Radiation-induced angiosarcoma: case report

Lucas Aguiar Alencar de Oliveira Antonio Fortes de Pádua Filho Maria Adélia Medeiros e Melo Elisa Rosa de Carvalho Gonçalves Nunes Galvão Mharcus Carneiro Vieira Jerúsia Oliveira Ibiapina Danilo Rafael da Silva Fontinele Sabas Carlos Vieira About the authors

ABSTRACT

Angiosarcoma of the breast accounts for less than 1% of breast tumors. This tumor may be primary or secondary to previous radiation therapy and it is also named “radiogenic angiosarcoma of the breast”, which is still a rare entity with a poor prognosis. So far, there are only 307 cases reported about these tumors in the literature. We present a case of a 73-year-old woman with a prior history of breast-conserving treatment of right breast cancer, exhibiting mild pinkish skin changes in the ipsilateral breast. Her mammography was consistent with benign alterations (BI-RADS 2). On incisional biopsy specimens, hematoxylin-eosin showed atypical vascular lesion and suggested immunohistochemisty for diagnostic elucidation. Resection of the lesions was performed and histology showed radiogenic angiosarcoma. The patient underwent simple mastectomy. Immunohistochemistry was positive for antigens related to CD31 and CD34, and C-MYC oncogene amplification, confirming the diagnosis of angiosarcoma induced by breast irradiation. A delayed diagnosis is an important concern. Initial skin changes in radiogenic angiosarcoma are subtle, therefore, these alterations may be confused with other benign skin conditions such as telangiectasia. We highlight this case clinical aspects with the intention of alerting to the possibility of angiosarcoma of the breast in patients with a previous history of adjuvant radiation therapy for breast cancer treatment. Sixteen months after the surgery the patient remains asymptomatic.

Keywords:
Hemangiosarcoma; Breast neoplasms/radiotherapy; Mastectomy

RESUMO

Os angiossarcomas de mama representam menos de 1% dos tumores da mama e podem ser primários ou secundários à radioterapia prévia. Tais tumores são chamados de “angiossarcomas radiogênicos da mama” e representam uma entidade mais rara ainda e de prognóstico ruim. Atualmente, na literatura, são encontrados apenas 307 casos desses tumores. Relatamos o caso de uma mulher de 73 anos, com história prévia de tratamento conservador de câncer de mama direita, apresentando alteração rósea discreta em pele da mama homolateral. A mamografia demostrou resultado compatível com alterações benignas (BI-RADS 2). No material de biópsia incisional, a hematoxilina-eosina demonstrou lesão vascular atípica e sugeriu imuno-histoquímica para elucidação diagnóstica. A paciente foi submetida à ressecção de lesões, e a histologia demonstrou angiossarcoma radiogênico. Em seguida, mastectomia simples foi realizada. A imuno-histoquímica demonstrou positividade para os antígenos relacionados a CD31 e CD34, e a amplificação do oncogene C-MYC confirmou o diagnóstico de angiossarcoma induzido por radiação mamária. O atraso no diagnóstico constitui questão importante. Considerando que as alterações iniciais da pele do angiossarcoma radiogênico são sutis e podem ser confundidas com outras condições benignas da pele, como telangiectasias, neste relato destacamos os aspectos clínicos, no intuito de alertar sobre a possibilidade de angiossarcoma de mama em pacientes com história prévia de radioterapia adjuvante para tratamento de câncer de mama. A paciente permaneceu assintomática 16 meses após a cirurgia.

Descritores:
Hemangiossarcoma; Neoplasias da mama/radioterapia; Mastectomia

INTRODUCTION

Angiosarcoma of the breast accounts for less than 1% of breast tumors. It may be primary or secondary to previous radiation therapy and/or chronic lymphedema after breast cancer treatment.(11. Kamat L, Rosa M, Weinfurtner R, Drukteinis J, Falcon S, Patel B. Primary breast angiosarcoma in a male. Breast J. 2015;21(5):545-8.)

Secondary angiosarcoma of the breast is generally related to breast radiation therapy and is termed radiogenic angiosarcoma of the breast (RASB). The absolute risk of developing RASB is low, less than 0.5% and the relative risk of developing the condition is 15.9 in patients who received breast radiation therapy.(22. Huang J, Mackillop WJ. Increased risk of soft tissue sarcoma after radiotherapy in women with breast carcinoma. Cancer. 2001;92(1):172-80.)

