark III Figure 3: Breslow thickness in different types of melanoma. Figure 4: Clark’s invasion level in different types of melanoma. survival across the whole study. However, they found a significant survival disadvantage in the ALM stage IIIA. It ALM occurs are less likely to be noticed. So we diagnose this can be understood that ALM worsens the prognosis of subtype late, in advanced stages, with high penetration depth melanoma in the early stages of lymphatic spread, and this and high rate of ulceration. In Lee et al.’s study, the mean type may need to be evaluated for the indication of addi- duration of melanoma diagnosis in all groups was 20 tional treatments such as SLNB and adjuvant therapy months, ranging from 1 to 120 months. In contrast, the [14, 16]. mean duration of diagnosing ALM and non-ALM was ALM has also been reported as an independent negative 27± 33 and 12± 14 months, respectively. Notably, when this predictor of melanoma-specific survival in different studies variable was stratified against ethnicity, the delay was re- [12, 16, 17]. An extensive nationwide study in the Nether- ported to be 22± 28 months in Asians and 7± 5 months for lands showed that NM and ALM subtypes had lower survival Caucasians (P � 0.09) [15]. than SSM and LMM. In Gumaste et al.’s study, the hazard However, in various studies, the ALM subtype’s survival ratio of survival for ALMs vs. non-ALMs was 2.64 rate remained lower than other subtypes, even after con- (P � 0.001). Moreover, the ALM subtype’s recurrence rate trolling melanoma stages. Evidence exists to show that in- was statically more than the others (49% vs. 30%, p � 0.007), herent biologic differences in melanoma subtypes may also particularly in tumors with less than 2 mm penetration play an essential role in the prognosis and even therapeutic depth. )ese pieces of evidence suggest that ALM is a tough strategy of cutaneous melanoma. Patients with ALM have variant of melanoma and may require unique and more been shown to demonstrate specific genetic aberrations, invasive treatments [16, 17]. indicating that the potency of invasion and ALM progres- Various possible explanations have been put forward for sion may be biologically distinct from other types of cuta- these pieces of evidence. Patients with ALM often have neous melanoma [18]. Moreover, in contrast to Caucasians, deeper, more advanced stages, and a higher rate of ulceration the lower incidence rate and less awareness about melanoma at the time of diagnosis. Tumor thickness and ulceration in dark-skinned and Asian populations lead to a delay in have been reported as the most influential independent diagnosis and advanced stages at the presentation. Socio- predictors of survival for melanoma [13, 18]. In our study, economic status is also an important prognostic factor most ALM cases (45.5%) had Breslow thicknesses of 2.1 to among these groups. )is evidence highlights the impor- 4 mm [Figure 3, Table 1], and 54.5% were diagnosed at Clark tance of raising awareness about melanoma for all racial and invasion level IV [Figure 4, Table 1]. ethnic groups, particularly Asians [12]. )e most common Breslow thickness across the entire Our study’s primary limitation to the generalization of study was more than 4 mm (35.6%), and 42.2% of melanoma these results is the small sample size. However, our results patients were diagnosed at Clark invasion level IV [Table 2]. showed the same trend as other studies. According to Lee et al.’s study, the mean Breslow thickness in ALM subtypes was 2.5± 2.3 mm, while this amount in 5. Conclusion non-ALM subtypes was only 1.7± 2.0 mm (P � 0.30). )e highest rate of ulceration in the current study was also seen Our study showed that the ALM is the most prevalent in the ALM subtype (52.62%) [15]. melanoma subtype among the Iranian population. Our )e anatomic location and atypical presentation of ALM findings regarding the histopathology subtype, anatomic may also contribute to the poorer prognosis of ALM. In our location, tumor thickness, and Clark invasion level were also study, the most common tumor sites were foot and toes in agreement with other studies conducted in the Asian (31.1%) [Table 3]. In fact, the most common areas where population. 