Strahlentherapie und Onkologie

Case Study

Pilomatrix Carcinoma with Lymph Node and Pulmonary Metastases Nikolaos Tselis, Reinhard Heyd, Hans-Georg Vogt, Nikolaos Zamboglou1

Case Report: A 72-year-old male patient developed a locally recurrent pilomatrix carcinoma (PC) of the right upper shank. Within a 2-year period he also developed bilateral pulmonary as well as inguinal, cervical and paraaortic lymph node metastases. After external-beam radiation therapy (EBRT) alone, sole interstitial high-dose-rate (HDR) brachytherapy (BRT) or postoperative EBRT with interstitial HDR-BRT boost, the patient demonstrated regressive or stable disease at the lymphatic sites. Systemic chemotherapy with intravenous paclitaxel failed to assure a substantial pulmonary response. In the course of the disease after 28 months pulmonary progression has led to continuing clinical deterioration. Conclusion: In accordance with literature data the hitherto course of this case corroborates that radiation therapy (RT) modalities can play an important role in the treatment of PC. Key Words: Pilomatrix carcinoma · Cutaneous adnexal tumors · Matrical tumors · Radiation therapy Strahlenther Onkol 2006;182:727–32 DOI 10.1007/s00066-006-1600-2 Pilomatrixkarzinom mit lymphogener und pulmonaler Metastasierung Fallbericht: Ein 72-jähriger Patient mit Lokalrezidiv eines Pilomatrixkarzinoms am proximalen Unterschenkel entwickelte innerhalb von 2 Jahren bilaterale pulmonale sowie inguinale, zervikale und paraaortale Lymphknotenmetastasen. Nach alleiniger perkutaner Radiotherapie (EBRT), interstitieller High-Dose-Rate-(HDR-)Brachytherapie (BRT) oder postoperativer EBRT mit HDR-BRT-Boost zeigte der Patient Regress bzw. Größenstabilität der Lymphknotenmetastasen. Eine systemische Chemotherapie mit Paclitaxel erbrachte kein nennenswertes Ansprechen der pulmonalen Läsionen. Nach einem 28-monatigen Krankheitsverlauf ist der Patient pulmonal progredient. Schlussfolgerung: Basierend auf den eigenen klinischen Beobachtungen und in Einklang mit den Ergebnissen anderer Arbeitsgruppen können strahlentherapeutische Therapiemodalitäten in der Behandlung des Pilomatrixkarzinoms als effektiv erachtet werden. Schlüsselwörter: Pilomatrixkarzinom · Kutane adnexale Tumoren · Matrixtumoren · Strahlentherapie

Introduction Pilomatrixoma is a slow-growing benign dermal tumor of the hair matrix cells, first described in 1880 by Malherbe & Chenantais [17] as “calcifying epithelioma”. Although the locally aggressive behavior of some cases of pilomatrixoma was suggested by Gromiko [6] in 1927, the malignant variant of this lesion was not seriously considered until 1980, when Lopansri & Mihm [14] reported on a patient with aggressive pilomatrixoma and reviewed five similar cases from the literature. They proposed the term “calcifying epitheliocarcinoma 1

of Malherbe” or “pilomatrix carcinoma” (PC) and since then less than 80 cases of PC have been reported in the medical literature [30]. PC generally occurs as an asymptomatic mass and lesions are mainly situated on the scalp, posterior area of the neck, buttocks, and upper extremities, although they have also been reported in other areas such as the axilla [7] and inguinal region [36]. Recurrences of PC are common, but metastasizing disease is exceedingly rare, with only twelve cases reported in the medical literature (Table 1).

Department of Radiotherapy, Offenbach Hospital, Offenbach, Germany.

