CASE REPORT
In-Transit Metastasis from Primary Cutaneous Squamous Cell Carcinoma in a Nonimmunosuppressed Patient ¨ lku¨men, Utkan Kızıltac¸, Tu¨lin Yu¨ksel, Ays¸e Seza Kunter, and Selma S¸engiz Erhan Emek Kocatu¨rk, Pelin Kuteyla U Background: In-transit metastases are dermal and subcutanous metastatic foci located between the tumor and the closest regional lymph node. Although in-transit metastasis has been commonly described for malignant melanoma, there have been some reports of in-transit metastases arising from primary cutaneous malignancies. The risk of development of in-transit metastases is higher in patients with high-risk squamous cell carcinoma. Case Report: We present a case of in-transit metastasis in a nonimmunosuppressed patient with a primary cutaneous squamous cell carcinoma. Contexte: Les me´tastases en transit sont des foyers me´tastatiques dermiques ou sous-cutane´s, situe´s entre la tumeur et le nœud lymphoı¨de re´gional le plus pre`s. Les me´tastases en transit sont souvent de´crites en lien avec les me´lanomes, mais des rapports font aussi e´tat de me´tastases en transit, issues de tumeurs malignes cutane´es primitives. Le risque de me´tastases en transit est plus e´leve´ chez les patients atteints d’un carcinome squameux a` risque e´leve´. Expose´ de cas: Sera expose´ ici un cas me´tastase en transit chez un patient non immunode´prime´, atteint d’un carcinome squameux primitif de la peau.
UTANEOUS SQUAMOUS CELL CARCINOMA (CSCC) is the second most common nonmelanoma skin cancer, with a lifetime incidence between 7 and 11%, and the frequency of incidence is increasing.1–3 There is a 100-fold increased risk of CSCC in organ transplant recipients (OTRs), and the sites of distribution of primary tumors do not change in immunosuppressed patients.4 The percentage of local and distant metastasis of CSCC is reported to be around 5%; however, the percentage increases up to 15 to 38% in cases of high-risk squamous cell carcinoma.1 In immunosuppressed patients, the metastatic rate of CSCC is reported as 12.9%, twice the rate of nonimmunosuppressed patients.5 Even though the prognosis is favorable in general, approximately 1.5% of cases are reported to die from the disease.3 In-transit metastases are rare and present as dermal and subcutaneous metastatic foci located between the tumor and the closest regional lymph node.6 Although in-transit
C
From the Departments of Dermatology and Pathology, Okmeydanı Training and Research Hospital, Istanbul, Turkey. Address reprint requests to: Emek Kocatu¨rk, MD, Department of Dermatology, Okmeydanı Training and Research Hospital, Nadiraga Sok. No: 25/9 Go¨ztepe, 34730, Istanbul, Turkey; e-mail: [email protected].
DOI 10.2310/7750.2014.14047 # 2014 Canadian Dermatology Association
metastasis has been commonly described for malignant melanoma, there have been some reports of in-transit metastases arising from cutaneous malignancies such as squamous cell carcinoma, basal cell carcinoma, Merkel cell carcinoma, malignant fibrous histiocytoma, primary mucinous carcinoma, and primary eccrine porocarcinoma.7–13 Recently, in-transit metastasis of primary CSCC in organ transplant recipients and nonimmunosuppressed patients has been reported in the literature.6 We present a case of in-transit metastasis in a nonimmunosuppressed patient with a primary CSCC.
Case Report A 59-year-old man presented to our dermatology clinic with painful, nonhealing ulcerations on the right leg and inguinal area. When the patient was asked about his history, we learned that a tumoral lesion on the fifth toe of the right foot had been amputated at the metatarsophalangeal joint level 6 months ago, and histopathologic examination of the specimen revealed a moderately differentiated squamous cell carcinoma with cartilage, perineural, and vascular invasion. Metatarsal amputation and right inguinal lymph node dissection had been performed due to recurrence of the tumor. The patient was staged as grade 4 (T4N1MX) squamous cell carcinoma and received radiotherapy to the right
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Figure 1. Linear ulceration and satellite noduloulcerations in the right groin.
foot (64 Gy in 32 fractions) and inguinal area (60 Gy in 30 fractions) 5 days a week. Three months after the radiotherapy, the patient developed 1 to 3 cm necrotic ulcers and papulopustular lesions. The right leg appeared firm and swollen from ankle to groin (Figure 1, Figure 2, and Figure 3). A biopsy from the lesions revealed metastatic squamous cell carcinoma (Figure 4, Figure 5 and Figure 6). The patient was diagnosed as having in-transit metastasis of squamous cell carcinoma due to the locations of the lesions between the primary tumor and the closest regional lymph node. After consultation with the oncology department, chemotherapy could not be performed due to his general health and infection. The patient died after 2 months due to sepsis.
