Basal Cell Carcinoma: A Patient and Physician’s Experience

Basal Cell Carcinoma: A Patient and Physician’s Experience Dermatol Ther (Heidelb) https://doi.org/10.1007/s13555-018-0245-2 COMMENTARY Basal Cell Carcinoma: A Patient and Physician’s Experience . . Barbara J. Cohen Eliahou S. Cohen Philip R. Cohen Received: May 14, 2018 The Author(s) 2018 PATIENT’S EXPERIENCE ABSTRACT When I was a young girl my parents thought it In this article, the first coauthor, a patient with was healthy to put baby oil on one’s skin before a basal cell carcinoma on her upper lip, dis- going outside to be in the sun. Little did they cusses her experience with Mohs micrographic know that this action would cause so many surgery for the treatment of the skin cancer. The problems for me once I grew up and became an second coauthor, who is the patient’s physician adult. (a dermatologist who shares her last name but is Being fair-skinned and a redhead with blue not a relative), diagnosed her skin cancer and eyes, I had many sunburns followed by big referred her for Mohs surgery. The third coau- water blisters due to exposure to the sun’s rays. thor, who is the patient’s son and not only a As I became older, the dermatologist froze many dermatologist, but also a dermatopathologist areas of my body to correct the damage caused and a Mohs surgeon (and also shares her last by the sun’s rays in my youth. name), summarizes the presentation and treat- I had my first Mohs surgery more than ment of the basal cell carcinoma. 50 years ago. This was on my face, and I remember having the doctor cut the affected area, cover it with a bandage, and send me back Keywords: Basal; Cancer; Carcinoma; Cell; to the waiting room until the skin sample could Controlled; Experience; Micrographic; Mohs; be checked to make certain that all of the Patient; Physician; Skin; Surgery; Treatment cancerous cells had been removed. Another Enhanced digital features To view enhanced digital time, again on another part of my face while I features for this article go to https://doi.org/10.6084/ was still living in upstate New York, another m9.figshare.6292811. Mohs surgeon did the same procedure. Fortu- nately, both of these men were excellent; I did B. J. Cohen not suffer from any discomfort and the scars Delray Beach, Florida, USA were not noticeable. E. S. Cohen Now, I am an 82-year-‘young’ patient. My Advanced Dermatology and Cosmetic Surgery, son—Philip R. Cohen, MD—is a dermatologist; Delray Beach, Florida, USA however, he practices in California. Recently, P. R. Cohen (&) my current dermatologist—in Florida (where I Department of Dermatology, University of live)—referred me to my third Mohs surgeon. California San Diego, La Jolla, San Diego, CA, USA e-mail: mitehead@gmail.com Dermatol Ther (Heidelb) It was the strangest thing as I thought I had change my bandage. When I arrived at the scratched my face just above the right side of Mohs surgeon’s office the next day his assistant my upper lip. The scratch did not go away. I carefully and gently removed the bandage. She made an appointment to see my dermatologist said that the healing after the procedure was and showed it to Dr. Eli Cohen; although we progressing nicely and that I should continue to share the same family name, we are not rela- do much better. She was correct; although I still tives. He took a biopsy of the lesion and sent it was having significant discomfort and tightness to a dermatopathologist (Fig. 1). I was shocked in the area, I was no longer bleeding. Indeed, when I received the call from his office; it was my biggest problem was that I am a person who not a scratch, but a basal cell carcinoma. smiles a great deal and it was painful to smile Dr. Cohen said he was going to send me to during this time. the Mohs surgeon who had previously done When I returned to the office after the first several procedures on my husband. week some of the stitches were removed. This I went to the Mohs surgeon thinking this was done in such a caring manner that I felt no would be a simple procedure just like my other discomfort from the procedure. two experiences. Wrong. The Mohs surgeon The following week the remainder of the explained that the cancer area began above my stitches were removed; sure enough, I was able lip and extended into my lip; therefore, this to smile without any pain. I could hardly tell I time the procedure would be bit more difficult had an operation. I was healing so well and my and a bit more uncomfortable. He knew I was face looked natural (Figs. 3, 4). on a blood thinner and told me I had to stop it a My only problem now is that I am a bit few days before the operation so that I would numb at the surgical site on the right side of my not bleed profusely. I then became aware that I upper lip. However, I was informed that it could would have many stitches on my face, but the take up to 1 year for the normal sensation in lip itself had to be handled differently. The that area to spontaneously return. I was also doctor explained that I would need a pressure told to massage the area twice a day for 5 min at bandage since there would be small area that he a time until my next appointment that will be would not stitch. in 1 month. Naturally I was concerned and nervous. I was I have seen other people who had similar assured that everything would be all right, but operations for skin cancer. Some of them did that I would experience discomfort for a period not have the wonderful outcome that I experi- of time. enced. I feel very fortunate that I have had such The day of the surgery arrived. The area of excellent doctors. my lip containing the skin cancer was anes- In addition to my basal cell carcinoma, I also thetized; I felt no discomfort from the proce- had several actinic keratoses that Dr. Cohen dure (Fig. 1). It was explained to me that I ‘froze’ with liquid nitrogen. Therefore, I have would feel pain later and that I could take my skin examined by the dermatologist every acetaminophen for the pain. A huge area was 3–6 months. In addition, I will continue to bandaged and I felt quite awkward when I left apply sunscreen to my face, neck, and arms the office (Fig. 2). I was told to make two each day. appointments to see the Mohs surgeon: the first visit in 1 week for some of the stitches to be PHYSICIAN’S PERSPECTIVE removed and the second visit the following week for the remaining stitches to be removed. Basal cell carcinoma is the most common type Later that day, I realized that being on a of skin cancer [1]. Similar to Mrs. Cohen’s blood thinner made my surgery more difficult. tumor, it most frequently presents as a flesh- Unfortunately, after I