TOPICS

The “Shield Sign” in Two Men with Metastatic Salivary Duct Carcinoma to the Skin: Cutaneous Metastases Presenting as Carcinoma Hemorrhagiectoides

a–cPhilip R. Cohen, MD*; c,dVictor G. Prieto*; eSarina A. Piha-Paul, MD; eRazelle Kurzrock, MD

aThe University of Houston Health Center, University of Houston, Houston, Texas; bThe Department of Dermatology, University of Texas–Houston
Medical School, Houston, Texas; cThe Departments of Dermatology, dPathology, and eClinical Therapeutics (A Phase I Program),
The University of Texas MD Anderson Cancer Center, Houston, Texas

Disclosure: The authors report no relevant conflicts of interest. *PRC and VGP contributed equally to this article.

Abstract
Background: Salivary duct carcinoma is an infrequent and highly aggressive cancer that rarely metastasizes to the skin. Inflammatory cutaneous metastatic carcinoma is characterized by tumor cells predominantly in dermal lymphatics (carcinoma erysipelatoides) or blood vessels (carcinoma telangiectoides). Purpose: The authors present a distinctive cutaneous distribution of skin metastases from a visceral malignancy that resembles a medieval knight’s shield and introduce a third pattern of inflammatory cutaneous metastatic carcinoma—carcinoma hemorrhagiectoides—which has a distinctive clinical presentation and pathological correlation. Methods: The authors describe the clinical and pathological characteristics of an unusual pattern of cutaneous metastases in two men with rapidly progressive salivary duct carcinoma and summarize the relevant literature. Immunoperoxidase stains with antibodies to CD31 and D2-40 were used to define the endothelial-lined dermal vessels containing tumor metastases: lymph vessels (CD31+/D2-40+) and blood vessels (CD31+/D2-40-). Results: Salivary duct carcinoma-related cutaneous metastases presented as large, violaceous, confluent, hemorrhagic and erythematous, dermal plaques across the chest and from the neck to the abdomen, reminiscent of a medieval knight’s shield in two men. Microscopic examination demonstrated not only extensive infiltration of the dermis by tumor cells, but also tumor-containing endothelial-lined vessels: lymphatics (1 patient) or lymphatics and blood vessels (1 patient). Red blood cells were also noted in the tumor-filled lymph vessels of both patients. Conclusion: Salivary duct carcinoma with cutaneous metastases is rare (five patients) and the most common skin sites of metastatic tumor were the neck and chest. In addition to carcinoma erysipelatoides and carcinoma telangiectoides, inflammatory cutaneous metastatic carcinoma also includes carcinoma hemorrhagiectoides (with metastatic tumor cells in dermal lymphatics, blood vessels, or both) in which the skin metastases clinically appear as purpuric violaceous indurated plaques and microscopically demonstrates moderate-to-extensive extravascular tumor infiltration in the dermis and hemorrhage of red blood cells into endothelial-lined lymph vessels. The distinctive pattern of cutaneous metastases in the patients described in this article, resembling a medieval knight’s shield, has also been observed—albeit rarely—in patients with a primary malignancy of the parotid gland, thyroid, or unknown origin. Hence, the “shield sign” may be an uncommon presentation of tumors originating and/or metastasizing to the head and neck.  (J Clin Aesthet Dermatol. 2012;5(9):27–36.)

Salivary duct carcinoma—described initially by Kleinsasser et al in 1968—is an aggressive, usually androgen-receptor positive, adenocarcinoma with a historically poor prognosis that is most commonly associated with the parotid gland and less frequently originating from either the submandibular gland or minor salivary glands.[1–9] Pathologically and immunophenotypically, salivary duct carcinoma resembles high-grade ductal breast adeno-carcinoma: both tumors typically demonstrate positive immunoreactivity for androgen receptor, carcinoembryonic antigen, gross cystic disease fluid protein, and occasionally human epidermal growth factor receptor 2 (HER2/neu) over expression.[1,2,6,7,10,11] Although invasive ductal carcinoma of the breast is commonly estrogen-receptor and progesterone-receptor positive, detection of positive staining of salivary duct carcinoma tumor cells for these receptors is seldom observed.[6,10–12] Also, in contrast to metastatic breast carcinoma, cutaneous metastases from salivary duct carcinoma are rare.[1–4,13]

The authors describe two men with rapidly progressive salivary duct carcinoma who developed cutaneous metastases that not only presented as carcinoma hemorrhagiectoides, but also had a distinctive pattern of distribution resembling a medieval knight’s shield. In addition, the authors summarize the clinical and associated pathological features of inflammatory cutaneous metastatic carcinoma (including carcinoma erysipelatoides, carcinoma hemorrhagiectoides, and carcinoma telangiectoides) and review the characteristics of patients who had salivary duct carcinoma-related cutaneous metastases. Finally, they suggest that the unique distribution of their patient’s cutaneous metastases be referred to as “the shield sign.”