Dıscussıon
Figure 3. Multiple necrotic ulcerations on the right shin.
by the American Joint Committee on Cancer. They are defined as intralymphatic metastases occurring more than 2 cm from the primary tumor, whereas intralymphatic metastases occurring within 2 cm of the primary tumor are termed satellites.6,7 In-transit metastasis from CSCC was described in OTRs by Berg and Otley in 2002.14 In-transit metastasis of CSCC is independent from the primary tumor dermal and subcutanous metastatic foci that locate between the tumor and the closest lymph node. They usually present as 0.1 to 1.2 cm exophytic dermal and subcutanous papules that locate approximately 2.5 cm away from the primary tumor. The mean number of lesions was reported as 3.5.6 Carucci and colleagues reported that in-transit metastasis appears approximately 10 weeks later than the primary tumor or treatment of a recurrent tumor.6 In our case, the lesions of in-transit
In-transit metastases have been commonly described for malignant melanoma and are classified as stage 3 disease
Figure 2. Firm papules and pustules beyond a large ulceration on the right thigh.
168
Figure 4. Ulceration on part of the epidermis and solid islands of atypical squamoid cells in the dermis (hematoxylin-eosin stain; 340 original magnification).
Canadian Dermatology Association | Journal of Cutaneous Medicine and Surgery, Vol 19, No 2 (March/April), 2015: pp 167–170
In-Transit Metastasis from Primary CSCC
Figure 5. Groups of poorly differentiated atypical squamoid cells and mitotic figures in the dermis (shown by black arrows) (hematoxylineosin stain; 3400 original magnification).
metastasis started 90 cm away and 6 months later from the primary lesion and spread rapidly to the whole leg, which resulted in numerous lesions. The mean age of patients with in-transit metastasis is 61. Men are more commonly affected than women. There were no patients reported in the literature with Fitzpatrick skin type 4, 5, or 6.6 Our patient’s age was 59, and he had Fitzpatrick skin type 3. The risk of development of in-transit metastasis is higher in patients with high-risk squamous cell carcinoma.6,8,15 High-risk CSCC is associated with features such as the lip, ear, forehead, scalp, and temple locations; size greater than
Figure 6. Islands of P63-stained atypical squamoid cells in the dermis (3 200 original magnification).
2 cm in diameter; thickness greater than 2 mm; Clark level 4 or more; perineural, lymphatic, or vascular invasion; poorly differentiated or undifferentiated; certain histologic types; occurrence in an immunosuppressed patient; human papillomavirus infection; recurrence; inadequate tumor resection; and expressions of certain tumor genes.1,2,6,8 Twenty-one patients with in-transit metastasis have been reported in a multicenter study, of whom 15 were immunosuppressed OTRs; one had chronic lymphocytic leukemia, whereas 5 were not immunosuppressed. The reason for in-transit metastasis was linked to the high-risk properties of the tumor in these five patients.6 In the study by Carucci and colleagues, primary tumors resulting in in-transit metastasis mostly derived from the forehead and scalp, whereas others were located on the nose, ear, temple, cheek, arm, shoulder, foot, and penis.6,15 In-transit metastases can also be seen in the umbilical region, which are defined as skin nodules developing from the dermal and subdermal lymphatics in the abdominal region prior to reaching the regional inguinal lymph nodes.16 Interestingly, histologic differentiation of primary tumor and in-transit metastasis has been reported to be mostly well differentiated in the literature, although poorly differentiated or undifferentiated tumors are classified as high-risk CSCC.1,6 In our case, primary tumor was moderately differentiated, whereas the histologic differentiation of in-transit metastasis was poor. In-transit metastasis invades the skin via lymphatic vessels and/or nerves.6,15 Dermal and subcutaneous tumoral infiltration without epidermal invasion is the histopathologic finding of metastasis.6 Lymphedema can also be a risk factor for in-transit metastasis by obstructing lymphadenopathy, which ends with a delay in lymphatic return and results in increased extravasation of tumor cells within the lymphedematous limb.8 Although in-transit metastasis from primary CSCC appears more common in OTRs than in nontransplant patients,6 our case was not associated with immunosuppression. But we believe that high-risk features such as tumor size larger than 2 cm, perivascular and perineural invasion, and a history of inadequate resection might result in the occurrence of in-transit metastasis. Even though primary tumors that resulted in-transit metastasis have been reported to be located in the head and scalp region, in our case, the primary tumor was localized to the foot. Lymphedema occurring after inguinal lymph node dissection resulted in a swollen limb and, we believe, accelerated the progression of the metastasis.