6 Journal of Skin Cancer United States, 1999–2006,” Journal of the American Academy Data Availability of Dermatology, vol. 65, no. 5, pp. S26.e1–S26.e13, 2011. [14] Y. Fujisawa, S. Yoshikawa, A. Minagawa et al., “Clinical and All data that support the findings of this study and the histopathological characteristics and survival analysis of 4594 patient’s consent are openly available from Dr. Fatemeh Japanese patients with melanoma,” Cancer Medicine, vol. 8, Mohaghegh, the corresponding author. no. 5, pp. 2146–2156, 2019. [15] H. Y. Lee, W. Y. Chay, M. B. Tang, M. T. Chio, and S. H. Tan, “Melanoma: differences between Asian and Caucasian pa- Consent tients,” Annals Academy of Medicine Singapore, vol. 41, no. 1, Written informed consent was obtained from the patients pp. 17–20, 2012. for the publication of this study. [16] M. A. El Sharouni, P. J. Van Diest, A. J. Witkamp, V. Sigurdsson, and C. H. Van Gils, “Subtyping cutaneous melanoma matters,” JNCI Cancer Spectrum, vol. 4, no. 6, Conflicts of Interest Article ID pkaa097, 2020. [17] P. V. Gumaste, N. H. Fleming, I. Silva et al., “Analysis of )e authors declare that they have no conflicts of interest recurrence patterns in acral versus nonacral melanoma: regarding the publication of this paper. should histologic subtype influence treatment guidelines?” Journal of the National Comprehensive Cancer Network, vol. 12, no. 12, pp. 1706–1712, 2014. References [18] P. Basurto-Lozada, C. Molina-Aguilar, C. Castaneda-Garcia et al., “Acral lentiginous melanoma: basic facts, biological [1] M. Lens, “Current clinical overview of cutaneous melanoma,” characteristics and research perspectives of an understudied British Journal of Nursing, vol. 17, no. 5, pp. 300–305, 2008. disease,” Pigment cell & melanoma research, vol. 34, no. 1, [2] G. C. Leonardi, L. Falzone, R. Salemi et al., “Cutaneous pp. 59–71, 2021. melanoma: from pathogenesis to therapy,” International Journal of Oncology, vol. 52, no. 4, pp. 1071–1080, 2018. [3] Y. Wang, Y. Zhao, and S. Ma, “Racial differences in six major subtypes of melanoma: descriptive epidemiology,” BMC Cancer, vol. 16, no. 1, pp. 691–699, 2016. [4] F. Dimitriou, R. Krattinger, E. Ramelyte et al., “)e world of melanoma: epidemiologic, genetic, and anatomic differences of melanoma across the globe,” Current Oncology Reports, vol. 20, no. 11, pp. 87–89, 2018. [5] F. M. Trindade, M. L. P. de Freitas, and F. V. Bittencourt, “Dermoscopic evaluation of superficial spreading melanoma,” Anais Brasileiros de Dermatologia, vol. 96, no. 2, pp. 139–147, 2021 Feb 1. [6] S. W. Menzies, F. J. Moloney, K. Byth et al., “Dermoscopic evaluation of nodular melanoma,” JAMA Dermatology, vol. 149, no. 6, pp. 699–709, 2013. [7] P. Pralong, E. Bathelier, S. Dalle, N. Poulalhon, S. Debarbieux, and L. )omas, “Dermoscopy of lentigo maligna melanoma: report of 125 cases,” British Journal of Dermatology, vol. 167, no. 2, pp. 280–287, 2012. [8] J. S. Goydos and S. L. Shoen, “Acral lentiginous melanoma,” Cancer Treatment and Research, vol. 167, pp. 321–329, 2016. [9] K. Kamyab, S. Kazemi, P. Azimi et al., “Characteristic features of cutaneous melanoma in a dermatology referral centre in Tehran, Iran,” Australasian Journal of Dermatology, vol. 58, no. 4, pp. e228–31, 2017. [10] F. Handjani, N. Saki, A. Parhizgar et al., “Epidemiology of malignant melanoma over a thirty-two year period (1981–2013) in southern Iran,” Middle East Journal of Cancer, vol. 7, no. 4, pp. 199–202, 2016. [11] J. H. Mun, J. Ohn, W. I. Kim, S. M. Park, and M. B. Kim, “Dermoscopy of melanomas on the trunk and extremities in Asians,” PLoS One, vol. 11, no. 7, Article ID e0158374, 2016. [12] K. Mahendraraj, K. Sidhu, C. S. Lau, G. J. McRoy, R. S. Chamberlain, and F. O. 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Histopathological Characteristics of Cutaneous Melanoma in Isfahan, Iran, from 2013 to 2018

Histopathological Characteristics of Cutaneous Melanoma in Isfahan, Iran, from 2013 to 2018

Abstract

<i>Objectives</i>. To investigate the histopathological characteristics of cutaneous melanoma in Isfahan from 2013 to 2018, according to histopathological subtype, lesions location, Clark level, and Breslow thickness. <i>Methods</i>. A descriptive, retrospective study in reports of Alzahra Hospital and Dr. Rajabi Pathology Laboratory in Isfahan. <i>Results</i>. In total, 45 patients were included in this study. The most prevalent histopathological subtype was acral lentiginous melanoma (48.89&#x0025;), followed by lentigo maligna melanoma (17.78&#x0025;), nodular melanoma (11.11&#x0025;), and superficial spreading melanoma (8.89&#x0025;). Most malignant lesions were on the foot and toes (31.1&#x0025;) and face (24.4&#x0025;). Tumor invasion level was mainly at Clark level IV (42.2&#x0025;). Furthermore, the mean depth of tumor penetration (Breslow thickness) was 3.87&#x2009;&#xb1;&#x2009;3.35. <i>Conclusions</i>. Our study revealed the characteristics of melanoma in the Iranian population. Our results showed a similar trend with previous studies in the Asian population. Further investigations are needed to elucidate the role of ethnic and environmental risk factors for developing melanoma in different populations.