Case Report
Case 1. In March 2008, a 71-year-old man presented with an enlarging left parotid gland mass. He underwent a left radical parotidectomy and modified radical neck dissection. Surgical pathology revealed a salivary duct carcinoma with extensive lymphovascular and perineural invasion; multiple lymph nodes were positive for tumor. The tumor cells were diffusely positive for androgen receptor and vascular endothelial growth factor (VEGF), focally positive for epidermal growth factor receptor (EGFR) and estrogen receptor-beta, and negative for HER2/neu; there was no phosphoinositide (PI) 3-kinase mutation and phosphatase and tensin homolog (PTEN) gene expression stained normally by immunohistochemistry. Postoperatively, he received six weeks of concurrent chemoradiation (60Gy in 30 fractions and weekly cisplatin) that concluded in July 2008.

In August 2009, he began to develop an asymptomatic red lesion on his chest, following blunt trauma to the area. Examination in November 2009, at 73 years of age, showed a lesion that was morphologically both purpuric and cellulitis-like. There was a large, violaceous, confluent, hemorrhagic and erythematous, dermal plaque with overlying black keratotic angiokeratoma-like papules that extended across his chest and from his neck to his upper abdomen, reminiscent of a medieval knight’s shield (Figure 1). It also involved his neck and left posterior shoulder.

Skin biopsies, from three separate locations, demonstrated metastatic carcinoma consistent with a salivary duct origin (Figure 2); the tumor cells were positive for keratin (with a pan cytokeratin antibody) and diffusely reactive for PTEN. There was not only extensive infiltration of the tumor cells in the dermis, but also within the vessels. The vessels showed strong expression of D2-40 while partially or completely lacking expression of CD31, thus suggesting that these vessels were lymphatics (Figure 3). In addition, red blood cells were observed within the lymph vessels. Dilated lymph vessels in the papillary dermis, which were filled with tumor and containing erythrocytes, protruded upwards with thinned overlying epithelium in areas that clinically corresponded to the angiokeratoma-like lesions (Figure 4). The management of the patient’s metastatic and recurrent salivary duct carcinoma and his response to therapy has previously been described.[14]

Case 2. A 69-year-old man noticed a left preauricular mass in February 2009. Within two months, he developed additional lesions in his left axilla and chest wall. The left parotid gland mass and left axillary lymph nodes were biopsied; pathology revealed a salivary duct carcinoma. The tumor cells were strongly and diffusely positive for pan-keratin, cytokeratin 7, and androgen receptor; focally, they were weakly positive for HER2/neu and negative for EGFR. There was no PI 3-kinase mutation. However, immunohistochemistry analysis revealed a loss of PTEN gene expression.

He received five cycles of docetaxel with a very good response to treatment. Subsequently, he was treated with four weeks of concurrent chemoradiation (45Gy in 20 fractions and weekly cetuximab) that concluded in October 2009. However, two months later (at 70 years of age), computerized tomographic scans demonstrated disease progression with new mediastinal and bilateral axillary lymphadenopathy. In addition, he noticed a new purple discoloration of his right face and neck that also involved his central chest.

Examination showed an asymptomatic, confluent and violaceous, indurated, hemorrhagic-appearing purpuric dermal plaque suggestive of a medieval knight’s shield that extended across his chest and from his right face and neck to his mid-abdomen (Figure 5). Focally, bullae and pseudovesicles were also noted. Skin biopsies, from two separate sites, demonstrated metastatic salivary duct carcinoma that infiltrated extensively in the dermis (Figure 6). The tumor cells were strongly diffusely positive for keratin 7 and androgen receptors; they were negative for estrogen receptor, progesterone receptor, and HER2/neu. Loss of PTEN gene expression was again demonstrated.