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Treatment choices for in-transit metastasis are Mohs surgery or excision surgery, radiotherapy, excision followed by radiotherapy, amputation, intralesional or systemic chemotherapy (cis-platinum, 5-fluorouracil [5FU], bleomycin, and methotrexate), oral retinoids (13-cisretinoic acid) immunotherapy (interferon-2a), reduction of immunosuppressive medication, and anti–epidermal growth factor receptor (EGFR) agents.6,8,15 The recurrent tumor in our case was treated with surgery plus radiotherapy, but the patient’s health condition and the presence of infection did not allow the use of systemic therapy. The patient died because of sepsis after 2 months. The prognosis of in-transit metastasis is poor, especially in organ transplant patients. The 3-year diseasespecific survival in OTRs with metastatic skin cancer is reported to be 56%.17 The presented case died approximately 1 year after the diagnosis of primary CSCC.
Conclusion Even though it is mostly reported in association with malignant melanoma, in-transit metastasis can also occur in CSCC. Once it has occurred, the prognosis is unfavorable.
Acknowledgment Financial disclosure of authors and reviewers: None reported.
References 1. Nun˜o-Gonza´lez A, Vicente-Martı´n FJ, Pinedo-Moraleda F, Lo´pezEstebaranz JL. High-risk cutaneous squamous cell carcinoma. Actas Dermosifiliogr 2012;103:567–78, doi:10.1016/j.ad.2011.09.005. 2. Martorell-Calatayud A, Sanmartı´n Jimenez O, Cruz Mojarrieta J, Guille´n Barona C. Cutaneous squamous cell carcinoma: defining the high-risk variant. Actas Dermosifiliogr 2013;104:367–79, doi: 10.1016/j.ad.2011.12.019. 3. Karia PS, Han J, Schmults CD. Cutaneous squamous cell carcinoma: estimated incidence of disease, nodal metastasis, and deaths from disease in the United States. J Am Acad Dermatol 2012;68:957–66, doi:10.1016/j.jaad.2012.11.037.
170
4. Lindelo¨f B, Dal H, Wolk K, Malmborg N. Cutaneous squamous cell carcinoma in organ transplant recipients: a study of the Swedish cohort with regard to tumor site. Arch Dermatol 2005; 141:447–51, doi:10.1001/archderm.141.4.447. 5. Rowe DE, Carroll RJ, Day CL. Prognostic factors for local recurrence, metastasis, and survival rates in squamous cell carcinoma of the skin, ear, and lip. J Am Acad Dermatol 1992;26:976–90, doi:10.1016/01909622(92)70144-5. 6. Carucci JA, Martinez JC, Zeitouni NC, et al. In-transit metastasis from primary cutaneous squamous cell carcinoma in organ transplant recipients and nonimmunosuppressed patients: clinical characteristics, management, and outcome in a series of 21 patients. Dermatol Surg 2004;30:651, doi:10.1111/j.1524-4725.2004.30151.x. 7. Hayes AJ, Clark MA, Harries M, Thomas JM. Management of intransit metastases from cutaneous malignant melanoma. Br J Surg 2004;91:673–82, doi:10.1002/bjs.4610. 8. Wain EM, Webber NK, Stefanato CM, et al. Multiple in-transit cutaneous metastases from a primary cutaneous squamous cell carcinoma. Clin Exp Dermatol 2009;34:522–4, doi:10.1111/j.13652230.2008.02967.x. 9. Khan MK, Powell S, Cox N, et al. Cervical in-transit metastasis from a truncal basal cell carcinoma. BMJ Case Rep 2010 Jul 21. DOI: 10.1136/bcr.09.2009.2281. 10. Zeitouni NC, Giordano CN, Kane JM 3rd. In-transit Merkel cell carcinoma treated with isolated limb perfusion or isolated limb infusion: a case series of 12 patients. Dermatol Surg 2011;37:357– 64, doi:10.1111/j.1524-4725.2011.01883.x. 11. Fujimura T, Sugawara M, Haga T, et al. Malignant fibrous histiocytoma with in-transit metastasis. Case Rep Dermatol 2011;3: 164–9, doi:10.1159/000331324. 12. Homma E, Hata H, Aoyagi S, Shimizu H. Primary mucinous carcinoma of the skin with in-transit metastasis. J Eur Acad Dermatol Venereol 2014 Apr 22. [Epub ahead of print]. 