went home, I noticed that colored papule or nodule on a sun-exposed site, I had bled through the bandage. I called the such as the face. Excision, using microscopically Mohs surgeon’s office; his staff told me to come controlled margins (Mohs micrographic back to the office the next day and they would Dermatol Ther (Heidelb) Fig. 1 a–d An 82-year-old woman developed a basal cell biopsy site (circled in purple ink), appears as a flesh-colored carcinoma on the right side of her upper lip. The upper lip, nodule. c Mohs surgery (with the tumor being cleared after right side, was the site of the non-healing scratch. a taking one surgical stage) was performed to excise the skin Photograph of the site after a shave biopsy had been cancer; purple ink (extending from the surgery-created performed to determine the diagnosis of the persistent skin tumor-free wound) marks the vermillion border between lesion (below the purple triangle and between the purple the cutaneous and mucosal upper lip. d The surgical linear lines); the surface of the lesion has been cauterized. b wound was modified into an ellipse; the wound was The residual basal cell carcinoma, which is located at the subsequently sutured in a side-to-side manner surgery), is a very effective management strat- Sun exposure (ultraviolet A and ultraviolet B egy for these tumors. However, the clinical radiation) is the most common risk factor for presentation of basal cell carcinoma can vary, developing basal cell carcinoma. Indeed, basal and there are several potential treatment cell carcinoma occurs more frequently in indi- modalities available for patients. viduals with certain physical features: blue or This article does not contain any new studies green eyes, freckles, blond or red hair, fair or with human or animal subjects performed by light skin color, and always burning and never any of the authors. tanning after being exposed to the sun. Dermatol Ther (Heidelb) Fig. 4 Closer views of the upper lip—no smiling (a) and smiling (b)—show that the surgical site has healed nicely and that the scar is well placed among the other skin folds on the upper lip Genomic analysis of basal cell carcinoma Fig. 2 Photograph of the patient taken postoperatively tumors has associated the cancer with an aber- showing a bulky pressure dressing on her upper lip ration of the Hedgehog pathway, with muta- tions affecting the PTCH1 (patched 1) gene [2–5]. Other risk factors also contribute to the pathogenesis of basal cell carcinoma. These include exposure to either an environmental toxin (such as arsenic, coal tar, and paraffin) and or to other sources of radiation, such as tanning beds and ionizing radiotherapy. Inju- ries to the skin (such as burns or chronic trauma) can also promote the development of this skin cancer. In addition, immunosuppres- sion is a risk factor that can predispose an individual to develop basal cell carcinoma—ei- ther iatrogenic-related secondary to the medi- cations to prevent rejection in the recipients of solid organ transplants or viral-associated in individuals with human immunodeficiency virus infection. Also, basal cell carcinoma is more prevalent in patients with certain inher- ited disorders; some of these genodermatoses include basal cell nevus syndrome, Bazex syn- drome, epidermolysis bullosa simplex (Dowling Fig. 3 Distant view of the patient’s face shows the upper Meara subtype), oculocutaneous albinism, lip following complete healing of the surgical site Rombo syndrome, and xeroderma pigmentosa [3, 4, 6–9]. Dermatol Ther (Heidelb) In addition to nodular basal cell carcino- Table 2 Histologic types of basal cell carcinoma mas—similar to that of Ms. Cohen’s skin can- Histologic types of basal cell carcinoma cer—that appear as telangiectatic or flesh- colored, smooth or ulcerated smaller papules of Amyloid deposit-associated \ 5 mm or as larger nodules of [ 6 mm, the Fibroepithelioma of Pinkus clinical presentation of these cancers can be Granular cell variable (Table 1)[5, 6, 10–19]. They also fre- quently appear as red plaques (superficial basal Infiltrative (morpheaform or sclerosing) cell carcinomas) or white indurated scar-like flat Infundibulocystic lesions (infiltrated basal cell carcinomas) [3]. Less commonly, they present as pedunculated Keratotic tag-like lesions often on the abdomen (fibroep- Nodular ithelioma of Pinkus) [14, 17] or red flat macules frequently on the face that mimic telangiec- Metatypical (basosquamous) tasias (red dot basal cell carcinomas) [11, 12, 15] Mixed or brown or black papules or patches that mimic melanocytic tumors (pigmented basal cell car- Micronodular cinomas) [6, 18]. In seldom cases, basal cell Myoepithelial differentiation carcinomas are linear in morphology [18]or Ossification-associated advanced cancers [5] or giant-sized tumors [19]; metastatic basal cell carcinomas with tumor Pigmented that has spread to other organs, such as the lung Pleomophic or liver, are extraordinarily rare [10, 13]. Mrs. Cohen’s basal cell carcinoma occurred Superficial on her upper cutaneous lip and extended beyond the vermillion border into her mucosal lip. Indeed, similar to her tumor, most basal cell sites, at locations that have been shielded from carcinomas occur on skin that has been directly the sun, or both; these include the axilla [6, 16], exposed to the sun. However, albeit less com- breast and nipple [20], buttock and perianal mon, basal cell carcinomas can occur at usual area [21], foot, groin, penis and scrotum, peri- ungual and subungual area (adjacent and Table 1 Clinical types of basal cell carcinoma beneath the nail) [22, 23], umbilicus [24], and Clinical types of basal cell carcinoma vulva. Each of the clinical variants of basal cell Advanced carcinoma has corresponding pathologic fea- Fibroepithelioma of Pinkus tures (Table 2)[3, 6, 14, 17–19, 25–33]. Tumors with fibroepithelioma of Pinkus, keratotic, Giant infundibulocystic, nodular, and superficial Infiltrating (morpheaform or sclerosing) pathologic growth patterns are at lower risk for persistence following treatment as compared to Linear those tumors with a more aggressive pathology Metastatic subtype, such as basosquamous, infiltrative, micronodular, and mixed [3, 26, 27, 30]. Less Nodular common pathologic variants (such as pig- Pigmented mented [6, 18], granular [28] and pleomorphic [29, 31] subtypes) and tumors with either asso- Red dot ciated amyloid [32] or myoepithelial differenti- Superficial ation [25] or osteoma cutis [33] typically demonstrate less aggressive biologic behavior. Dermatol Ther (Heidelb) A combination of clinical characteristics and Table 4 Treatment of basal cell carcinoma