Received: April 28, 2006; accepted: August 3, 2006

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The main diagnostic difficulty is to distinguish PC from at the inguinal site. Pelvic MRI showed a large tumor with pilomatrixoma, and immunohistochemistry and flow cytomenhanced signal characteristics on T1-weighted spin-echo etry have failed to differentiate the malignant form from its sequences (Figure 1). Surgical assessment determined the more common benign counterpart [14, 19, 21, 25, 31, 36]. recurrent mass unresectable and a combined treatment apSurgical excision with safety margins remains the preproach of EBRT with HDR-BRT boost was planned. The ferred primary treatment [9] and external-beam radiation tumor received 25.2 Gy in five weekly fractions of 1.8 Gy in therapy (EBRT) has been employed primarily or after surEBRT mode to the right inguinal region, followed by 35 Gy gery with mixed results [2, 5, 27, 31, 37, 38]. To date, computed in seven fractions of 5 Gy (one fraction daily over 7 consecutomography-(CT-)guided interstitial high-dose-rate (HDR) tive days) as HDR-BRT boost (D90 = 5.4 Gy, V100 = 93.2%, V150 = 62.5%, and V200 = 36.5%) in CT-guided technique brachytherapy (BRT) has not been employed in the treatment (Figures 2a and 2b). of PC. We present a case of PC in which multiple local recurrences and distant metaTable 1. Summary of reported cases with metastatic pilomatrix carcinoma. stases developed within a few months. Tabelle 1. Literaturübersicht metastasierter Pilomatrixkarzinome. The patient received a multimodal therapy regimen, consisting of surgery, cyReference Year Distant metastases site totoxic chemotherapy, EBRT and CTGould et al. [5] 1984 Lungs guided interstitial HDR-BRT. Case Report A 72-year-old white male was initially treated with surgical excision for a small painless mass of the right upper shank postoperatively diagnosed as PC. Subsequently, due to nonradical surgical margins the patient underwent wider local excision without any additional therapy. Past medical history was significant for diabetes mellitus, chronic renal failure, nephrosclerosis, and hypertension with chronic global cardiac insufficiency. After 4 months of follow-up he was admitted to our institution presenting an indurated scar at the previous surgical site and a newly diagnosed subcutaneous lesion in the right inguinal region. The scar was widened to provide an ample margin and a specimen from the right inguinal lymphatics was also obtained. The histopathologic study of the bioptic tissues revealed recurrent and metastatic PC, respectively. The local recurrence was treated by repeated wider excision and repaired by means of a laminar graft obtained from the same leg. For the metastatic lymphadenopathy, sole radical lymphonodectomy was selected as treatment of choice. Physical examination, magnetic resonance imaging (MRI) of the pelvic region, thoracoabdominal CT and bone scan showed no other findings of note. 2 months after surgery the patient presented an extensive local recurrence

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Mir et al. [23] Tateyama et al. [36] O’Donovan et al. [28] Hanly et al. [8] Mack et al. [15] Monchy et al. [25] Niedermeyer et al. [27] Li et al. [13] Bremnes et al. [2] De Galvez-Aranda et al. [3] Stern et al. [35] Current case

1986 1992 1993 1994 1994 1995 1996 1997 1999 2002 2004 2006

Lungs and axillary lymph nodes Inguinal lymph nodes Superior pubic ramus Lungs Lungs and inguinal lymph nodes Submandibular lymph nodes Lungs and brain Liver Cervical lymph nodes, lungs and thoracic spine Lungs and inguinal lymph nodes Axillary lymph nodes Lungs and inguinal, cervical and paraaortic lymph nodes

Figure 1. Coronal T1-weighted MR image shows blooming of the signal intensity within the inguinal localized tumor. Distinct infiltration of subcutaneous structures. Abbildung 1. Koronare T1-gewichtete MRT-Aufnahme mit angehobener Signalintensität innerhalb des Tumors. Deutliche lymphogene Infiltration der subkutanen inguinalen Strukturen.

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Tselis N, et al. Metastatic Pilomatrix Carcinoma

Figure 2a – Abbildung 2a

Figure 2b – Abbildung 2b

Figures 2a and 2b. Example of the CT-guided brachytherapy implant in the right inguinal region. a) Catheters fixed at the entrance and exit points on the skin surface by buttons. b) Representative CT image showing the catheter geometry, as well as the planning target volume (PTV) with isodose lines. The reference dose is 5.0 Gy. Abbildungen 2a und 2b. CT-gestütztes Brachytherapieimplantat der rechtsseitigen Inguinalregion. a) Durch Knöpfe an den Ein- und Austrittsstellen fixierte Brachytherapieapplikatoren. b) Repräsentatives CT-Schnittbild mit Wiedergabe der Kathetergeometrie sowie Darstellung des Planungszielvolumens (PTV) mit Isodosenverteilung. Die Referenzdosis beträgt 5,0 Gy.