13. Snow SN, Reizner GT. Eccrine porocarcinoma of the face. J Am Acad Dermatol 1992;27(2 Pt 2):306–11, doi:10.1016/0190-9622 (92)70187-K. 14. Berg D, Otley CC. Skin cancer in organ transplant recipients: epidemiology, pathogenesis, and management. J Am Acad Dermatol 2002;47:1–17, doi:10.1067/mjd.2002.125579. 15. Padmavathy L, Rao LL, Sylvester, et al. In-transit metastases from squamous cell carcinoma penis. Indian J Dermatol 2012;57:291–3, doi:10.4103/0019-5154.97674. 16. Macripo` G, Caliendo V, Grassi M, et al. Squamous cell carcinoma of the umbilicus: management of an unusual localization. Tumori 2011;97:236–8. 17. Martinez JC, Otley CC, Stasko T, et al. Defining the clinical course of metastatic skin cancer in organ transplant recipients: a multicenter collaborative study. Arch Dermatol 2003;139:301–6, doi:10.1001/archderm.139.3.301.
Canadian Dermatology Association | Journal of Cutaneous Medicine and Surgery, Vol 19, No 2 (March/April), 2015: pp 167–170
In-Transit Metastasis from Primary Cutaneous Squamous Cell Carcinoma in a Nonimmunosuppressed Patient ¨ lku¨men, Utkan Kızıltac¸, Tu¨lin Yu¨ksel, Ays¸e Seza Kunter, and Selma S¸engiz Erhan Emek Kocatu¨rk, Pelin Kuteyla U Background: In-transit metastases are dermal and subcutanous metastatic foci located between the tumor and the closest regional lymph node. Although in-transit metastasis has been commonly described for malignant melanoma, there have been some reports of in-transit metastases arising from primary cutaneous malignancies. The risk of development of in-transit metastases is higher in patients with high-risk squamous cell carcinoma. Case Report: We present a case of in-transit metastasis in a nonimmunosuppressed patient with a primary cutaneous squamous cell carcinoma. Contexte: Les me´tastases en transit sont des foyers me´tastatiques dermiques ou sous-cutane´s, situe´s entre la tumeur et le nœud lymphoı¨de re´gional le plus pre`s. Les me´tastases en transit sont souvent de´crites en lien avec les me´lanomes, mais des rapports font aussi e´tat de me´tastases en transit, issues de tumeurs malignes cutane´es primitives. Le risque de me´tastases en transit est plus e´leve´ chez les patients atteints d’un carcinome squameux a` risque e´leve´. Expose´ de cas: Sera expose´ ici un cas me´tastase en transit chez un patient non immunode´prime´, atteint d’un carcinome squameux primitif de la peau.
UTANEOUS SQUAMOUS CELL CARCINOMA (CSCC) is the second most common nonmelanoma skin cancer, with a lifetime incidence between 7 and 11%, and the frequency of incidence is increasing.1–3 There is a 100-fold increased risk of CSCC in organ transplant recipients (OTRs), and the sites of distribution of primary tumors do not change in immunosuppressed patients.4 The percentage of local and distant metastasis of CSCC is reported to be around 5%; however, the percentage increases up to 15 to 38% in cases of high-risk squamous cell carcinoma.1 In immunosuppressed patients, the metastatic rate of CSCC is reported as 12.9%, twice the rate of nonimmunosuppressed patients.5 Even though the prognosis is favorable in general, approximately 1.5% of cases are reported to die from the disease.3 In-transit metastases are rare and present as dermal and subcutaneous metastatic foci located between the tumor and the closest regional lymph node.6 Although in-transit
C
From the Departments of Dermatology and Pathology, Okmeydanı Training and Research Hospital, Istanbul, Turkey. Address reprint requests to: Emek Kocatu¨rk, MD, Department of Dermatology, Okmeydanı Training and Research Hospital, Nadiraga Sok. No: 25/9 Go¨ztepe, 34730, Istanbul, Turkey; e-mail: [email protected].