pathologic features of the tumor are consistent Treatment of basal cell carcinoma with basal cell carcinomas that have a higher Nonsurgical intervention risk for persistence (which is manifested clini- cally by recurrence) following treatment Cryosurgery (Table 3)[3, 34]. The therapeutic intervention Photodynamic therapy of choice for high-risk basal cell carcinomas is Mohs micrographic surgery—the treatment that Radiation therapy Mrs. Cohen received [34, 36]. Traditionally, the Topical therapies: 5-fluorouracil, imiquimod surgeon who removes the cancer also performs the microscopic evaluation of that surgical Surgical intervention specimen. This technique allows for evaluation Curettage and electrodessication of the entire peripheral margin of excision during the surgical process in order to confirm Excision (standard) that the cancer has been completely removed; if Mohs micrographic surgery residual tumor is noted, addition layers of tis- sue—at the sites indicated from examination of Systemic interventions the prior skin specimen—are taken until a Immune checkpoint inhibitors: nivolumab tumor-free border is achieved. Then, the surgi- Smoothened inhibitors: sonidegib, vismodegib cal wound is repaired. In addition to Mohs micrographic surgery, there are other surgical, nonsurgical, and sys- temic treatments for basal cell carcinoma treatments are considered for individuals with (Table 4)[5, 10, 13, 34, 35, 37–41]. Systemic either giant, advanced, or metastatic basal cell carcinomas [5, 10, 13]. Radiation therapy may Table 3 Features of high-risk basal cell carcinomas be considered for patients for whom surgery is not feasible or is contraindicated; in addition, Features of high-risk basal cell carcinomas adjuvant radiotherapy may be recommended Aggressive pathologic growth pattern for some individuals with high-risk basal cell carcinomas—such as patients whose tumors Borders of tumor: poorly defined have perineural invasion or have not been able Immunosuppressed patient to achieve a tumor-free margins of excision, or Location and corresponding size of tumor both [34, 35, 41]. Nonsurgical topical interven- tions may be considered in patients with Trunk and extremities (excluding hands, feet, nail superficial basal cell carcinomas units, pretibial and ankles): C 20 mm [34, 35, 37, 38, 40]. However, the cure rates of Cheeks, forehead, scalp, neck and pretibial : C 10 mm other treatment modalities are lower than those observed in patients whose tumors have been Central face, eyelids, eyebrows, periorbital skin, nose, excised using Mohs micrographic surgery. lips, chin, mandible, preauricular and postauricular skin/sulci, temple, ear, genitalia, hands and feet: C 1 mm (all of these locations constitute high-risk OUR PATIENT basal cell carcinoma independent of the tumor size) Mrs. Cohen presented to me with a persistent Perineural tumor involvement microscopically lesion on her upper lip. She has the phenotypic Radiation therapy previously at the tumor site features that have been associated with an increased risk for the development of skin can- Recurrent tumors cer, two prior basal cell carcinomas on her face, and a history of actinic keratoses that have Dermatol Ther (Heidelb) regularly been treated with liquid nitrogen disclose with regards to the publication of this cryotherapy. Mrs. Cohen was convinced this article. was only a scratch that was slow to heal; indeed, Compliance with Ethics Guidelines. This non-neoplastic conditions can mimic a basal article does not contain any new studies with cell carcinoma [42]. Also, bacterial or human or animal subjects performed by any of mycobacterial infection and basal cell carci- the authors. noma can be present in the same lesion [43]. However, I suspected that Mrs. Cohen had a Peer Review. Please note, contrary to the new basal cell carcinoma and performed a journal’s standard double-blind peer review biopsy to establish the diagnosis. process, as a commentary this article underwent The report from the dermatopathologist review by a member of the journal’s Editorial confirmed the diagnosis of a nodular basal cell Board. carcinoma. I referred Ms. Cohen to a Mohs surgeon to have the cancer removed. Her tumor Open Access. This article is distributed was cleared after one stage of excision, and the under the terms of the Creative Commons Mohs surgeon was able to repair the surgical Attribution-NonCommercial 4.0 International wound with a side-to-side closure. License (http://creativecommons.org/licenses/ Mrs. Cohen has achieved an excellent func- by-nc/4.0/), which permits any noncommer- tional and cosmetic result following the treat- cial use, distribution, and reproduction in any ment of her upper lip basal cell carcinoma. She medium, provided you give appropriate credit and I have discussed that after a patient devel- to the original author(s) and the source, provide ops a basal cell carcinoma, there is between a a link to the Creative Commons license, and 30–70% cumulative risk of developing another indicate if changes were made. basal cell carcinoma within the next 3 years [44–47]. Therefore, I will continue to regularly see Mrs. Cohen for total body skin checks. REFERENCES ACKNOWLEDGEMENTS 1. Cohen PR. Basal cell carcinoma. J Gt Houst Dent Soc. 1995;67(1):20–1. 2. Bakshi A, Chaudhary SC, Rana M, Elmets CA, Athar Funding. The authors are fully responsible M. Basal cell carcinoma pathogenesis and therapy for all content and editorial decisions and involving hedgehog signaling and beyond. Mol received no financial support or other form of Carcinog. 2017;56(12):2543–57. compensation related to the development of 3. Prieto-Granada C, Rodriguez-Waitkus P. Basal cell this manuscript. No funding was received for carcinoma: epidemiology, clinical and histologic publication of this article. features, and basic science review. Curr Probl Can- cer. 2015;39:198–205. Authorship. All named authors meet the 4. Verkouteren JAC, Ramdas KHR, Wakke M, Nijsten International Committee of Medical Journal T. Epidemiology of basal cell carcinoma: scholarly Editors (ICMJE) criteria for authorship of this review. Br J Dermatol. 2017;177(2):359–72. manuscript, take responsibility for the integrity of the work as a whole, and have given final 5. Goodman AM, Kato S, Cohen PR et al. Genomic landscape of advanced basal cell carcinoma: impli- approval for the version to be published. The cations for precision treatment with targeted and opinions expressed in the manuscript are those immune therapies. Oncoimmunology. of the authors. 