Tumor cells were also in the endothelial-lined vessels that also contained erythrocytes (Figure 7). Many of the vascular spaces were CD31 positive and D2-40 negative staining, thus consistent with blood vessels (Figure 8). In addition, a few of the tumor-containing vessels were CD31 positive and D2-40 positive staining, consistent with lymphatics (Figure 9). The subsequent management of the patient’s metastatic and progressive salivary duct carcinoma and his response to treatment has previously been reported.[14]

Discussion
Cutaneous metastases of visceral malignancies may result from direct spread of the tumor to the overlying skin or from either hematogenous or lymphatic spread. The reported incidence of solid tumor metastases to skin varies from less than one percent to approximately 10 percent. Indeed, cutaneous metastases can occasionally be the presenting manifestation of a previously undiagnosed cancer.[15–19]

Cutaneous metastases can mimic a bacterial infection (such as an acute paronychia20) or a viral infection (such as herpes zoster[18,21]). They can also mimic primary skin tumors, such as an epidermoid cyst,[22–26] a keratoacanthoma,[24,27] or a pyogenic granuloma.[28] Distinctive patterns of cutaneous metastases are most commonly observed in women with metastatic breast cancer; however, they have also been seen with other tumors. Some of the patterns include alopecia neoplastica,[29–31] carcinoma en cuirassee,[16,25,32] and inflammatory metastatic carcinoma of the skin.[33–36]

Inflammatory cutaneous metastatic carcinoma has more than one clinical morphology (Table 1)[37,38]; however, this category of metastases to skin is unified by the pathology finding of metastatic tumor cells predominantly located in dermal vessels—either lymphatics or blood vessels. In addition, similar to inflammatory carcinoma of the breast, tumor cells may also be present in the dermis in between the bundles of collagen. The advent of antibody-containing immunoperoxidase stains that bind to specific antigens primarily on lymphatic vessels (D2-40, referred to as podoplanin, which is a small mucin-like transmembrane glycoprotein expressed by lymphatic—but not blood vessel—endothelial cells) or both lymphatics and blood vessels (CD31, also referred to as platelet endothelial cell adhesion molecule-1, which is expressed by lymphatic and blood vessel endothelial cells) enables the identification of the tumor-infiltrated dermal vessels.[37,39,40]

Inflammatory cutaneous metastatic carcinoma has previously been considered to have two classical clinical presentations; however, there are rare individuals in whom a simultaneous combination of both lesion morphologies has been observed.[41] Carcinoma erysipelatoides appears as sharply demarcated macular erythematous patches and plaques that mimic a streptococcal skin infection and demonstrates infiltration of tumor aggregates predominantly in the dermal lymphatics.[37,41,42] Carcinoma telangiectoides appears as erythematous patches with prominent telangiectasias and shows tumor thrombi predominantly in the blood vessels of the upper dermis.[37,41,43]

The authors introduce a third pattern of inflammatory cutaneous metastatic carcinoma that has both a distinctive clinical presentation and pathological correlation—carcinoma “hemorrhagiectoides.” The metastatic cutaneous lesions have a hemorrhagic and purpuric appearance. Microscopically, there is hemorrhage of red blood cells into the lymphatic vessels of the upper dermis along with partial or extensive infiltration of the dermis by metastatic tumor. The authors were able to definitively establish the identification of the tumor-containing vascular spaces by evaluating the tissue sections with specific immuno-peroxidase stains containing antibodies to antigens, such as D2-40 that predominantly labels lymphatics and anti-CD31 that labels both lymphatics and blood vessels. Using these antibodies, they were able to indeed confirm that the tumor-containing vascular spaces in which erythrocytes were also present were predominantly lymphatics; however, in some areas, the authors were also able to discover tumor cells in blood vessels.

The pathogenesis of carcinoma hemorrhagiectoides remains to be established. Indeed, the pathology findings in carcinoma hemorrhagiectoides share features of both carcinoma erysipelatoides and carcinoma telangiectoides—tumor-containing vessels in the dermis and infiltration of the interstitial dermis by cancer cells. However, in contrast to the paucity of tumor cells in the dermis associated with carcinoma erysipelatoides and carcinoma telangiectoides, the degree of tumor infiltration in carcinoma hemorrhagiectoides is usually extensive and may be responsible for the plaque-like appearance of the cutaneous metastases.