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Hindawi Publishing Corporation
ISSN
2090-2905
eISSN
2090-2913
DOI
10.1155/2022/4490648
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Abstract

Hindawi Journal of Skin Cancer Volume 2022, Article ID 4490648, 6 pages https://doi.org/10.1155/2022/4490648 Research Article Histopathological Characteristics of Cutaneous Melanoma in Isfahan, Iran, from 2013 to 2018 1 2 3 4 Zahra Malakoutikhah , Fatemeh Mohaghegh , Siavash Karimi , Parvin Rajabi , and Elham T. Tabatabaei Applied Physiology Research Center, Cardiovascular Research Institute, Isfahan University of Medical Sciences, Isfahan, Iran Department of Dermatology, Skin Diseases and Leishmaniasis Research Center, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran Department of Pathology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran Correspondence should be addressed to Fatemeh Mohaghegh; f.mohaghegh@med.mui.ac.ir Received 13 July 2022; Accepted 2 September 2022; Published 19 September 2022 Academic Editor: Nihal Ahmad Copyright © 2022 Zahra Malakoutikhah 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. Objectives. To investigate the histopathological characteristics of cutaneous melanoma in Isfahan from 2013 to 2018, according to histopathological subtype, lesions location, Clark level, and Breslow thickness. Methods. A descriptive, retrospective study in reports of Alzahra Hospital and Dr. Rajabi Pathology Laboratory in Isfahan. Results. In total, 45 patients were included in this study. �e most prevalent histopathological subtype was acral lentiginous melanoma (48.89%), followed by lentigo maligna melanoma (17.78%), nodular melanoma (11.11%), and super—cial spreading melanoma (8.89%). Most malignant lesions were on the foot and toes (31.1%) and face (24.4%). Tumor invasion level was mainly at Clark level IV (42.2%). Furthermore, the mean depth of tumor penetration (Breslow thickness) was 3.87 ± 3.35. Conclusions. Our study revealed the characteristics of melanoma in the Iranian population. Our results showed a similar trend with previous studies in the Asian population. Further investigations are needed to elucidate the role of ethnic and environmental risk factors for developing melanoma in dišerent populations. CM is a multifactorial disease, having a heterogeneous 1. Introduction presentation. �e goal of current strategies is to reduce the Although cutaneous melanoma accounts for a small pro- disease burden by improving the understanding of the causal portion of all skin cancers diagnosed each year, it is one of factors and their relationships [2]. the most malignant forms of skin cancer, representing up to Cutaneous melanoma varies signi—cantly in genomic 80% of all deaths from skin cancers. Cutaneous melanoma pro—le, clinical manifestations, incidence, and mortality (CM) is also one of the few cancers that are on the rise depending on ethnicity, country of residence, degree of sun globally. It is estimated that melanoma incidence has doubled exposure, and socioeconomic status. �us, the characteris- in the last 20 years, becoming a signi—cant health concern tics of cutaneous melanoma show apparent dišerences worldwide [1]. among various countries and nationalities [3]. Moreover, the development of dišerent subtypes of melanoma is not CM originates from genetically altered and activated melanocytes in the basal epidermis that are producing explained by a single evolutionary pathway. melanin, the material that protects us against radiation Melanoma’s clinical presentation and dermatoscopic exposure and DNA alteration. features depend on the histopathological type of cancer and 2 Journal of Skin Cancer the anatomic location of lesions [4]. )ere are four major types of cutaneous melanoma, including superficial spreading melanoma (SSM), nodular melanoma (NM), Male lentigo maligna melanoma (LMM), and acral lentiginous Female 44% 