Early alterations in RASB are subtle and may be confused with other benign skin conditions such as telangiectasia, which may not alert the physician to the diagnosis.

We present a case of RASB and discuss diagnostic and treatment aspects.

CASE REPORT

A Caucasian, 73-year-old woman sought the breast disorder division with the complaint of a pinkish skin change in her right breast for about 30 days. A bilateral mammogram had been performed five months previously, showing benign alterations ( Breast Imaging Reporting and Data System – BI-RADS™ 2). The patient had a personal history of a G3 invasive right breast carcinoma of no special type, treated with segmental resection and axillary lymph node dissection level I and II on December 2011. At the time of the operation, the tumor measured 3.0cm and three axillary lymph nodes had metastases (3/10). Immunohistochemistry showed that the tumor was estrogen receptor positive (90%), progesterone receptor positive (2%), HER-2 negative and Ki-67 positive (60%), luminal B subtype. Adjuvant therapy of the patient included six cycles of doxorubicin, cyclophosphamide and paclitaxel chemotherapy followed by radiation therapy (25 sessions with a 50Gy dose to the whole right breast and supraclavicular fossa, in addition to a 10Gy boost). She is currently undergoing endocrine therapy with letrozole (sixth year of treatment). On physical examination, the patient had two pinkish-violaceous lesions in the right breast, one that was mildly erythematous and almost imperceptible at the junction of the upper quadrants (UQJ) and another more intensely violet lesion at the junction of the lower quadrants (LQJ) measuring 0.5cm ( Figure 1 ).

Figure 1
Pinkish/violaceous lesions being one located at the junction of the upper quadrants (A) and another at the junction of the lower quadrants measuring 0.5cm (B)

An incisional biopsy of the lesion in the LQJ was performed and demonstrated an atypical vascular lesion on hematoxylin-eosin stain. A complementary immunohistochemical study was suggested for diagnostic conclusion. Due to this result, the patient underwent a wide resection of both cutaneous lesions. In the meantime, immunohistochemical study result revealed an angiosarcoma. Anatomic pathological report of the resected specimens showed a well-differentiated angiosarcoma (G1), a neoplasm characterized by anastomosing vascular ducts lined by atypical endothelial cells characterized by hyperchromatism and anisocariosis, sometimes containing red blood cells, arranged in an infiltrative growth pattern, permeating the mammary parenchyma and dermis ( Figure 2 ) at the UQJ measuring 1.9x1.4cm, and at the LQJ a neoplasm restricted to the dermis, measuring 1.1x0.5cm ( Figure 3 ).Immunohistochemical revealed positivity for the expression of cluster of differentiation 31 (CD31) and oncogene C-MYC (C-Myc), confirming malignancy secondary to radiation therapy ( Figure 4 ). Computed tomography of the chest and abdomen and bone scintigraphy showed no signs of distant metastases. The patient underwent a right simple mastectomy without reconstruction as complementary treatment. The final histopathology report showed a well-differentiated angiosarcoma (G1) and three more microscopic foci were found in the breast parenchyma, the largest measuring 2mm. Two years after surgery, the patient has no evidence of disease recurrence.

Figure 2
Pathological anatomy
Figure 3
Specimens obtained from skin lesions resected at the junction of the upper quadrants and junction of the lower quadrants of the right breast
Figure 4
Immunohistochemical study showing positivity for (A) cluster of differentiation 31, and (B) oncogene C-MYC

DISCUSSION

As opposed to primary angiosarcoma of the breast that affects young women, mean patient age at diagnosis of RASB was 70 years and the mean latency period between radiation therapy and diagnosis was 6 years.(33. Dogan A, Kern P, Schultheis B, Häusler G, Rezniczek GA, Tempfe CB. Radiogenic angiosarcoma of the breast: case report and systematic review of the literature. BMC Cancer. 2018;18(1):463. Review.) The pathogenesis of RASB is still unclear.(44. Shah S, Rosa M. Radiation-associated angiosarcoma of the breast: clinical and pathologic features. Arch Pathol Lab Med. 2016;140(5):477-81.)