2017;7(3):e1404217. Disclosures. Barbara J. Cohen, Eliahou S. 6. Cohen PR. Axillary basal cell carcinoma in patients with Goltz-Gorlin syndrome: report of basal cell Cohen, and Philip R. Cohen have nothing to carcinoma in both axilla of a woman with basal cell Dermatol Ther (Heidelb) nevus syndrome and literature review. Dermatol contributing to excessive growth. Indian J Derma- Online J 2014;20(8). pii: 13030/qt7pg665b9. tol. 2018;63(2):147–54. 7. Griffin JR, Cohen PR, Tschen JA et al. Basal cell 20. Chun KA, Cohen PR. Basal cell carcinoma of the carcinoma in childhood: case report and literature nipple-areola complex: a comprehensive review of review. J Am Acad Dermatol. 2007;57[5 the world literature. Dermatol Ther (Heidelb). Suppl]:S97–102. 2016;6(3):379. 8. Cohen PR. Genodermatoses with malignant 21. Cohen PR. Basal cell carcinoma of the buttock. potential. Am Fam Physician. 1992;45(5):1479–86. Skinmed. 2018;16(2):114–9. 9. Witmanowski H, Szychta P, Blochowiak K, Jundzill 22. Shimizu I, Cohen PR, Macfarlane DF. Surgical A, Czajkowski R. Basal cell nevus syndrome (Gorlin- treatment of basal cell carcinoma of the nail unit. Goltz syndrome): genetic predisposition, clinical Int J Dermatol. 2013;52(8):996–8. picture and treatment. Postepy Dermatol Alergol. 2017;34(4):381–7. 23. Martinelli PT, Cohen PR, Schulze KE, Dorsey KE, Nelson BR. Periungual basal cell carcinoma: case 10. Cohen PR, Kato S, Goodman AM, Ikeda S, Kurzrock report and literature review. Dermatol Surg. R. Appearance of new cutaneous superficial basal 2006;32(2):320–3. cell carcinomas during successful nivolumab treat- ment of refractory metastatic disease: implications 24. Narala S, Cohen PR. Basal cell carcinoma of the for immunotherapy in early versus late disease. Int J umbilicus: a comprehensive literature review. Cur- Mol Sci 2017;18(8). https://doi.org/10.3390/ eus. 2016;8(9):e770. ijms18081663 25. Cohen PR. Basal cell carcinoma with myoepithelial 11. Cohen PR. Red dot basal cell carcinoma. J Clin differentiation: case report and literature review. Aesthet Dermatol. 2017;10(5):56–8. Cureus. 2018;10(1):e2081. 12. Cohen PR. Red dot basal cell carcinoma: report of 26. Cohen PR. Cancer-associated perineural invasion cases and review of this unique presentation of versus reexcision-associated perineural invasion. basal cell carcinoma. Cureus. 2017;9(3):e1110. J Cutan Pathol. 2011;38(1):78–9. 13. Ikeda S, Goodman AM, Cohen PR, et al. Metastatic 27. Cohen PR, Schulze KE, Nelson BR. Basal cell carci- basal cell carcinoma with amplification of PD-L1: noma with mixed histology: a possible pathogene- exceptional response to anti-PD1 therapy. NPJ sis for recurrent skin cancer. Dermatol Surg. Genom Med 2016;1. https://doi.org/10.1038/ 2006;32(4):542–51. npjgenmed.2016.37. 28. Ma X, Wang G, Kuwadekar A et al. Granular cell 14. Haddock ES, Cohen PR. Fibroepithelioma of Pinkus basal cell carcinoma: a case report. J Cutan Pathol. revisited. Dermatol Ther (Heidelb). 2018;45(3):223–5. 2016;6(3):347–62. 29. Tschen JP, Cohen PR, Schulze KE, Tschen JA, Nel- 15. Loh TY, Cohen PR. Red dot basal cell carcinoma: an son BR. Pleomorphic basal cell carcinoma: case unusual variant of a common malignancy. J Drugs reports and review. South Med J. Dermatol. 2016;15(5):645–7. 2006;99(3):296–302. 16. Cohen PR. Basal cell carcinoma of the axilla: review 30. Cohen PR, Schulze KE, Nelson BR. Cutaneous car- of the world literature. Am J Clin Dermatol. cinoma with mixed histology: a potential etiology 2014;15(2):95–100. for skin cancer recurrence and an indication for Mohs microscopically controlled surgical excision. 17. Cohen PR, Tschen JA. Fibroepithelioma of Pinkus South Med J. 2005;98(7):740–7. presenting as a sessile thigh nodule. Skinmed. 2003;2(6):385–7. 31. Garcia JA, Cohen PR, Herzberg AJ, Wallis ME, Rap- ini RP. Pleomorphic basal cell carcinoma. J Am 18. Chopra KF, Cohen PR. 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Ratoosh SL, Cohen PR, Troncoso P. Cutaneous the management of basal cell carcinoma. Br J Der- malignancy and leprosy. Report of a patient with matol. 2008;159:35–48. Mycobacterium leprae and basal cell carcinoma con- currently present in the same lesion. J Dermatol 36. Eliezri Y, Cohen PR. Cancer recurrence following Surg Oncol. 1994;20(9):613–8. Mohs micrographic surgery: a mechanism of tumor persistence. Plast Reconstr Surg. 1992;90(1):121–5. 44. Karagas MR, Stukel TA, Greenberg ER, Baron JA, Mott LA, Stern RS. Risk of subsequent basal cell 37. Maytin EV, Kaw U, Ilyas M, Mack JA, Hu B. Blue carcinoma and squamous cell carcinoma of the skin light versus red light for photodynamic therapy of among patients with prior skin cancer. Skin Cancer basal cell carcinoma in patients with Gorlin syn- Prevention Study Group. JAMA. drome: a bilaterally controlled comparison study. 1992;267(24):3305–10. Photodiagn Photodyn Ther. 2018. https://doi.org/ 10.1016/j.pdpdt.2018.02.009. 45. Marcil I, Stern RS. Risk of developing a subsequent nonmelanoma skin cancer in patients with a his- 38. Ariza S, Espinosa S, Naranjo M. Nonsurgical thera- tory of nonmelanoma skin cancer: a critical review pies for basal cell carcinoma: a review. Actas Der- of the literature and meta-analysis. Arch Dermatol. mosifiliogr. 2017;108(9):809–17. 2000;136(12):1524–30. 39. Lanoue J, Goldenberg G. Basal cell carcinoma: a 46. Ramachandran S, Rajaratnam R, Smith AG, Lear JT, comprehensive review of existing and emerging Strange RC. Patients with both basal and squamous nonsurgical therapies. J Clin Aesthet Dermatol. cell carcinomas are at a lower risk of further basal cell carcinomas than patients with only a basal cell 2016;9(5):26–36. carcinoma. J Am Acad Dermatol. 2009;61(2):247–51. 40. Hanna E, Abadi R, Abbas O. Imiquimod in derma- tology: an overview. Int J Dermatol. 2016;55(8):831–44. 47. Flohil SC, van der Leest RJ, Arends LR, de Vries E, Nijsten T. Risk of subsequent cutaneous malig- 41. Alter M, Hillen U, Leiter U, Sachse M, Gutzmer R. nancy in patients with prior keratinocyte carci- Current diagnosis and treatment of basal cell car- noma: a systematic review and meta-analysis. Eur J cinoma. J Dtsch Dermatol Ges. 2015;13(9):863–74. Cancer. 2013;49(10):2365–75. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Dermatology and Therapy Springer Journals

Basal Cell Carcinoma: A Patient and Physician’s Experience

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Abstract