DOI 10.2310/7750.2014.14047 # 2014 Canadian Dermatology Association
metastasis has been commonly described for malignant melanoma, there have been some reports of in-transit metastases arising from cutaneous malignancies such as squamous cell carcinoma, basal cell carcinoma, Merkel cell carcinoma, malignant fibrous histiocytoma, primary mucinous carcinoma, and primary eccrine porocarcinoma.7–13 Recently, in-transit metastasis of primary CSCC in organ transplant recipients and nonimmunosuppressed patients has been reported in the literature.6 We present a case of in-transit metastasis in a nonimmunosuppressed patient with a primary CSCC.
Case Report A 59-year-old man presented to our dermatology clinic with painful, nonhealing ulcerations on the right leg and inguinal area. When the patient was asked about his history, we learned that a tumoral lesion on the fifth toe of the right foot had been amputated at the metatarsophalangeal joint level 6 months ago, and histopathologic examination of the specimen revealed a moderately differentiated squamous cell carcinoma with cartilage, perineural, and vascular invasion. Metatarsal amputation and right inguinal lymph node dissection had been performed due to recurrence of the tumor. The patient was staged as grade 4 (T4N1MX) squamous cell carcinoma and received radiotherapy to the right
Canadian Dermatology Association | Journal of Cutaneous Medicine and Surgery, Vol 19, No 2 (March/April), 2015: pp 167–170
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Figure 1. Linear ulceration and satellite noduloulcerations in the right groin.
foot (64 Gy in 32 fractions) and inguinal area (60 Gy in 30 fractions) 5 days a week. Three months after the radiotherapy, the patient developed 1 to 3 cm necrotic ulcers and papulopustular lesions. The right leg appeared firm and swollen from ankle to groin (Figure 1, Figure 2, and Figure 3). A biopsy from the lesions revealed metastatic squamous cell carcinoma (Figure 4, Figure 5 and Figure 6). The patient was diagnosed as having in-transit metastasis of squamous cell carcinoma due to the locations of the lesions between the primary tumor and the closest regional lymph node. After consultation with the oncology department, chemotherapy could not be performed due to his general health and infection. The patient died after 2 months due to sepsis.
Dıscussıon
Figure 3. Multiple necrotic ulcerations on the right shin.
by the American Joint Committee on Cancer. They are defined as intralymphatic metastases occurring more than 2 cm from the primary tumor, whereas intralymphatic metastases occurring within 2 cm of the primary tumor are termed satellites.6,7 In-transit metastasis from CSCC was described in OTRs by Berg and Otley in 2002.14 In-transit metastasis of CSCC is independent from the primary tumor dermal and subcutanous metastatic foci that locate between the tumor and the closest lymph node. They usually present as 0.1 to 1.2 cm exophytic dermal and subcutanous papules that locate approximately 2.5 cm away from the primary tumor. The mean number of lesions was reported as 3.5.6 Carucci and colleagues reported that in-transit metastasis appears approximately 10 weeks later than the primary tumor or treatment of a recurrent tumor.6 In our case, the lesions of in-transit
In-transit metastases have been commonly described for malignant melanoma and are classified as stage 3 disease
Figure 2. Firm papules and pustules beyond a large ulceration on the right thigh.
168
Figure 4. Ulceration on part of the epidermis and solid islands of atypical squamoid cells in the dermis (hematoxylin-eosin stain; 340 original magnification).