The two largest published case series of RASB, one with 79 cases and another with 95 cases reported that the 5-year disease-free survival (DFS) was 47% and 62.6%, respectively.(55. Torres KE, Ravi V, Kin K, YI M, Guadagnolo BA, May CD, et al. Long-term outcomes in patients with radiation-associated angiosarcomas of the breast following surgery and radiotherapy for breast cancer. Ann Surg Oncol. 2013;20(4):1267-74.,66. D'Angelo SP, Antonescu CR, Kuk D, Quin L, Moraco N, Carvajal RC, et al. High-risk features in radiation-associated breast angiosarcomas. Br J Cancer. 2013;109(9):2340-6.)

However, RASB has a high local recurrence rate and metastasis is more common to the lungs and liver, occurring simultaneously or soon after local recurrences.(77. Alves I, Marques JC. Radiation-induced angiosarcoma of the breast: a retrospective analysis of 15 years' experience at an oncology center. Radiol Bras. 2018;51(5):281-6.)

Clinical manifestations of RASB are frequently described as small, violaceous skin lesions, which resemble telangiectasia. Nevertheless, nodules, plaques or patches may also appear.(33. Dogan A, Kern P, Schultheis B, Häusler G, Rezniczek GA, Tempfe CB. Radiogenic angiosarcoma of the breast: case report and systematic review of the literature. BMC Cancer. 2018;18(1):463. Review.)

Imaging of angiosarcoma is nonspecific. Mammography and ultrasonography have no pathognomonic features. Magnetic resonance imaging is considered the most promising imaging test for malignancy patterns.(88. Arora TK, Terracina KP, Soong J, Idowu MO, Takabe K. Primary and secondary angiosarcoma of the breast. Gland Surg. 2014;3(1):28-34. Review.)

Diagnosis of angiosarcoma is made by biopsy. Histological features of primary angiosarcoma of the breast RASB are indistinguishable, except for the more common cutaneous involvement in RASB, as well a higher proportion of less-differentiated epithelioid tumors.(88. Arora TK, Terracina KP, Soong J, Idowu MO, Takabe K. Primary and secondary angiosarcoma of the breast. Gland Surg. 2014;3(1):28-34. Review.,99. Bordoni D, Bolletta E, Falco G, Cadenelli P, Rocco N, Tessone A, et al. Primary angiosarcoma of the breast. Int J Surg Case Rep. 2016;20(Suppl):12-15.) To date, three main histopathologic grades have been described for angiosarcoma: low-grade or type 1 (G1), intermediate-grade or type 2 (G2) and high-grade or type 3 (G3).(11. Kamat L, Rosa M, Weinfurtner R, Drukteinis J, Falcon S, Patel B. Primary breast angiosarcoma in a male. Breast J. 2015;21(5):545-8.) D'Angelo et al.,(66. D'Angelo SP, Antonescu CR, Kuk D, Quin L, Moraco N, Carvajal RC, et al. High-risk features in radiation-associated breast angiosarcomas. Br J Cancer. 2013;109(9):2340-6.) have shown that tumor grade does not seem to have prognostic value and even low-grade lesions may metastasize. Espat et al.,(1010. Espat NJ, Lewis JJ, Woodruff JM, Antonescu C, Xia J, Leung D, et al. Confirmed angiosarcoma: prognostic factors and outcome in 50 prospectively followed patients. Sarcoma. 2000;4(4):173-7.) consider that all angiosarcomas associated with radiation are considered high-grade tumors. Thus, the tumor grade has no prognostic value in breast angiosarcomas.

On immunohistochemistry, angiosarcomas are positive for antigens related to CD31, CD34 and sometimes podoplanin for the diagnosis of less-differentiated tumors.(66. D'Angelo SP, Antonescu CR, Kuk D, Quin L, Moraco N, Carvajal RC, et al. High-risk features in radiation-associated breast angiosarcomas. Br J Cancer. 2013;109(9):2340-6.) Laé et al.,(1111. Laé M, Lebel A, Hamel-Viard F, Asselain B, Trassard M, Sastre X, et al. Can c-myc amplification reliably discriminate postradiation from primary angiosarcoma of the breast? Cancer Radiother. 2015;19(3):168-74.) found a 5-to 20-fold amplification of the C-MYC in all angiosarcomas induced by breast irradiation. These data may provide a basis for additional targeted therapy.(1111. Laé M, Lebel A, Hamel-Viard F, Asselain B, Trassard M, Sastre X, et al. Can c-myc amplification reliably discriminate postradiation from primary angiosarcoma of the breast? Cancer Radiother. 2015;19(3):168-74.) The expression and amplification of c-MYC in RASB is also important in the differential diagnosis of benign lesions named atypical vascular lesions. Positivity of antigens related to CD31 and CD34 confirms the diagnosis of angiosarcoma and expression and amplification of cC-MYC are shown in RASB.(33. Dogan A, Kern P, Schultheis B, Häusler G, Rezniczek GA, Tempfe CB. Radiogenic angiosarcoma of the breast: case report and systematic review of the literature. BMC Cancer. 2018;18(1):463. Review.)