Dermatol Ther (Heidelb) https://doi.org/10.1007/s13555-018-0245-2 COMMENTARY Basal Cell Carcinoma: A Patient and Physician’s Experience . . Barbara J. Cohen Eliahou S. Cohen Philip R. Cohen Received: May 14, 2018 The Author(s) 2018 PATIENT’S EXPERIENCE ABSTRACT When I was a young girl my parents thought it In this article, the first coauthor, a patient with was healthy to put baby oil on one’s skin before a basal cell carcinoma on her upper lip, dis- going outside to be in the sun. Little did they cusses her experience with Mohs micrographic know that this action would cause so many surgery for the treatment of the skin cancer. The problems for me once I grew up and became an second coauthor, who is the patient’s physician adult. (a dermatologist who shares her last name but is Being fair-skinned and a redhead with blue not a relative), diagnosed her skin cancer and eyes, I had many sunburns followed by big referred her for Mohs surgery. The third coau- water blisters due to exposure to the sun’s rays. thor, who is the patient’s son and not only a As I became older, the dermatologist froze many dermatologist, but also a dermatopathologist areas of my body to correct the damage caused and a Mohs surgeon (and also shares her last by the sun’s rays in my youth. name), summarizes the presentation and treat- I had my first Mohs surgery more than ment of the basal cell carcinoma. 50 years ago. This was on my face, and I remember having the doctor cut the affected area, cover it with a bandage, and send me back Keywords: Basal; Cancer; Carcinoma; Cell; to the waiting room until the skin sample could Controlled; Experience; Micrographic; Mohs; be checked to make certain that all of the Patient; Physician; Skin; Surgery; Treatment cancerous cells had been removed. Another Enhanced digital features To view enhanced digital time, again on another part of my face while I features for this article go to https://doi.org/10.6084/ was still living in upstate New York, another m9.figshare.6292811. Mohs surgeon did the same procedure. Fortu- nately, both of these men were excellent; I did B. J. Cohen not suffer from any discomfort and the scars Delray Beach, Florida, USA were not noticeable. E. S. Cohen Now, I am an 82-year-‘young’ patient. My Advanced Dermatology and Cosmetic Surgery, son—Philip R. Cohen, MD—is a dermatologist; Delray Beach, Florida, USA however, he practices in California. Recently, P. R. Cohen (&) my current dermatologist—in Florida (where I Department of Dermatology, University of live)—referred me to my third Mohs surgeon. California San Diego, La Jolla, San Diego, CA, USA e-mail: mitehead@gmail.com Dermatol Ther (Heidelb) It was the strangest thing as I thought I had change my bandage. When I arrived at the scratched my face just above the right side of Mohs surgeon’s office the next day his assistant my upper lip. The scratch did not go away. I carefully and gently removed the bandage. She made an appointment to see my dermatologist said that the healing after the procedure was and showed it to Dr. Eli Cohen; although we progressing nicely and that I should continue to share the same family name, we are not rela- do much better. She was correct; although I still tives. He took a biopsy of the lesion and sent it was having significant discomfort and tightness to a dermatopathologist (Fig. 1). I was shocked in the area, I was no longer bleeding. Indeed, when I received the call from his office; it was my biggest problem was that I am a person who not a scratch, but a basal cell carcinoma. smiles a great deal and it was painful to smile Dr. Cohen said he was going to send me to during this time. the Mohs surgeon who had previously done When I returned to the office after the first several procedures on my husband. week some of the stitches were removed. This I went to the Mohs surgeon thinking this was done in such a caring manner that I felt no would be a simple procedure just like my other discomfort from the procedure. two experiences. Wrong. The Mohs surgeon The following week the remainder of the explained that the cancer area began above my stitches were removed; sure enough, I was able lip and extended into my lip; therefore, this to smile without any pain. I could hardly tell I time the procedure would be bit more difficult had an operation. I was healing so well and my and a bit more uncomfortable. He knew I was face looked natural (Figs. 3, 4). on a blood thinner and told me I had to stop it a My only problem now is that I am a bit few days before the operation so that I would numb at the surgical site on the right side of my not bleed profusely. I then became aware that I upper lip. However, I was informed that it could would have many stitches on my face, but the take up to 1 year for the normal sensation in lip itself had to be handled differently. The that area to spontaneously return. I was also doctor explained that I would need a pressure told to massage the area twice a day for 5 min at bandage since there would be small area that he a time until my next appointment that will be would not stitch. in 1 month. Naturally I was concerned and nervous. I was I have seen other people who had similar assured that everything would be all right, but operations for skin cancer. Some of them did that I would experience discomfort for a period not have the wonderful outcome that I experi- of time. enced. I feel very fortunate that I have had such The day of the surgery arrived. The area of excellent doctors. my lip containing the skin cancer was anes- In addition to my basal cell carcinoma, I also thetized; I felt no discomfort from the proce- had several actinic keratoses that Dr. Cohen dure (Fig. 1). It was explained to me that I ‘froze’ with liquid nitrogen. Therefore, I have would feel pain later and that I could take my skin examined by the dermatologist every acetaminophen for the pain. A huge area was 3–6 months. In addition, I will continue to bandaged and I felt quite awkward when I left apply sunscreen to my face, neck, and arms the office (Fig. 2). I was told to make two each day. appointments to see the Mohs surgeon: the first visit in 1 week for some of the stitches to be PHYSICIAN’S PERSPECTIVE removed and the second visit the following week for the remaining stitches to be removed. Basal cell carcinoma is the most common type Later that day, I realized that being on a of skin cancer [1]. Similar to Mrs. Cohen’s blood thinner made my surgery more difficult. tumor, it most frequently presents as a flesh- Unfortunately, after I went home, I noticed that colored papule or nodule on a sun-exposed site, I had bled through the bandage. I called the such as the face. Excision, using microscopically Mohs surgeon’s office; his staff told me to come controlled margins (Mohs micrographic back to the office the next day and they would Dermatol Ther (Heidelb) Fig. 1 a–d An 82-year-old woman developed a basal cell biopsy site (circled in purple ink), appears as a flesh-colored carcinoma on the right side of her upper lip. The upper