Canadian Dermatology Association | Journal of Cutaneous Medicine and Surgery, Vol 19, No 2 (March/April), 2015: pp 167–170
In-Transit Metastasis from Primary CSCC
Figure 5. Groups of poorly differentiated atypical squamoid cells and mitotic figures in the dermis (shown by black arrows) (hematoxylineosin stain; 3400 original magnification).
metastasis started 90 cm away and 6 months later from the primary lesion and spread rapidly to the whole leg, which resulted in numerous lesions. The mean age of patients with in-transit metastasis is 61. Men are more commonly affected than women. There were no patients reported in the literature with Fitzpatrick skin type 4, 5, or 6.6 Our patient’s age was 59, and he had Fitzpatrick skin type 3. The risk of development of in-transit metastasis is higher in patients with high-risk squamous cell carcinoma.6,8,15 High-risk CSCC is associated with features such as the lip, ear, forehead, scalp, and temple locations; size greater than
Figure 6. Islands of P63-stained atypical squamoid cells in the dermis (3 200 original magnification).
2 cm in diameter; thickness greater than 2 mm; Clark level 4 or more; perineural, lymphatic, or vascular invasion; poorly differentiated or undifferentiated; certain histologic types; occurrence in an immunosuppressed patient; human papillomavirus infection; recurrence; inadequate tumor resection; and expressions of certain tumor genes.1,2,6,8 Twenty-one patients with in-transit metastasis have been reported in a multicenter study, of whom 15 were immunosuppressed OTRs; one had chronic lymphocytic leukemia, whereas 5 were not immunosuppressed. The reason for in-transit metastasis was linked to the high-risk properties of the tumor in these five patients.6 In the study by Carucci and colleagues, primary tumors resulting in in-transit metastasis mostly derived from the forehead and scalp, whereas others were located on the nose, ear, temple, cheek, arm, shoulder, foot, and penis.6,15 In-transit metastases can also be seen in the umbilical region, which are defined as skin nodules developing from the dermal and subdermal lymphatics in the abdominal region prior to reaching the regional inguinal lymph nodes.16 Interestingly, histologic differentiation of primary tumor and in-transit metastasis has been reported to be mostly well differentiated in the literature, although poorly differentiated or undifferentiated tumors are classified as high-risk CSCC.1,6 In our case, primary tumor was moderately differentiated, whereas the histologic differentiation of in-transit metastasis was poor. In-transit metastasis invades the skin via lymphatic vessels and/or nerves.6,15 Dermal and subcutaneous tumoral infiltration without epidermal invasion is the histopathologic finding of metastasis.6 Lymphedema can also be a risk factor for in-transit metastasis by obstructing lymphadenopathy, which ends with a delay in lymphatic return and results in increased extravasation of tumor cells within the lymphedematous limb.8 Although in-transit metastasis from primary CSCC appears more common in OTRs than in nontransplant patients,6 our case was not associated with immunosuppression. But we believe that high-risk features such as tumor size larger than 2 cm, perivascular and perineural invasion, and a history of inadequate resection might result in the occurrence of in-transit metastasis. Even though primary tumors that resulted in-transit metastasis have been reported to be located in the head and scalp region, in our case, the primary tumor was localized to the foot. Lymphedema occurring after inguinal lymph node dissection resulted in a swollen limb and, we believe, accelerated the progression of the metastasis.
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Treatment choices for in-transit metastasis are Mohs surgery or excision surgery, radiotherapy, excision followed by radiotherapy, amputation, intralesional or systemic chemotherapy (cis-platinum, 5-fluorouracil [5FU], bleomycin, and methotrexate), oral retinoids (13-cisretinoic acid) immunotherapy (interferon-2a), reduction of immunosuppressive medication, and anti–epidermal growth factor receptor (EGFR) agents.6,8,15 The recurrent tumor in our case was treated with surgery plus radiotherapy, but the patient’s health condition and the presence of infection did not allow the use of systemic therapy. The patient died because of sepsis after 2 months. The prognosis of in-transit metastasis is poor, especially in organ transplant patients. The 3-year diseasespecific survival in OTRs with metastatic skin cancer is reported to be 56%.17 The presented case died approximately 1 year after the diagnosis of primary CSCC.
Conclusion Even though it is mostly reported in association with malignant melanoma, in-transit metastasis can also occur in CSCC. Once it has occurred, the prognosis is unfavorable.
Acknowledgment Financial disclosure of authors and reviewers: None reported.