From the molecular point of view, it is assumed that point mutations in BRCA2 are causes of some secondary angiosarcomas of the breast. The loss of function of BRCA mutated prevents to exert protection against radiation-induced DNA damage.(1212. Esposito E, Avino F, di Giacomo R, Donzelli I, Marone U, Melucci MT, et al. Angiosarcoma of the breast, the unknown-a review of the current literature. Transl Cancer Res. 2019;8(Suppl. 5):S510-7.) West et al.,(1313. West JG, Weitzel JN, Tao ML, Carpenter M, West JE, Fanning C. BRCA mutations and the risk of angiosarcoma after breast cancer treatment. Clin Breast Cancer. 2008;8(6):533-7.) presented a case report in which a patient with BRCA2 who developed chest wall angiosarcoma after mastectomy. Later, Kadouri et al.,(1414. Kadouri L, Sagi M, Goldberg Y, Lerer I, Hamburger T, Peretz T. Genetic predisposition to radiation induced sarcoma: possible role for BRCA and p53 mutations. Breast Cancer Res Treat. 2013;140(1):207-11.) reported the genetic evaluation of three cases of secondary breast angiosarcoma, two BRCA1 and one with BRCA2 and one without. They estimated an approximately twice as high risk of angiosarcoma in patients with BRCA1/2. However, this risk should not be considered in the irradiation treatment of this mutated population.(1212. Esposito E, Avino F, di Giacomo R, Donzelli I, Marone U, Melucci MT, et al. Angiosarcoma of the breast, the unknown-a review of the current literature. Transl Cancer Res. 2019;8(Suppl. 5):S510-7.)

There is no gold standard for surgical treatment of angiosarcoma. A wide local resection or mastectomy is the most commonly performed treatment. Simple mastectomy is the surgery of choice. It is debatable whether axillary dissection is required, since nodal involvement is uncommon.(55. Torres KE, Ravi V, Kin K, YI M, Guadagnolo BA, May CD, et al. Long-term outcomes in patients with radiation-associated angiosarcomas of the breast following surgery and radiotherapy for breast cancer. Ann Surg Oncol. 2013;20(4):1267-74.)

In general, chemotherapy regimen is chosen empirically due to the rarity of the disease and lack of definite standardized treatment. Some studies(55. Torres KE, Ravi V, Kin K, YI M, Guadagnolo BA, May CD, et al. Long-term outcomes in patients with radiation-associated angiosarcomas of the breast following surgery and radiotherapy for breast cancer. Ann Surg Oncol. 2013;20(4):1267-74.,99. Bordoni D, Bolletta E, Falco G, Cadenelli P, Rocco N, Tessone A, et al. Primary angiosarcoma of the breast. Int J Surg Case Rep. 2016;20(Suppl):12-15.) have suggested that treatment with anthracyclin-based chemotherapy, with either doxorubicin, or epirubicin with ifosfamide may improve both disease-free DFS and overall survival (OS). Systemic chemotherapy and re-irradiation are indicated only in RASB patients with local and/or systemic recurrences.(33. Dogan A, Kern P, Schultheis B, Häusler G, Rezniczek GA, Tempfe CB. Radiogenic angiosarcoma of the breast: case report and systematic review of the literature. BMC Cancer. 2018;18(1):463. Review.)

Table 1 present case report studies and case series (up to 10 cases) on radiation-induced breast angiosarcoma after treatment for breast cancer from the last five years (2015-2020) indexed in PubMed.gov .

Table 1
Radiation-induced breast angiosarcoma after treatment for breast cancer(1515. Abbenante D, Malosso M, Raone B. Radiation-induced cutaneous angiosarcoma of the breast. Am J Med. 2020;33(10):1156-7.

16. Shiraki E, Kang Y, Shibayama T, Tsuyuki S. Two cases of breast angiosarcoma after breast conserving surgery. Surg Case Rep. 2020;6(1):81.