Unique to carcinoma hemorrhagiectoides—and possibly accounting for its violaceous purpuric appearance—is the hemorrhage of red blood cells into the lymph vessels in the upper dermis. The authors hypothesize that the presence of erythrocytes in the dermal lymphatics may be secondary to fistula formation between the metastatic tumor-containing lymphatics and the adjacent dermal capillaries. Indeed, the development of fistulas secondary to solid tumors infiltrating into adjacent structures has previously been described in oncology patients.[44,45] The intravascular pressure in the blood vessels is greater than that of the juxtaposed lymphatics. Therefore, once a fistula has been created, the red blood cells hemorrhage from the capillary into the tumor-filled lymph vessel.

Alternatively, the infiltration of metastatic tumor in the dermis may not only contribute to the clinical appearance of an indurated and raised area of cutaneous metastasis, but also the subsequent hemorrhage of red blood cells into the superficial dermal lymphatics. The dermal metastases, particularly if extensive, may damage—either directly or indirectly via cytokines and inflammatory mediators—the integrity of the adjacent superficial small blood vessels that would then allow hemorrhage of erythrocytes into the surrounding dermis. Subsequently, some of these red blood cells are absorbed by the lymphatics in that area.

Salivary duct carcinoma is an uncommon head and neck malignancy; tumors with metastases to the skin are extraordinarily rare. Indeed, to the best of the authors’ knowledge, metastatic parotid duct carcinoma to the skin has only been described in five individuals—including their patients (Table 2).[1–4] The morphology of the cutaneous metastases included angiokeratoma-like lesions, bullae, erythematous patches and plaques, nodules, purpuric violaceous plaques, and pseudovesicles.

The most common locations of cutaneous metastases in patients with salivary duct carcinoma were the neck and chest (3 patients); other sites included the face (2 patients), extremities [arm (1 patient) or leg (1 patient)], abdomen (2 patients), and back (1 patient) (Table 2).[1–4] The authors’ patients had a unique cutaneous distribution of their metastastic tumor that morphologically mimicked a medieval shield. Specifically, the cutaneous tumor infiltration extended from the anterior shoulders across the chest and from the sternal notch downward toward the umbilicus.

The authors respectfully refer to the unusual skin distribution of metastatic salivary duct carcinoma in both of their patients as the “shield sign.” This dramatic presentation of cutaneous metastasis is not solely restricted to salivary duct carcinoma; similar—albeit less extensive—presentation of tumor metastases to skin has also been observed in other patients with adenocarcinoma,[46,47] anaplastic carcinoma,[48] or squamous cell carcinoma[49] from either the parotid gland,[46] the thyroid,[48] or unknown origin.[47,49] Indeed, the “shield sign” may be an uncommon presentation of tumors originating and/or metastasizing to the head and neck, probably by involvement of the lymphatic vessels originating in the neck and extending downward to the chest.

Conclusion
In conclusion, salivary duct carcinoma is an uncommon, yet highly aggressive, head and neck tumor. Cutaneous metastases of salivary duct carcinoma are extraordinarily rare. The authors have observed two men with a distinctive pattern of distribution of the cutaneous metastases from their salivary duct carcinoma that spread from their primary tumor to involve the skin across their chest and extending to their abdomen, thereby mimicking a medieval knight’s shield. The “shield sign,” a term the authors introduce to describe this unique presentation of skin metastases from visceral cancer, has also been observed—albeit rarely—in patients with a primary malignancy of the parotid gland, thyroid, or unknown origin. In addition, the morphology of both of the patients’ cutaneous metastases—carcinoma hemorrhagiectoides—was clinically distinctive with a pathognomonic pathological correlation: the purpuric and hemorrhagic dermal plaques microscopically demonstrated tumor-filled vessels (mostly lymphatic) in the superficial dermis into which red blood cells had hemorrhaged and partial-to-extensive infiltration of the adjacent dermis by metastatic tumor. The advent of specialized immuno-peroxidase markers for lymph vessels (D2-40) and both blood vessels and lymphatics (CD31) should enable confirmation of carcinoma hemorrhagiectoides when oncology patients present with hemorrhagic plaques of suspected cutaneous metastases—especially if the distribution of the lesions corresponds to that of a medieval knight’s shield.

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