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- Copyright © 2013 Elisabeth Enzenhofer et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Abstract
Hindawi Publishing Corporation Journal of Skin Cancer Volume 2013, Article ID 973123, 6 pages http://dx.doi.org/10.1155/2013/973123 Review Article Elisabeth Enzenhofer, Philipp Ubl, Christian Czerny, and Boban M. Erovic Department of Otolaryngology Head and Neck Surgery, Medical University of Vienna, Waehringer Guertel 18-20, 1090 Vienna, Austria Correspondence should be addressed to Boban M. Erovic; boban.erovic@meduniwien.ac.at Received 24 October 2012; Accepted 4 January 2013 Academic Editor: Justin Lee Copyright © 2013 Elisabeth Enzenhofer et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Merkel cell carcinoma (MCC) is a rare, aggressive neuroendocrine tumor of the skin with a mortality rate of approximately 25% (Peloschek et al., 2010). Accurate assessment of nodal involvement in patients with MCC predicts significantly overall outcome (Smith et al., 2012 and Ortin-Perez et al., 2007). Due to the rarity of this highly aggressive disease, only a few imaging reports on MCC were published, and subsequently still to date no accepted imaging algorithm for MCC is available. For primary staging of MCC, general recommendations have included ultrasonography, chest X-ray CT, and MRI, but recent articles show that the use of sentinel node and FDG-PET/PET-CT is gaining more and more importance. 1. Introduction and Overview Merkel cell carcinoma are often biopsied or nonaccurately resected with close margins [2]. In fact, patients present- Merkel cell carcinoma is a rare and highly aggressive neu- ing with unclear new skin lesions should undergo clinical roendocrine tumor of the skin. It develops predominantly examination, and lesion still highly suspicious for Merkel cell on sun-exposed area of the head and neck [1, 2]. In 1972, carcinoma should be excised with clear and wide margins. Toker described an unknown, trabecular carcinoma of the Diagnosis and management of nodal metastasis in patients skin in vfi e caucasian patients [ 3]. In 1982, Tang and Toker without a primary tumor can be challenging. In particular proposed that the MCC derives from the Merkel cell, a MCCmetastasiscan mimicmetastasisfromother smallcell mechanoreceptor of the hair follicle [3, 4]. neoplasms, that is, for example lung carcinoma [3, 11]. In 2%– MCC typically develops rapidly and manifests as rfi m, 19% of the patients no primary tumor can be found—defined nontender, dome-shaped red, purple or violet nodule [5, 6]. as MCC of unknown primary (MCCUP) [11]. Due to the The overlying skin is smooth and shiny, sometimes exhibiting rarity of this disease, theliteratureonMCCUP is very limited ulcerative, acneiform, or telangiectatic features [5, 7]. [12, 13]. MCC tends to metastasize to the regional nodes and Agelli performed multiple epidemiological studies show- in 50% of the patients it spreads hematogenously to other ing that between 1986 and 2001 the age-adapted incidence of organs [8], that is, the liver, bone, brain, and lung [2]. In MCChas increased3-foldwithanannualincreaseof8%[14]. 1993, Haag and colleagues defined a commonly used staging This growing incidence rate has given a significant input for system [2, 9]: stage I is defined by local disease without lymph a growing interest in disease management of patients with node involvement or distant metastases, in stage II carcinoma Merkel cell carcinoma [15, 16]. has spread to lymph nodes but no systemic metastases are Unfortunately, there is sparse literature on imaging algo- detectable, and in stage III distant metastases are detectable rithms in patients with Merkel cell carcinoma and no widely [9]. accepted guidelines for imaging of Merkel cell carcinoma are available [5, 8]. This paper reviews the literature on imaging of Diagnosis of MCC can be challenging because in many cases MCC lesions mimic benign skin lesions [10]. Unfor- Merkel cell carcinoma discussing the role of the most recent tunately, in clinical practice, lesions highly suspicious for imaging and diagnostic tools. 2 Journal of Skin Cancer 2. Ultrasonography the head and neck region, no nodal disease could be detected [27]. In particular, in 5 out of 74 clinically node-negative Ultrasonography is a highly accurate and cost-effective tech- patients who underwent preoperative lymphoscintigraphy, nique in tumor staging. In regard to Merkel cell carcinoma, lymphoscintigram failed to identify positive nodes metas- work up and staging of the neck should be started with an tases [27]. In 2002, Nguyen and colleagues recommended ultrasonographic examination [2]. lymphoscintigraphy in combination with perioperative lym- Primary skin lesions can appear as single or multicen- phatic mapping. tric hypoechoic solid nodules arising from the dermis and extending in the subcutaneous fat, with variable degrees of posterior acoustic transmission [5, 8]. Ultrasonographic fea- 4. Computed Tomography (CT) turesofMerkelcellcarcinoma appear similartomorecom- Due to the usefulness of CT for imaging lymph nodes of mon skin tumors such as melanoma or basal cell carcinoma the head and neck as well as for nodular metastases in [8]. It has been shown that in sonographically easy accessible subcutaneous fat and visceral metastases, several authors regions, such as the neck, differentiation of malignant from proposed that CT is a reliable imaging method for the initial benign lymphnodes canbeachievedwithanaccuracy stagingofpatientswithMerkelcellcarcinoma [2, 5, 8]. In of 89%–94% [17, 18]. Furthermore, ultrasonography has a particular, Colgan and colleagues proposed sensitivity and key role in real-time imaging during n fi e needle biopsy of specificity rates of 47% and 97%, respectively, with positive nonpalpable lesions of Merkel cell carcinoma [8]. Except for a and negative predictive values of 94% and 68%, respectively, few published case reports, ultrasound guided and nonguided