56% melanoma (ALM). Superficial spreading melanoma is the most common histologic subtype in Caucasian populations. )is subtype is the most likely to be related to a pre-existing nevus. Furthermore, SSM can appear in any anatomic site, but it is more prevalent in men’s back and women’s lower extremities [5]. Nodular melanoma is the second most prevalent subtype, which frequently presents a uniform color or amelanotic hue, symmetric borders, and relatively Female small diameters. )ese benignant features make timely di- Male agnosis difficult, and most NMs are thicker than 2 mm at the Figure 1: Distribution of cutaneous melanoma according to time of diagnosis [6]. Lentigo maligna melanoma is the most gender. prevalent subtype of melanoma on the face, which often occurs in chronically sun-damaged skin of the face and neck of elderly individuals. )is subtype’s precursor is lentigo invasion were determined for each sample and specified in a maligna (LM) or LMM in situ, which grows slowly for years relevant table. Demographic data, including the patient’s and eventually progresses to LMM [7]. Although acral age, gender, and address, were also registered. lentiginous melanoma is the least prevalent subtype among All data were uploaded in SPSS Ver 16 software. Sta- the Caucasian population, it is the most prevalent subtype in tistical analysis was performed using the independent t-test the Asian and dark-skinned population. )is subtype is also and chi-square test (Fisher’s exact test) for categorical values found in glabrous skin, mainly palms, soles, and subungual comparison (P-value <0.05). areas [8]. Dermatoscopical characteristics of melanomas can in- dicate their melanocytic origin, including aggregated brown 3. Results or black globules, pigment networks, and location-related feathers. However, a melanoma may have no clinically and Forty-five patients with a confirmed diagnosis of CM were dermatoscopically specific and well-defined features. Indeed found, of which 44.4% (20 cases) were male, and 55.6% (25 there is no exclusive or typical clinical presentation of cases) were female with a male to female ratio of 0.8 :1 melanoma. Hence, diagnosis of CM continues to be com- [Figure 1]. plicated and challenging for specialists. )e mean age of all patients was 63.31 ± 15.38, with a )e present study aimed to evaluate patients’ histo- range of 32 to 92 years. )e age variable follows the normal pathological features with cutaneous melanoma attending a distribution. )e oldest group was nodular melanoma pa- referral hospital in Isfahan from 2013 to 2018. Hopefully, tients [Table 1]. these findings will help physicians to diagnose melanoma in According to the frequency of different histopathologic this area in a more timely and accurate manner. types, the most common type seen in our study was ALM (48.89%), followed by LLM type (17.78%). Moreover, his- topathologic types’ frequency had no significant differences 2. Materials and Methods between men and women (P � 0.97) and between different It was a retrospective, descriptive study of histopathological age groups (P � 0.86) [Figure 2]. types of CM in Isfahan, from 2013 to 2018, from the records )e mean depth of tumor penetration (Breslow thick- of Alzahra Hospital and Dr. Rajabi Pathology Laboratory. ness) was 3.87± 3.35 mm with a range of 0.8–15 mm in the Slides with a report of cutaneous melanoma were ob- present study. )e tumor penetration depth does not follow tained and re-evaluated by a dermatopathologist. Eligible the normal distribution [Table 2]. samples were those that had the patient’s data and the )e highest rate of tumor invasion was to the reticular patient’s pathology sheet. Moreover, the histopathology dermis (Clark IV) and then to the fat layer (Clark V), 42.2% and 22.2%, respectively [Table 2]. )e most common tumor type, Breslow, and Clark must be visible in the studied slides. If, according to the examining