lip, nodule. c Mohs surgery (with the tumor being cleared after right side, was the site of the non-healing scratch. a taking one surgical stage) was performed to excise the skin Photograph of the site after a shave biopsy had been cancer; purple ink (extending from the surgery-created performed to determine the diagnosis of the persistent skin tumor-free wound) marks the vermillion border between lesion (below the purple triangle and between the purple the cutaneous and mucosal upper lip. d The surgical linear lines); the surface of the lesion has been cauterized. b wound was modified into an ellipse; the wound was The residual basal cell carcinoma, which is located at the subsequently sutured in a side-to-side manner surgery), is a very effective management strat- Sun exposure (ultraviolet A and ultraviolet B egy for these tumors. However, the clinical radiation) is the most common risk factor for presentation of basal cell carcinoma can vary, developing basal cell carcinoma. Indeed, basal and there are several potential treatment cell carcinoma occurs more frequently in indi- modalities available for patients. viduals with certain physical features: blue or This article does not contain any new studies green eyes, freckles, blond or red hair, fair or with human or animal subjects performed by light skin color, and always burning and never any of the authors. tanning after being exposed to the sun. Dermatol Ther (Heidelb) Fig. 4 Closer views of the upper lip—no smiling (a) and smiling (b)—show that the surgical site has healed nicely and that the scar is well placed among the other skin folds on the upper lip Genomic analysis of basal cell carcinoma Fig. 2 Photograph of the patient taken postoperatively tumors has associated the cancer with an aber- showing a bulky pressure dressing on her upper lip ration of the Hedgehog pathway, with muta- tions affecting the PTCH1 (patched 1) gene [2–5]. Other risk factors also contribute to the pathogenesis of basal cell carcinoma. These include exposure to either an environmental toxin (such as arsenic, coal tar, and paraffin) and or to other sources of radiation, such as tanning beds and ionizing radiotherapy. Inju- ries to the skin (such as burns or chronic trauma) can also promote the development of this skin cancer. In addition, immunosuppres- sion is a risk factor that can predispose an individual to develop basal cell carcinoma—ei- ther iatrogenic-related secondary to the medi- cations to prevent rejection in the recipients of solid organ transplants or viral-associated in individuals with human immunodeficiency virus infection. Also, basal cell carcinoma is more prevalent in patients with certain inher- ited disorders; some of these genodermatoses include basal cell nevus syndrome, Bazex syn- drome, epidermolysis bullosa simplex (Dowling Fig. 3 Distant view of the patient’s face shows the upper Meara subtype), oculocutaneous albinism, lip following complete healing of the surgical site Rombo syndrome, and xeroderma pigmentosa [3, 4, 6–9]. Dermatol Ther (Heidelb) In addition to nodular basal cell carcino- Table 2 Histologic types of basal cell carcinoma mas—similar to that of Ms. Cohen’s skin can- Histologic types of basal cell carcinoma cer—that appear as telangiectatic or flesh- colored, smooth or ulcerated smaller papules of Amyloid deposit-associated \ 5 mm or as larger nodules of [ 6 mm, the Fibroepithelioma of Pinkus clinical presentation of these cancers can be Granular cell variable (Table 1)[5, 6, 10–19]. They also fre- quently appear as red plaques (superficial basal Infiltrative (morpheaform or sclerosing) cell carcinomas) or white indurated scar-like flat Infundibulocystic lesions (infiltrated basal cell carcinomas) [3]. Less commonly, they present as pedunculated Keratotic tag-like lesions often on the abdomen (fibroep- Nodular ithelioma of Pinkus) [14, 17] or red flat macules frequently on the face that mimic telangiec- Metatypical (basosquamous) tasias (red dot basal cell carcinomas) [11, 12, 15] Mixed or brown or black papules or patches that mimic melanocytic tumors (pigmented basal cell car- Micronodular cinomas) [6, 18]. In seldom cases, basal cell Myoepithelial differentiation carcinomas are linear in morphology [18]or Ossification-associated advanced cancers [5] or giant-sized tumors [19]; metastatic basal cell carcinomas with tumor Pigmented that has spread to other organs, such as the lung Pleomophic or liver, are extraordinarily rare [10, 13]. Mrs. Cohen’s basal cell carcinoma occurred Superficial on her upper cutaneous lip and extended beyond the vermillion border into her mucosal lip. Indeed, similar to her tumor, most basal cell sites, at locations that have been shielded from carcinomas occur on skin that has been directly the sun, or both; these include the axilla [6, 16], exposed to the sun. However, albeit less com- breast and nipple [20], buttock and perianal mon, basal cell carcinomas can occur at usual area [21], foot, groin, penis and scrotum, peri- ungual and subungual area (adjacent and Table 1 Clinical types of basal cell carcinoma beneath the nail) [22, 23], umbilicus [24], and Clinical types of basal cell carcinoma vulva. Each of the clinical variants of basal cell Advanced carcinoma has corresponding pathologic fea- Fibroepithelioma of Pinkus tures (Table 2)[3, 6, 14, 17–19, 25–33]. Tumors with fibroepithelioma of Pinkus, keratotic, Giant infundibulocystic, nodular, and superficial Infiltrating (morpheaform or sclerosing) pathologic growth patterns are at lower risk for persistence following treatment as compared to Linear those tumors with a more aggressive pathology Metastatic subtype, such as basosquamous, infiltrative, micronodular, and mixed [3, 26, 27, 30]. Less Nodular common pathologic variants (such as pig- Pigmented mented [6, 18], granular [28] and pleomorphic [29, 31] subtypes) and tumors with either asso- Red dot ciated amyloid [32] or myoepithelial differenti- Superficial ation [25] or osteoma cutis [33] typically demonstrate less aggressive biologic behavior. Dermatol Ther (Heidelb) A combination of clinical characteristics and Table 4 Treatment of basal cell carcinoma pathologic features of the tumor are consistent Treatment of basal cell carcinoma with basal cell carcinomas that have a higher Nonsurgical intervention risk for persistence (which is manifested clini- cally by recurrence) following treatment Cryosurgery (Table 3)[3, 34]. The therapeutic intervention Photodynamic therapy of choice for high-risk basal cell carcinomas is Mohs micrographic surgery—the treatment that Radiation therapy Mrs. Cohen received [34, 36]. Traditionally, the Topical therapies: 