5 months later, the patient presented with a fast-growing local relapse on the primary tumor site at the right upper shank. MRI of the area showed a 2.2 cm × 2.1 cm × 2.5 cm large tumor, which displaced the vascular structures but did not infiltrate muscles or bones (Figure 3). A thoracoabdominal and abdominopelvic CT scan ruled out regressive disease in the right inguinal region, with no further pathologic findings. The patient received CT-guided interstitial HDR-BRT at the recurrence site, i.e., 30 Gy (D90 = 3.5 Gy, V100 = 93.8%, V150 = 71.5%, and V200 = 53%) in ten fractions of 3 Gy (two fractions daily over 5 consecutive days; Figure 4). The patient remained free of progressive disease for 6 subsequent months, when he developed a new 3.5-cm lump at the right cervical region, and pathologically enlarged paraaortic lymph nodes were revealed by abdominopelvic CT scan. He received 20 Gy with CT-guided HDR-BRT (D90 = 5.3 Gy, V100 = 91.5%, V150 = 61.5%, and V200 = 33.0%) in four fractions of 5 Gy to the cervical lesion (two fractions daily over 2 consecutive days) and 50.4 Gy in five weekly fractions of 1.8 Gy in EBRT mode to the paraaortic lymphatics. 2 months later, planned follow-up examinations confirmed stable paraaortic disease and durational regression at the BRT sites, but multiple pulmonary secondaries were shown. Chemotherapy with paclitaxel (60 mg/m2) for eight

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Figure 3. Axial T1-weighted contrast-enhanced MR image of the upper shanks, showing a 2.2 × 2.1 × 2.5 cm large tumor at the dorsal part of the right shank. The lesion extends by infiltrating the skin and displacing vascular structures but without affecting muscles or bones. Abbildung 3. Axiale T1-gewichtete MRT-Aufnahme der proximalen Unterschenkel nach intravenöser Kontrastmittelgabe. Die rechtsseitig dorsal lokalisierte Tumorformation (2,2 × 2,1 × 2,5 cm) wächst verdrängend mit kutaner Invasion, jedoch ohne Gefäß-, Muskel- oder Knocheninfiltration.

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Figure 4a – Abbildung 4a

Figure 4b – Abbildung 4b Figures 4a and 4b. Example of the CT-guided brachytherapy implant in the right upper shank. a) Representative CT image showing the catheter geometry, as well as the planning target volume (PTV) with isodose lines. The reference dose is 3.0 Gy. b) Dose-volume histogram for the PTV. Abbildungen 4a und 4b. CT-gestütztes Brachytherapieimplantat des rechtsseitigen proximalen Unterschenkels. a) Repräsentatives CT-Schnittbild mit Wiedergabe der Kathetergeometrie sowie Darstellung des Planungszielvolumens (PTV) mit Isodosenverteilung. Die Referenzdosis beträgt 3,0 Gy. b) Dosis-Volumen-Histogramm für das PTV.

cycles over 2 months was administered, with no substantial response. However, a repeat CT scan 4 months after completion of chemotherapy showed signs of progressive pulmonary disease. Currently, 28 months from the initial diagnosis, tomographic imaging modalities showed neither progressive disease at the paraaortic lymphatics nor signs of recurrence in all sites treated by HDR-BRT. Clinically and radiologically, the patient is presenting pulmonary progression while refusing cytotoxic chemotherapy or radiation treatment (RT). Discussion Pilomatrixoma is an uncommon benign tumor of hair matrix origin with an incidence of 1 per 824 skin specimens examined [24]. The neoplasm predominantly occurs in females (male : female ratio of 2 : 3) in a bimodal distribution (age < 30 years and 60–70 years) [30]. By contrast, PC, the markedly rare malignant counterpart of pilomatrixoma, occurs more commonly in males than in females (ratio 3 : 1) with preponderance in the 6th and 7th decade of life [9]. PC has a great capacity for infiltrating both laterally and in depth. It is a locally aggressive tumor with a tendency to recur and it can disseminate via the lymphatics or the blood system. Although metastases were initially considered excep-

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tional, this report brings the total number of cases with metastases to 13, which is more than 10% of all reported cases of PC (Table 1). Histologically, the diagnosis of PC can be challenging, because there are no clear histological criteria distinguishing this neoplasm from other matrical tumors. PC has characteristics of pilomatrixoma and most authors emphasize architectural features on scanning magnification as being more useful in the histopathologic diagnosis of PC than cytomorphologic features alone, especially because both PC and pilomatrixoma may inhibit increased mitotic activity [9]. The main indicators of malignancy appear to be nuclear pleomorphism, frequent atypical mitoses, central necrosis, infiltration of skin, soft tissue, blood and lymphatic vessels and ulceration [2]. So far, immunohistochemistry investigations have failed to delineate a specific marker for PC [18]. Owing to the rarity of PC, there are not well-defined standards in the surgical management of these neoplasms. Several reports have advocated wide excision with margins varying from 5 to 10 mm with a low rate of tumor recurrence, whereas recurrence rates up to 50% have been observed with simple excision [30]. The impact of cytotoxic chemotherapy as treatment option, particularly for metastatic disease, is extremely sobering.