dermatopathologist opinion, lesion site was the foot and toes (31.1%), followed by the face (24.4%). )e lesion site’s frequency distribution based on the diagnosis of CM was not definitive, the sample would be excluded from the study. If the anonymous review was age, sex, and Breslow thickness is summarized in Table 3. disagreed with the original report, a secondary anonymous Vascular invasion was seen in eight patients (17.8%), of review by another dermatopathologist was considered as a which 62.5% were seen in ALM type. Furthermore, 19 diagnostic criterion. patients (42.2%) had ulcers. )e highest ulcer rate was in the All samples were reviewed anonymously, without the ALM type (52.63%) and then in NM and LMM types dermatopathologist knowing the first diagnosis of each slide. (15.78%). )e frequency distribution of vascular invasion Histopathological type of cutaneous melanoma, Clark’s and ulceration in the samples based on the depth of tumor invasion level, Breslow thickness, ulcer status, and vascular penetration and the lesion’s location is shown in Table 4. Journal of Skin Cancer 3 Table 1: )e frequency distribution of multiple variables based on histopathologic subtypes of cutaneous melanoma. Histopathologic types of cutaneous melanoma ALM LMM NM SSM Others Number 22 8 5 4 6 Percent 48.89 17.78 11.11 8.89 13.33 Gender (%) Male 10 (45.5) 4 (50) 2 (40) 2 (50) 2 (33.3) Female 12 (54.5) 4 (50) 3 (60) 2 (50) 4 (66.7) Mean age± SD 62.00± 15.25 69.13± 15.18 70.20± 15.02 60.25± 8.88 56.67± 19.61 Clark’s invasion level (%) Level I 1 (4.5) 1 (12.5) — 1 (25.0) — Level II 4 (18.2) 2 (25.0) — 2 (50.0) — Level III 2 (9.1) 1 (12.5) — 1 (25.0) 1 (16.7) Level IV 12 (54.5) 3 (37.5) 3 (60.0) — 1 (16.7) Level V 3 (13.6) 1 (12.5) 2 (40.0) — 4 (66.7) Depth of tumor penetration (Breslow thickness) (%) <1.00 5 (22.7) 3 (37.5) — 3 (75.0) — 1.00–2.00 3 (13.6) 2 (25.0) — 1 (25.0) 1 (16.7) 2.01–4.00 10 (45.5) 1 (12.5) — — — >4.00 4 (18.2) 2 (25.0) 5 (100) — 5 (83.3) Mean± SD 3.11± 2.16 2.48± 2.15 7.90± 4.56 1.10± 0.60 7.03± 3.99 Tumor location (%) Face — 7 (87.5) 2 (40.0) — 2 (33.3) Scalp — 1 (12.5) — — — Trunk — — 1 (20.0) 2 (50.0) 1 (16.7) Arm — — — 2 (50.0) 1 (16.7) Hand 7 (31.8) — — — — Anus — — 1 (20.0) — — Leg 1 (4.5) — 1 (20.0) — 2 (33.3) Foot 14 (63.6) — — — — Moreover, the mean age in men was 65.55± 16.29, and in women was 61.52± 14.70, which was not statistically significant (P � 0.38). show the same trend as previous studies. Notably, the most Others prevalent histopathological subtype was ALM (48.89%), SSM 13% followed by LMM (17.78%), NM (11.11%), and SSM (8.89%) 9% ALM [Figure 2]. As previous studies conducted in Iran’s different NM 49% cities showed, the most common histopathological subtype 11% in our study was ALM. )e prevalence of the ALM subtype LMM in the Kamyab et al.’s study [9] in Tehran was 30%, and in the 18% Handjani et al.’s study [10] in southern Iran was 44.8%. )ese results are consistent with other research studies conducted in the Asian and dark-skinned populations [11, 12]. According to the SEER database, ALM was predominant ALM SSM LMM Others among African–Americans, while the most common histo- NM pathologic subtype in other racial and ethnic groups in the United States was SSM [12, 13]. A large-scale study conducted Figure 2: Distribution of cutaneous melanoma according to his- in the Japanese population reported ALM as the most topathological subtype. prevalent subtype (40.4%). In contrast, the proportion of this subtype in non-Hispanic whites was only 1.5% [14]. Based on these and other valid studies, we can conclude that the ALM is 4. Discussion the most prevalent histopathological subtype in Asian and )e increasing prevalence of cutaneous malignant mela- dark-skinned populations. )us, geographical and racial noma in recent years has attracted the attention of many variations in melanoma’s clinical manifestations have been researchers. Our study revealed