5-fluorouracil, imiquimod surgeon who removes the cancer also performs the microscopic evaluation of that surgical Surgical intervention specimen. This technique allows for evaluation Curettage and electrodessication of the entire peripheral margin of excision during the surgical process in order to confirm Excision (standard) that the cancer has been completely removed; if Mohs micrographic surgery residual tumor is noted, addition layers of tis- sue—at the sites indicated from examination of Systemic interventions the prior skin specimen—are taken until a Immune checkpoint inhibitors: nivolumab tumor-free border is achieved. Then, the surgi- Smoothened inhibitors: sonidegib, vismodegib cal wound is repaired. In addition to Mohs micrographic surgery, there are other surgical, nonsurgical, and sys- temic treatments for basal cell carcinoma treatments are considered for individuals with (Table 4)[5, 10, 13, 34, 35, 37–41]. Systemic either giant, advanced, or metastatic basal cell carcinomas [5, 10, 13]. Radiation therapy may Table 3 Features of high-risk basal cell carcinomas be considered for patients for whom surgery is not feasible or is contraindicated; in addition, Features of high-risk basal cell carcinomas adjuvant radiotherapy may be recommended Aggressive pathologic growth pattern for some individuals with high-risk basal cell carcinomas—such as patients whose tumors Borders of tumor: poorly defined have perineural invasion or have not been able Immunosuppressed patient to achieve a tumor-free margins of excision, or Location and corresponding size of tumor both [34, 35, 41]. Nonsurgical topical interven- tions may be considered in patients with Trunk and extremities (excluding hands, feet, nail superficial basal cell carcinomas units, pretibial and ankles): C 20 mm [34, 35, 37, 38, 40]. However, the cure rates of Cheeks, forehead, scalp, neck and pretibial : C 10 mm other treatment modalities are lower than those observed in patients whose tumors have been Central face, eyelids, eyebrows, periorbital skin, nose, excised using Mohs micrographic surgery. lips, chin, mandible, preauricular and postauricular skin/sulci, temple, ear, genitalia, hands and feet: C 1 mm (all of these locations constitute high-risk OUR PATIENT basal cell carcinoma independent of the tumor size) Mrs. Cohen presented to me with a persistent Perineural tumor involvement microscopically lesion on her upper lip. She has the phenotypic Radiation therapy previously at the tumor site features that have been associated with an increased risk for the development of skin can- Recurrent tumors cer, two prior basal cell carcinomas on her face, and a history of actinic keratoses that have Dermatol Ther (Heidelb) regularly been treated with liquid nitrogen disclose with regards to the publication of this cryotherapy. Mrs. Cohen was convinced this article. was only a scratch that was slow to heal; indeed, Compliance with Ethics Guidelines. This non-neoplastic conditions can mimic a basal article does not contain any new studies with cell carcinoma [42]. Also, bacterial or human or animal subjects performed by any of mycobacterial infection and basal cell carci- the authors. noma can be present in the same lesion [43]. However, I suspected that Mrs. Cohen had a Peer Review. Please note, contrary to the new basal cell carcinoma and performed a journal’s standard double-blind peer review biopsy to establish the diagnosis. process, as a commentary this article underwent The report from the dermatopathologist review by a member of the journal’s Editorial confirmed the diagnosis of a nodular basal cell Board. carcinoma. I referred Ms. Cohen to a Mohs surgeon to have the cancer removed. Her tumor Open Access. This article is distributed was cleared after one stage of excision, and the under the terms of the Creative Commons Mohs surgeon was able to repair the surgical Attribution-NonCommercial 4.0 International wound with a side-to-side closure. License (http://creativecommons.org/licenses/ Mrs. Cohen has achieved an excellent func- by-nc/4.0/), which permits any noncommer- tional and cosmetic result following the treat- cial use, distribution, and reproduction in any ment of her upper lip basal cell carcinoma. She medium, provided you give appropriate credit and I have discussed that after a patient devel- to the original author(s) and the source, provide ops a basal cell carcinoma, there is between a a link to the Creative Commons license, and 30–70% cumulative risk of developing another indicate if changes were made. basal cell carcinoma within the next 3 years [44–47]. Therefore, I will continue to regularly see Mrs. Cohen for total body skin checks. REFERENCES ACKNOWLEDGEMENTS 1. Cohen PR. Basal cell carcinoma. J Gt Houst Dent Soc. 1995;67(1):20–1. 2. Bakshi A, Chaudhary SC, Rana M, Elmets CA, Athar Funding. The authors are fully responsible M. Basal cell carcinoma pathogenesis and therapy for all content and editorial decisions and involving hedgehog signaling and beyond. Mol received no financial support or other form of Carcinog. 2017;56(12):2543–57. compensation related to the development of 3. Prieto-Granada C, Rodriguez-Waitkus P. Basal cell this manuscript. No funding was received for carcinoma: epidemiology, clinical and histologic publication of this article. features, and basic science review. Curr Probl Can- cer. 2015;39:198–205. Authorship. All named authors meet the 4. Verkouteren JAC, Ramdas KHR, Wakke M, Nijsten International Committee of Medical Journal T. Epidemiology of basal cell carcinoma: scholarly Editors (ICMJE) criteria for authorship of this review. Br J Dermatol. 2017;177(2):359–72. manuscript, take responsibility for the integrity of the work as a whole, and have given final 5. Goodman AM, Kato S, Cohen PR et al. Genomic landscape of advanced basal cell carcinoma: impli- approval for the version to be published. The cations for precision treatment with targeted and opinions expressed in the manuscript are those immune therapies. Oncoimmunology. of the authors. 2017;7(3):e1404217. Disclosures. Barbara J. Cohen, Eliahou S. 6. Cohen PR. Axillary basal cell carcinoma in patients with Goltz-Gorlin syndrome: report of basal cell Cohen, and Philip R. Cohen have nothing to carcinoma in both axilla of a woman with basal cell Dermatol Ther (Heidelb) nevus syndrome and literature review. Dermatol contributing to excessive growth. Indian J Derma- Online J 2014;20(8). pii: 13030/qt7pg665b9. tol. 2018;63(2):147–54. 7. Griffin JR, Cohen PR, Tschen JA et al. Basal cell 20. Chun KA, Cohen PR. Basal cell carcinoma of the carcinoma in childhood: case report and literature nipple-areola complex: a comprehensive review of review. J Am Acad Dermatol. 