References 1. Nun˜o-Gonza´lez A, Vicente-Martı´n FJ, Pinedo-Moraleda F, Lo´pezEstebaranz JL. High-risk cutaneous squamous cell carcinoma. Actas Dermosifiliogr 2012;103:567–78, doi:10.1016/j.ad.2011.09.005. 2. Martorell-Calatayud A, Sanmartı´n Jimenez O, Cruz Mojarrieta J, Guille´n Barona C. Cutaneous squamous cell carcinoma: defining the high-risk variant. Actas Dermosifiliogr 2013;104:367–79, doi: 10.1016/j.ad.2011.12.019. 3. Karia PS, Han J, Schmults CD. Cutaneous squamous cell carcinoma: estimated incidence of disease, nodal metastasis, and deaths from disease in the United States. J Am Acad Dermatol 2012;68:957–66, doi:10.1016/j.jaad.2012.11.037.
170
4. Lindelo¨f B, Dal H, Wolk K, Malmborg N. Cutaneous squamous cell carcinoma in organ transplant recipients: a study of the Swedish cohort with regard to tumor site. Arch Dermatol 2005; 141:447–51, doi:10.1001/archderm.141.4.447. 5. Rowe DE, Carroll RJ, Day CL. Prognostic factors for local recurrence, metastasis, and survival rates in squamous cell carcinoma of the skin, ear, and lip. J Am Acad Dermatol 1992;26:976–90, doi:10.1016/01909622(92)70144-5. 6. Carucci JA, Martinez JC, Zeitouni NC, et al. In-transit metastasis from primary cutaneous squamous cell carcinoma in organ transplant recipients and nonimmunosuppressed patients: clinical characteristics, management, and outcome in a series of 21 patients. Dermatol Surg 2004;30:651, doi:10.1111/j.1524-4725.2004.30151.x. 7. Hayes AJ, Clark MA, Harries M, Thomas JM. Management of intransit metastases from cutaneous malignant melanoma. Br J Surg 2004;91:673–82, doi:10.1002/bjs.4610. 8. Wain EM, Webber NK, Stefanato CM, et al. Multiple in-transit cutaneous metastases from a primary cutaneous squamous cell carcinoma. Clin Exp Dermatol 2009;34:522–4, doi:10.1111/j.13652230.2008.02967.x. 9. Khan MK, Powell S, Cox N, et al. Cervical in-transit metastasis from a truncal basal cell carcinoma. BMJ Case Rep 2010 Jul 21. DOI: 10.1136/bcr.09.2009.2281. 10. Zeitouni NC, Giordano CN, Kane JM 3rd. In-transit Merkel cell carcinoma treated with isolated limb perfusion or isolated limb infusion: a case series of 12 patients. Dermatol Surg 2011;37:357– 64, doi:10.1111/j.1524-4725.2011.01883.x. 11. Fujimura T, Sugawara M, Haga T, et al. Malignant fibrous histiocytoma with in-transit metastasis. Case Rep Dermatol 2011;3: 164–9, doi:10.1159/000331324. 12. Homma E, Hata H, Aoyagi S, Shimizu H. Primary mucinous carcinoma of the skin with in-transit metastasis. J Eur Acad Dermatol Venereol 2014 Apr 22. [Epub ahead of print]. 13. Snow SN, Reizner GT. Eccrine porocarcinoma of the face. J Am Acad Dermatol 1992;27(2 Pt 2):306–11, doi:10.1016/0190-9622 (92)70187-K. 14. Berg D, Otley CC. Skin cancer in organ transplant recipients: epidemiology, pathogenesis, and management. J Am Acad Dermatol 2002;47:1–17, doi:10.1067/mjd.2002.125579. 15. Padmavathy L, Rao LL, Sylvester, et al. In-transit metastases from squamous cell carcinoma penis. Indian J Dermatol 2012;57:291–3, doi:10.4103/0019-5154.97674. 16. Macripo` G, Caliendo V, Grassi M, et al. Squamous cell carcinoma of the umbilicus: management of an unusual localization. Tumori 2011;97:236–8. 17. Martinez JC, Otley CC, Stasko T, et al. Defining the clinical course of metastatic skin cancer in organ transplant recipients: a multicenter collaborative study. Arch Dermatol 2003;139:301–6, doi:10.1001/archderm.139.3.301.
Canadian Dermatology Association | Journal of Cutaneous Medicine and Surgery, Vol 19, No 2 (March/April), 2015: pp 167–170