the histopathological confirmed. )e high prevalence of ALM might be a significant characteristics of melanoma in patients referred to Alzahra cause of the high mortality rate among these races despite the Hospital and Dr. Rajabi Pathology Laboratory in Isfahan, low incidence rate [3, 15]. According to the SEER study, from 2013 to 2018. Our melanoma patients’ mean age was African–Americans had significantly shorter melanoma- 63.31± 15.38, with a range of 32–92 years. )ese findings specific survival than Caucasians. In African–Americans 4 Journal of Skin Cancer Table 2: Frequency distribution of Breslow thickness and tumor invasion level. Variable Number Percent Depth of tumor penetration (Breslow thickness) <1.00 11 24.4 1.00–2.00 7 15.6 2.01–4.00 11 24.4 >4.00 16 35.6 Total 45 100 Clark’s invasion level Level I: limited to the epidermis 3 6.7 Level II: invasion of the papillary dermis 8 17.8 Level III: filling the papillary dermis to connect the reticular dermis 5 11.1 Level IV: invasion of the reticular dermis 19 42.2 Level V: fat invasion 10 22.2 Total 45 100 Table 3: )e frequency distribution of lesion site based on sex, age, and Breslow thickness. Gender (%) Tumor location Number Percent Mean age± SD Breslow’s thickness Male Female Face 11 24.4 6 (30.0) 5 (20.0) 69.55± 16.80 3.35± 2.47 Scalp 1 2.2 — 1 (4.0) 76.00 6.00 Trunk 4 8.9 3 (15.0) 1 (4.0) 63.50± 7.32 6.15± 6.29 Arm 3 6.7 — 3 (12.0) 59.67± 6.65 3.93± 4.42 Hand 7 15.6 — 7 (28.0) 59.57± 13.37 3.10± 1.27 Anus 1 2.2 — 1 (4.0) 73.00 15.00 Leg 4 8.9 2 (10.0) 2 (8.0) 51.25± 19.36 4.17± 2.07 Foot 14 31.1 9 (45.0) 5 (20.0) 62.86± 16.94 2.98± 2.54 Total 45 100 20 (100) 25 (100) Table 4: )e frequency distribution of vascular invasion and ulceration in the samples based on the lesion’s location and depth of tumor penetration. Vascular invasion (%) Ulceration (%) Variable Yes No Yes No )e whole sample 8 (17.8) 37 (82.2) 19 (42.2) 26 (57.8) Tumor location Face 1 (12.5) 10 (27.0) 6 (31.6) 5 (19.2) Scalp — 1 (2.7) — 1 (3.8) Trunk 1 (12.5) 3 (8.1) 1 (5.3) 3 (11.5) Arm 1 (12.5) 2 (5.4) 1 (5.3) 2 (7.7) Hand 1 (12.5) 6 (16.2) 5 (26.3) 2 (7.7) Anus — 1 (2.7) 1 (5.3) — Leg 1 (12.5) 3 (8.1) 1 (5.3) 3 (11.5) Foot 3 (37.5) 11 (29.7) 4 (21.1) 10 (38.5) Total 8 (100) 37 (100) 19 (100) 26 (100) Depth of tumor penetration (Breslow thickness) <1.00 — 11 (29.7) 1 (5.3) 10 (38.5) 1.00–2.00 — 7 (18.9) 3 (15.8) 4 (15.4) 2.01–4.00 1 (12.5) 10 (27.0) 6 (31.6) 5 (19.2) >4.00 7 (87.5) 9 (24.3) 9 (47.4) 7 (26.9) Total 8 (100) 37 (100) 19 (100) 26 (100) Mean± SD 7.12± 3.18 3.17± 2.98 5.08± 3.51 2.99± 2.98 melanoma patients with NM or ALM subtype, melanoma- In several other studies, the survival of the ALM subtype specific mortality was statically higher, while 5-year survival has also been compared with other subtypes. According to a was statically lower. Interestingly, African–Americans ex- study conducted by Ishihara et al., the survival of ALM was perienced higher melanoma-specific mortality and lower significantly lower than SSM in the Japanese population. survival for NM and ALM than Caucasians [12]. Fujisawa et al. reported no association between ALM and Journal of Skin Cancer 5 12 14 0 0 ALM LMM NM SSM Others ALM LMM NM SSM Others <1.00 2.01 - 4.00 Clark I Clark IV 1.00 - 2.00 >4.00 Clark II Clark V Clark III Figure 3: Breslow thickness in different types of melanoma. Figure 4: Clark’s invasion level in different types of melanoma. survival across the whole study. However, they found a significant survival disadvantage in the ALM stage IIIA. It ALM occurs are less likely to be noticed. So we diagnose this can be understood that ALM worsens the prognosis of subtype late, in advanced stages, with high penetration depth melanoma in the early stages of lymphatic spread, and this and high rate of ulceration. In Lee et al.’s study, the mean type may need to be evaluated for the indication of addi- duration of melanoma diagnosis in all groups