2007;57[5 the world literature. Dermatol Ther (Heidelb). Suppl]:S97–102. 2016;6(3):379. 8. Cohen PR. Genodermatoses with malignant 21. Cohen PR. Basal cell carcinoma of the buttock. potential. Am Fam Physician. 1992;45(5):1479–86. Skinmed. 2018;16(2):114–9. 9. Witmanowski H, Szychta P, Blochowiak K, Jundzill 22. Shimizu I, Cohen PR, Macfarlane DF. Surgical A, Czajkowski R. Basal cell nevus syndrome (Gorlin- treatment of basal cell carcinoma of the nail unit. Goltz syndrome): genetic predisposition, clinical Int J Dermatol. 2013;52(8):996–8. picture and treatment. Postepy Dermatol Alergol. 2017;34(4):381–7. 23. Martinelli PT, Cohen PR, Schulze KE, Dorsey KE, Nelson BR. Periungual basal cell carcinoma: case 10. Cohen PR, Kato S, Goodman AM, Ikeda S, Kurzrock report and literature review. Dermatol Surg. R. Appearance of new cutaneous superficial basal 2006;32(2):320–3. cell carcinomas during successful nivolumab treat- ment of refractory metastatic disease: implications 24. Narala S, Cohen PR. Basal cell carcinoma of the for immunotherapy in early versus late disease. Int J umbilicus: a comprehensive literature review. Cur- Mol Sci 2017;18(8). https://doi.org/10.3390/ eus. 2016;8(9):e770. ijms18081663 25. Cohen PR. Basal cell carcinoma with myoepithelial 11. Cohen PR. Red dot basal cell carcinoma. J Clin differentiation: case report and literature review. Aesthet Dermatol. 2017;10(5):56–8. Cureus. 2018;10(1):e2081. 12. Cohen PR. Red dot basal cell carcinoma: report of 26. Cohen PR. Cancer-associated perineural invasion cases and review of this unique presentation of versus reexcision-associated perineural invasion. basal cell carcinoma. Cureus. 2017;9(3):e1110. J Cutan Pathol. 2011;38(1):78–9. 13. Ikeda S, Goodman AM, Cohen PR, et al. Metastatic 27. Cohen PR, Schulze KE, Nelson BR. Basal cell carci- basal cell carcinoma with amplification of PD-L1: noma with mixed histology: a possible pathogene- exceptional response to anti-PD1 therapy. NPJ sis for recurrent skin cancer. Dermatol Surg. Genom Med 2016;1. https://doi.org/10.1038/ 2006;32(4):542–51. npjgenmed.2016.37. 28. Ma X, Wang G, Kuwadekar A et al. Granular cell 14. Haddock ES, Cohen PR. Fibroepithelioma of Pinkus basal cell carcinoma: a case report. J Cutan Pathol. revisited. Dermatol Ther (Heidelb). 2018;45(3):223–5. 2016;6(3):347–62. 29. Tschen JP, Cohen PR, Schulze KE, Tschen JA, Nel- 15. Loh TY, Cohen PR. Red dot basal cell carcinoma: an son BR. Pleomorphic basal cell carcinoma: case unusual variant of a common malignancy. J Drugs reports and review. South Med J. Dermatol. 2016;15(5):645–7. 2006;99(3):296–302. 16. Cohen PR. Basal cell carcinoma of the axilla: review 30. Cohen PR, Schulze KE, Nelson BR. Cutaneous car- of the world literature. Am J Clin Dermatol. cinoma with mixed histology: a potential etiology 2014;15(2):95–100. for skin cancer recurrence and an indication for Mohs microscopically controlled surgical excision. 17. Cohen PR, Tschen JA. Fibroepithelioma of Pinkus South Med J. 2005;98(7):740–7. presenting as a sessile thigh nodule. Skinmed. 2003;2(6):385–7. 31. Garcia JA, Cohen PR, Herzberg AJ, Wallis ME, Rap- ini RP. Pleomorphic basal cell carcinoma. J Am 18. Chopra KF, Cohen PR. Linear basal cell carcinoma: Acad Dermatol. 1995;32(5 Pt 1):740–6. report of multiple sequential tumors localized to a radiotherapy port and review of the literature. Tex 32. Satti MB, Azzopardi JG. Amyloid deposits in basal Med. 1997;93(7):57–9. cell carcinoma of the skin: a pathologic study of 199 cases. J Am Acad Dermatol. 1990;22:1082–7. 19. Purnell JC, Gardner JM, Brown JA, Shalin SC. Conventional versus giant basal cell carcinoma, a 33. Boyd AS, King LE. Basal cell carcinoma with ossifi- review of 57 cases: histologic differences cation. J Am Acad Dermatol. 1998;38:906–10. Dermatol Ther (Heidelb) 34. Work Group; Invited Reviewers, Kim JYS et al. 42. Cohen PR, Eliezri YD. Cutaneous odontogenic sinus Guidelines of care for the management of basal cell simulating a basal cell carcinoma: case report and carcinoma. J Am Acad Dermatol 2018; literature review. Plast Reconstr Surg. 78(3):540–559. 1990;86(1):123–7. 35. Telfer NR, Colver GB, Morton CA. Guidelines for 43. Ratoosh SL, Cohen PR, Troncoso P. Cutaneous the management of basal cell carcinoma. Br J Der- malignancy and leprosy. Report of a patient with matol. 2008;159:35–48. Mycobacterium leprae and basal cell carcinoma con- currently present in the same lesion. J Dermatol 36. Eliezri Y, Cohen PR. Cancer recurrence following Surg Oncol. 1994;20(9):613–8. Mohs micrographic surgery: a mechanism of tumor persistence. Plast Reconstr Surg. 1992;90(1):121–5. 44. Karagas MR, Stukel TA, Greenberg ER, Baron JA, Mott LA, Stern RS. Risk of subsequent basal cell 37. Maytin EV, Kaw U, Ilyas M, Mack JA, Hu B. Blue carcinoma and squamous cell carcinoma of the skin light versus red light for photodynamic therapy of among patients with prior skin cancer. Skin Cancer basal cell carcinoma in patients with Gorlin syn- Prevention Study Group. JAMA. drome: a bilaterally controlled comparison study. 1992;267(24):3305–10. Photodiagn Photodyn Ther. 2018. https://doi.org/ 10.1016/j.pdpdt.2018.02.009. 45. Marcil I, Stern RS. Risk of developing a subsequent nonmelanoma skin cancer in patients with a his- 38. Ariza S, Espinosa S, Naranjo M. Nonsurgical thera- tory of nonmelanoma skin cancer: a critical review pies for basal cell carcinoma: a review. Actas Der- of the literature and meta-analysis. Arch Dermatol. mosifiliogr. 2017;108(9):809–17. 2000;136(12):1524–30. 39. Lanoue J, Goldenberg G. Basal cell carcinoma: a 46. Ramachandran S, Rajaratnam R, Smith AG, Lear JT, comprehensive review of existing and emerging Strange RC. Patients with both basal and squamous nonsurgical therapies. J Clin Aesthet Dermatol. cell carcinomas are at a lower risk of further basal cell carcinomas than patients with only a basal cell 2016;9(5):26–36. carcinoma. J Am Acad Dermatol. 2009;61(2):247–51. 40. Hanna E, Abadi R, Abbas O. Imiquimod in derma- tology: an overview. Int J Dermatol. 2016;55(8):831–44. 47. Flohil SC, van der Leest RJ, Arends LR, de Vries E, Nijsten T. Risk of subsequent cutaneous malig- 41. Alter M, Hillen U, Leiter U, Sachse M, Gutzmer R. nancy in patients with prior keratinocyte carci- Current diagnosis and treatment of basal cell car- noma: a systematic review and meta-analysis. Eur J cinoma. J Dtsch Dermatol Ges. 2015;13(9):863–74. Cancer. 2013;49(10):2365–75.

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Dermatology and TherapySpringer Journals

Published: Jun 2, 2018

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