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Unexceptionally, all reported cases with administration of intravenous chemotherapy confirm primary resistance to the utilized cytotoxic or immune-modulating agents (bleomycin, 5-fluorouracil, cisplatin, vinblastine, interferon) [2, 5, 22, 23, 27, 28, 35]. RT has been proven to be effective in the treatment of cutaneous adnexal tumors with matrical differentiation with doses being prescribed ranging from 25 to 60 Gy [1, 20, 29, 32–34]. Regarding PC, only very few cases employing RT have been described and its role in the treatment of this lesion is still unclear, mainly due to very limited experience and diverse results reported after its use [2, 5, 27, 31, 35, 37, 38]. However, five cases who were treated initially by RT or surgery followed by RT did not experience local tumor recurrence [5, 31, 37, 38]. Gould et al. [5] treated a 67-year-old white male with EBRT following surgical excision for recurrent PC of the upper back. The patient received 6,000 rad in 2 months to the excision site and, after 2 years of follow-up, pulmonary secondaries but no local recurrence were observed. Sau et al. [31] reported on two patients from the files of the US Armed Forces Institute of Pathology (one 28-year-old male and one 69-year-old female) with PC of the posterior neck region. Both patients underwent surgical wide excision and postoperative RT. Irradiation was given 3–4 weeks postoperatively to a total dose of 30 and 45 Gy, respectively. After a follow-up period up to 36 months, recurrence-free convalescence was noted in both patients. Weedon et al. [38] treated a 93-year-old male with ablation and subsequent RT for PC of the left preauricular region. The excision area was treated with 2,000 rad in a single fraction and no evidence of recurrence or metastasis could be revealed in the long-term follow-up. Veliath et al. [37] also administered a combined treatment regimen on a 39-year-old female with local irradiation after partial excision for PC of the left cheek. Roentgen therapy (200 KV, 15 mA, 1 mm Cu filtration, FSD [focus-source distance] 40 cm) was given with a total tumor dose of 45 Gy in a period of 3 weeks. The treatments were given 5 days a week with a daily tumor dose of 3 Gy at a depth of 2 cm. At 36 months of follow-up, no recurrence had occurred and no local complications attributable to the irradiation were described. The present case history is unusual in the repeated local recurrence and locoregional lymphadenopathy over a period of 19 months before extralymphatic metastatic disease eventually developed. Consistent with other reports [5, 23, 27, 28], the clinical course of the disease reflects that PC is capable of metastasizing and, moreover, illustrates the highly aggressive biological behavior of the metastatic lesions. In accordance with treatment data reported in previous cases [2, 9, 22, 23, 27, 35], the disease appeared resistant to cytotoxic chemotherapy but gratifyingly not resistant to irradiation. In respect of the latter, CT-guided interstitial HDR-BRT [11, 12, 16] appears to play an important role.

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Theoretically, interstitial HDR-BRT allows advantage in the treatment of adnexal tumors with matrical differentiation because of its radiobiological characteristics [10]. Because of prior therapy, the tumor bed is generally more hypoxic with recurrent lesions. The higher radiation doses that are applied with interstitial HDR-BRT may provide an advantage in the therapy of recurrent but also residual or newly diagnosed PC. To the best of our knowledge, our case is the first to be treated inter alia by CT-guided interstitial HDR-BRT for both local recurrence and lymph node metastases of PC. With the objective of implant upgrading, our reliable BRT method [11, 12] is not based on the Paris System [39]. Planning target volume (PTV) and critical structure definition, as well as catheter reconstruction are being performed based on postimplant CT scans. Tomographic anatomic information helps at this geometry-oriented optimization of the three-dimensional (3-D) dose distribution and thereby achievement of a uniform dose value on the surface of the PTV (the dose distribution is normalized relative to the calculated mean dose value on the PTV surface and the reference dose specified as the 100% value). 192Ir dwell positions and times are adjusted to minimize the dose to organs at risk. In accordance with the American Brachytherapy Society (ABS), American College of Medical Physics (ACMP) and American College of Radiation Oncology (ACRO) intersociety standards for the performance of BRT [26], prescribed and reported doses are specified by D90 , as determined by dose-volume histograms (Figure 4b). Similarly, dose heterogeneity is specified volumetrically by V100 , V150 , and V200 . The treatment-related clinical and radiologic outcome indicates that RT, and especially CT-guided interstitial HDR-BRT with 3-D optimized target-oriented dose application, can be considered an integral aspect in the management of PC. In addition, effective chemotherapy for palliation with a view to health-related quality of life [4] has not been established yet.

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Address for Correspondence Dr. Nikolaos Tselis Strahlenklinik Klinikum Offenbach Starkenburgring 66 63069 Offenbach Germany Phone (+49/69) 8405-3333, Fax -3334 e-mail: [email protected]

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