was 20 tional treatments such as SLNB and adjuvant therapy months, ranging from 1 to 120 months. In contrast, the [14, 16]. mean duration of diagnosing ALM and non-ALM was ALM has also been reported as an independent negative 27± 33 and 12± 14 months, respectively. Notably, when this predictor of melanoma-specific survival in different studies variable was stratified against ethnicity, the delay was re- [12, 16, 17]. An extensive nationwide study in the Nether- ported to be 22± 28 months in Asians and 7± 5 months for lands showed that NM and ALM subtypes had lower survival Caucasians (P � 0.09) [15]. than SSM and LMM. In Gumaste et al.’s study, the hazard However, in various studies, the ALM subtype’s survival ratio of survival for ALMs vs. non-ALMs was 2.64 rate remained lower than other subtypes, even after con- (P � 0.001). Moreover, the ALM subtype’s recurrence rate trolling melanoma stages. Evidence exists to show that in- was statically more than the others (49% vs. 30%, p � 0.007), herent biologic differences in melanoma subtypes may also particularly in tumors with less than 2 mm penetration play an essential role in the prognosis and even therapeutic depth. )ese pieces of evidence suggest that ALM is a tough strategy of cutaneous melanoma. Patients with ALM have variant of melanoma and may require unique and more been shown to demonstrate specific genetic aberrations, invasive treatments [16, 17]. indicating that the potency of invasion and ALM progres- Various possible explanations have been put forward for sion may be biologically distinct from other types of cuta- these pieces of evidence. Patients with ALM often have neous melanoma [18]. Moreover, in contrast to Caucasians, deeper, more advanced stages, and a higher rate of ulceration the lower incidence rate and less awareness about melanoma at the time of diagnosis. Tumor thickness and ulceration in dark-skinned and Asian populations lead to a delay in have been reported as the most influential independent diagnosis and advanced stages at the presentation. Socio- predictors of survival for melanoma [13, 18]. In our study, economic status is also an important prognostic factor most ALM cases (45.5%) had Breslow thicknesses of 2.1 to among these groups. )is evidence highlights the impor- 4 mm [Figure 3, Table 1], and 54.5% were diagnosed at Clark tance of raising awareness about melanoma for all racial and invasion level IV [Figure 4, Table 1]. ethnic groups, particularly Asians [12]. )e most common Breslow thickness across the entire Our study’s primary limitation to the generalization of study was more than 4 mm (35.6%), and 42.2% of melanoma these results is the small sample size. However, our results patients were diagnosed at Clark invasion level IV [Table 2]. showed the same trend as other studies. According to Lee et al.’s study, the mean Breslow thickness in ALM subtypes was 2.5± 2.3 mm, while this amount in 5. Conclusion non-ALM subtypes was only 1.7± 2.0 mm (P � 0.30). )e highest rate of ulceration in the current study was also seen Our study showed that the ALM is the most prevalent in the ALM subtype (52.62%) [15]. melanoma subtype among the Iranian population. Our )e anatomic location and atypical presentation of ALM findings regarding the histopathology subtype, anatomic may also contribute to the poorer prognosis of ALM. In our location, tumor thickness, and Clark invasion level were also study, the most common tumor sites were foot and toes in agreement with other studies conducted in the Asian (31.1%) [Table 3]. In fact, the most common areas where population. 6 Journal of Skin Cancer United States, 1999–2006,” Journal of the American Academy Data Availability of Dermatology, vol. 65, no. 5, pp. S26.e1–S26.e13, 2011. [14] Y. Fujisawa, S. Yoshikawa, A. 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Published: Sep 19, 2022

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