17. Jayarajah U, Nagodavithane K, Basnayake O, Seneviratne S. Unusual Presentation of Bilateral Radiation-Induced Angiosarcoma of the Breast. Case Rep Oncol Med. 2020;5768438. doi: 10.1155/2020/5768438.
https://doi.org/10.1155/2020/5768438...

18. Lewcun JA, Pameijer C, Kass R, Cream L, Hershock D, Brooks AJ, et al. Dodge DG. Doxorubicin, paclitaxel, and cisplatin based chemotherapy for the treatment of angiosarcoma: two case reports. Int J Surg Case Rep. 2020;68:83-7.

19. Kong J, Shahait AD, Kim S, Choi L. Radiation-induced undifferentiated pleomorphic sarcoma of the breast. BMJ Case Rep. 2020;13(2): e232616.

20. Suzuki Y, Taniguchi K, Hatono M, Kajiwara Y, Abe Y, Kawada K, et al. Recurring radiation-induced angiosarcoma of the breast that was treated with paclitaxel chemotherapy: a case report. Surg Case Rep. 2020;6(1):25.

21. Amajoud Z, Vertongen AS, Weytens R, Hauspy J. Radiation induced angiosarcoma of the breast: case series and review of the literature. Facts Views Vis Obgyn. 2018;10(4):215-20.

22. Lee H, MacDonald SM. Multifocal angiosarcoma secondary to partial breast irradiation: reirradiate? Int J Radiat Oncol Biol Phys. 2019:105(1):17-18.

23. Verdura V, Di Pace B, Concilio M, Guastafierro A, Fiorillo G, Alfano L, et al. A new case of radiation-induced breast angiosarcoma. Int J Surg Case Rep. 2019;60:152-5.

24. Tsapralis N, Vlachogiorgos A, Pham H, Mowatt D. Nothing is impossible: radiation induced angiosarcoma of breast in a male patient. J Surg Case Rep. 2019;2019(5):rjz158.

25. Wei NJ, Crowley TP, Ragbir M. Early breast angiosarcoma development after radiotherapy. Ann Plast Surg. 2019;83(2):152-3.

26. García Novoa A, Acea Nebril B, Bouzón Alejandro A, Cereijo Garea C, Antolín Novoa S. Radiation-induced angiosarcoma of the breast in a Li-Fraumeni patient. Cir Esp. 2019;97(2):114-6.

27. Bonzano E, Guenzi M, Corvò R. Salvage hypofractionated radiotherapy in a progressive radiation-induced angiosarcoma: a case report. Cureus. 2017;9(11):e1886.

28. Farran Y, Padilla O, Chambers K, Philipovskiy A, Nahleh Z. Atypical Presentation of Radiation-Associated Breast Angiosarcoma: a case report and review of literature. Am J Case Rep. 2017;18:1347-50.

29. Disharoon M, Kozlowski KF, Kaniowski JM. Case 242: radiation-induced angiosarcoma. Radiology. 2017;283(3):909-16.

30. Plichta JK, Hughes K. Radiation-Induced angiosarcoma after breast-cancer treatment. N Engl J Med. 2017;376(4):367.

31. Tato-Varela S, Albalat-Fernández R, Pabón-Fernández S, Núñez-García D, Calle-Marcos M. Radiation-induced breast angiosarcoma: a case report. Ecancermedicalscience. 2016;10:697.

32. Wronski K, Frackowiak L. Angiosarcoma following radiation therapy for breast cancer case report. Ann Ital Chir. 2016;5:S2239253X16025032.

33. Wilhelm IN, Penman EJ. Radiation associated angiosarcoma: case series from a community cancer center and review of the literature. Del Med J. 2016;88(3):78-82.

34. Mocerino C, Iannaci G, Sapere P, Luise R, Canonico S, Gambardella A. Multidisciplinary approach to breast angiosarcoma in an elderly patient: Repeated local relapses and significant objective responses. Int J Immunopathol Pharmacol. 2016;29(3):537-42.

35. Peterson CB, Beauregard S. Radiation-induced breast angiosarcoma: case report and clinical approach. J Cutan Med Surg. 2016;20(4):304-7.

36. Tidwell WJ, Haq J, Kozlowski KF, Googe PB. C-MYC positive angiosarcoma of skin and breast following MammoSite®treatment. Dermatol Online J. 2015;21(10):13030 /qt4t65q9nc.

37. Uryvaev A, Moskovitz M, Abdach-Bortnyak R, Hershkovitz D, Fried G. Post-irradiation angiosarcoma of the breast: clinical presentation and outcome in a series of six cases. Breast Cancer Res Treat. 2015;153(1):3-8.

38. Parvez E, Popovic S, Elavathil L, Okawara G, Hodgson N. Early occurrence of angiosarcoma in a woman with a brca2 gene variation of unknown significance treated with breast-conserving therapy for bilateral ductal carcinoma: a case report. Clin Breast Cancer. 2015;15(6):536-8.
-3939. Styring E, Klasson S, Rydholm A, Vult von Steyern F. Radiation-associated angiosarcoma after breast cancer: Improved survival by excision of all irradiated skin and soft tissue of the thoracic wall? A report of six patients. Acta Oncol. 2015;54(7):1078-80.)

CONCLUSION

Radiogenic angiosarcoma of the breast is a rare and late complication of breast irradiation. Alterations may be confused with other benign skin conditions such as telangiectasia. The prognosis in women is poor. We presented a case to highlight clinical aspects and alert to the diagnostic possibility in patients with a previous history of adjuvant radiation therapy for breast cancer treatment.

REFERENCES

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    Dogan A, Kern P, Schultheis B, Häusler G, Rezniczek GA, Tempfe CB. Radiogenic angiosarcoma of the breast: case report and systematic review of the literature. BMC Cancer. 2018;18(1):463. Review.
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    Shah S, Rosa M. Radiation-associated angiosarcoma of the breast: clinical and pathologic features. Arch Pathol Lab Med. 2016;140(5):477-81.
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    Torres KE, Ravi V, Kin K, YI M, Guadagnolo BA, May CD, et al. Long-term outcomes in patients with radiation-associated angiosarcomas of the breast following surgery and radiotherapy for breast cancer. Ann Surg Oncol. 2013;20(4):1267-74.
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    D'Angelo SP, Antonescu CR, Kuk D, Quin L, Moraco N, Carvajal RC, et al. High-risk features in radiation-associated breast angiosarcomas. Br J Cancer. 2013;109(9):2340-6.
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    Alves I, Marques JC. Radiation-induced angiosarcoma of the breast: a retrospective analysis of 15 years' experience at an oncology center. Radiol Bras. 2018;51(5):281-6.
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    Arora TK, Terracina KP, Soong J, Idowu MO, Takabe K. Primary and secondary angiosarcoma of the breast. Gland Surg. 2014;3(1):28-34. Review.
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    Bordoni D, Bolletta E, Falco G, Cadenelli P, Rocco N, Tessone A, et al. Primary angiosarcoma of the breast. Int J Surg Case Rep. 2016;20(Suppl):12-15.
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    Espat NJ, Lewis JJ, Woodruff JM, Antonescu C, Xia J, Leung D, et al. Confirmed angiosarcoma: prognostic factors and outcome in 50 prospectively followed patients. Sarcoma. 2000;4(4):173-7.
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    Laé M, Lebel A, Hamel-Viard F, Asselain B, Trassard M, Sastre X, et al. Can c-myc amplification reliably discriminate postradiation from primary angiosarcoma of the breast? Cancer Radiother. 2015;19(3):168-74.
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    Esposito E, Avino F, di Giacomo R, Donzelli I, Marone U, Melucci MT, et al. Angiosarcoma of the breast, the unknown-a review of the current literature. Transl Cancer Res. 2019;8(Suppl. 5):S510-7.
  • 13
    West JG, Weitzel JN, Tao ML, Carpenter M, West JE, Fanning C. BRCA mutations and the risk of angiosarcoma after breast cancer treatment. Clin Breast Cancer. 2008;8(6):533-7.
  • 14
    Kadouri L, Sagi M, Goldberg Y, Lerer I, Hamburger T, Peretz T. Genetic predisposition to radiation induced sarcoma: possible role for BRCA and p53 mutations. Breast Cancer Res Treat. 2013;140(1):207-11.
  • 15
    Abbenante D, Malosso M, Raone B. Radiation-induced cutaneous angiosarcoma of the breast. Am J Med. 2020;33(10):1156-7.
  • 16
    Shiraki E, Kang Y, Shibayama T, Tsuyuki S. Two cases of breast angiosarcoma after breast conserving surgery. Surg Case Rep. 2020;6(1):81.
  • 17
    Jayarajah U, Nagodavithane K, Basnayake O, Seneviratne S. Unusual Presentation of Bilateral Radiation-Induced Angiosarcoma of the Breast. Case Rep Oncol Med. 2020;5768438. doi: 10.1155/2020/5768438.
    » https://doi.org/10.1155/2020/5768438
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    Lewcun JA, Pameijer C, Kass R, Cream L, Hershock D, Brooks AJ, et al. Dodge DG. Doxorubicin, paclitaxel, and cisplatin based chemotherapy for the treatment of angiosarcoma: two case reports. Int J Surg Case Rep. 2020;68:83-7.
  • 19
    Kong J, Shahait AD, Kim S, Choi L. Radiation-induced undifferentiated pleomorphic sarcoma of the breast. BMJ Case Rep. 2020;13(2): e232616.
  • 20
    Suzuki Y, Taniguchi K, Hatono M, Kajiwara Y, Abe Y, Kawada K, et al. Recurring radiation-induced angiosarcoma of the breast that was treated with paclitaxel chemotherapy: a case report. Surg Case Rep. 2020;6(1):25.
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    Amajoud Z, Vertongen AS, Weytens R, Hauspy J. Radiation induced angiosarcoma of the breast: case series and review of the literature. Facts Views Vis Obgyn. 2018;10(4):215-20.
  • 22
    Lee H, MacDonald SM. Multifocal angiosarcoma secondary to partial breast irradiation: reirradiate? Int J Radiat Oncol Biol Phys. 2019:105(1):17-18.
  • 23
    Verdura V, Di Pace B, Concilio M, Guastafierro A, Fiorillo G, Alfano L, et al. A new case of radiation-induced breast angiosarcoma. Int J Surg Case Rep. 2019;60:152-5.
  • 24
    Tsapralis N, Vlachogiorgos A, Pham H, Mowatt D. Nothing is impossible: radiation induced angiosarcoma of breast in a male patient. J Surg Case Rep. 2019;2019(5):rjz158.
  • 25
    Wei NJ, Crowley TP, Ragbir M. Early breast angiosarcoma development after radiotherapy. Ann Plast Surg. 2019;83(2):152-3.
  • 26
    García Novoa A, Acea Nebril B, Bouzón Alejandro A, Cereijo Garea C, Antolín Novoa S. Radiation-induced angiosarcoma of the breast in a Li-Fraumeni patient. Cir Esp. 2019;97(2):114-6.
  • 27
    Bonzano E, Guenzi M, Corvò R. Salvage hypofractionated radiotherapy in a progressive radiation-induced angiosarcoma: a case report. Cureus. 2017;9(11):e1886.
  • 28
    Farran Y, Padilla O, Chambers K, Philipovskiy A, Nahleh Z. Atypical Presentation of Radiation-Associated Breast Angiosarcoma: a case report and review of literature. Am J Case Rep. 2017;18:1347-50.
  • 29
    Disharoon M, Kozlowski KF, Kaniowski JM. Case 242: radiation-induced angiosarcoma. Radiology. 2017;283(3):909-16.
  • 30
    Plichta JK, Hughes K. Radiation-Induced angiosarcoma after breast-cancer treatment. N Engl J Med. 2017;376(4):367.
  • 31
    Tato-Varela S, Albalat-Fernández R, Pabón-Fernández S, Núñez-García D, Calle-Marcos M. Radiation-induced breast angiosarcoma: a case report. Ecancermedicalscience. 2016;10:697.
  • 32
    Wronski K, Frackowiak L. Angiosarcoma following radiation therapy for breast cancer case report. Ann Ital Chir. 2016;5:S2239253X16025032.
  • 33
    Wilhelm IN, Penman EJ. Radiation associated angiosarcoma: case series from a community cancer center and review of the literature. Del Med J. 2016;88(3):78-82.
  • 34
    Mocerino C, Iannaci G, Sapere P, Luise R, Canonico S, Gambardella A. Multidisciplinary approach to breast angiosarcoma in an elderly patient: Repeated local relapses and significant objective responses. Int J Immunopathol Pharmacol. 2016;29(3):537-42.
  • 35
    Peterson CB, Beauregard S. Radiation-induced breast angiosarcoma: case report and clinical approach. J Cutan Med Surg. 2016;20(4):304-7.
  • 36
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Publication Dates

  • Publication in this collection
    07 Dec 2020
  • Date of issue
    2020

History

  • Received
    06 Oct 2019
  • Accepted
    12 June 2020
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