for diagnosis of lymph node involvement by CT imaging [29]. n fi e needle aspiration biopsy has been rarely described in However, Peloschek and coworkers claimed a specificity of MCC patients [19–23]. Den fi itive diagnosis of metastatic 96.2% and a sensitivity of 89.1% for CT in diagnostic imaging disease is challenging with n fi e needle aspiration cytology of Merkel cell carcinoma including lymph node involvement alone [20]. The cytomorphology resembles numerous other as well as evaluation of distant metastasis [2]. malignancies such as malignant lymphoma and malignant Compared to the muscle, primary skin lesions appear as melanoma [23]. Nevertheless, FNA of MCC can provide isodense to slightly hyperdense cutaneous rounded nodules an accurate and reliable diagnosis of primary or recurrent extending below the skin [30]. Cutaneous fat stranding adja- metastatic lesions [23]. In patients where positive nodes are cent to the primary lesion suggests engorgement and edema proven, a full body imaging should be done to detect distant from lymphatic invasion [8]. Furthermore, enhanced CT scan metastases [16]. is able to demonstrate high-attenuation lymphadenopathy and soft CT scan is able to demonstrate high-attenuation 3. Sentinel Node Biopsy (SLNB) tissue nodules, which are often clinically silent [ 5, 8, 30], suggesting focal metastases [30]. Lymphadenopathy mostly Sentinel lymph node biopsy provides the unique capac- occurs in the neck, especially in the parotid region followed ity to detect metastasis and micrometastasis and subse- by the axilla, mediastinum, retroperitoneum, and groin. quently lymph metastasis node draining [5]inpatientswith Distant metastases include local and retroperitoneal lymph melanoma [5], squamous cell carcinoma [24], and MCC [5] nodes, liver, bone, brain, and lung [31]. Using CT-imaging, by using lymphoscintigraphy [25]. SLNB in patients with metastases of abdominal organs manifest as hypervascular Merkel cell carcinoma appears to be a reliable staging tech- lesions with ring-like enhancement [5]. So-ft tissue metas- nique, whereas the prognostic relevance of positive tumor tases may involve the chest wall or abdominal wall with status of thesentinelnodestill remainsunclear [26]. musculoskeletal invasion. Gollub and colleagues conducted In up to two-thirds of patients with stage I MCC disease, a study in 12 patients with MCC and showed the ability of regional nodal spread has been diagnosed at initial presen- CT scanning to detect visceral and nodal metastases. They tation with SNLB, and in only 7%−31% nodes are clinically suggest follow-up CT scans at 3, 6, 12, and 18 months aeft r palpable in patients with stage II disease [5]. initial treatment to discover recurrent disease [30]. Lymphatic drainage pathways in the head and neck region are more variable than in any other location of the body and are challenging to be accurately predicted [27]. Occasionally, 5. Magnetic Resonance Imaging (MRI) head and neck lymphoscintigrams fail to identify a definitive lymphatic drainage pattern [27]. In particular, unexpected There are only a few studies and case reports describing nodal drainage is seen in 37%–84% of cases and is oen ft the usefulness of MRI in patients with MCC. In particular, missed without the use of lymphoscintigraphic guidance [5, case reports on large primary tumors of the sinonasal region 28]. Negative sentinel biopsy appears to be a relevant prog- [32], and abdominal wall [33] described MCC lesions as nostic factor for disease-free survival [26]. Consequently, inhomogeneous in signal intensity on T1- and T2-weighted false-negative findings in lymphadenectomy are leading to images [33, 34]. Focal central increased signal intensity on inadequate staging of MCC and aggressive but unnecessary T2-weighted images within large lesions has been described complete nodaldissectioninpatientswithtruestage Idisease as being associated with histologically proven central necrosis [5]. and hemorrhage [33, 34]. In MRI scans, lymphatic satellite However, Stadelmann and colleagues showed that in 5%– lesions are reflected by reticular stranding and subcutaneous 6,8% of patients with melanoma or Merkel cell carcinoma of masses.Thesameappearanceofsatellite lesionscan be Journal of Skin Cancer 3 observed by CT imaging. Large lymph node metastases appear as lesions with n fi e, compressed, retained fatty tissue [34]. Colgan showed in a study of 7 patients who underwent first MRI followed by sentinel lymph node biopsy or regional lymph node dissection a positive predictive value of 0% and a negative predictive value of 67% for the MRI [29]. However, Anderson and colleagues showed in 15 patients that MRI improves dieff rentiation of distant metastases [ 34]. Furthermore, intramuscular masses and perifascial tumors were better defined on MRI than by CT imaging [ 34]. MRIinMerkelcellcarcinomasishighlyaccuratefor evaluating soft tissue metastases, as well as involvement of brain and bone marrow. Invasion of the central nervous system is rare; however, in case of neurologic symptoms, workup should be performed with MRI [5, 35]. Figure 1: PET/CT: pathologic enhancement in the right parotideal region. 6. Somatostatin Receptor Scintigraphy (SRS) The rational for performing somatostatin receptor scintig- F-FDG is a glucose analog and a surrogate marker for raphy in MCC patients to detect locoregional and distant glucose metabolism [41]. In particular, increased glycolysis metastatic disease is based on the neuroendocrine char- in certain areas compared to healthy tissue is a distinctive acteristics of MCC. In 1992, Kweekeboom and colleagues feature of malignant transformation. Increased glycolysis can presented data for the eeff ctiveness of SRS in 4 patients with be captured using the FDG positron emission tomography MCC. In all 4 patients, in whom the tumor was detected by (PET) technique allowing differentiation between normal CT and sonography, tumor sites were also detected in SRS. andmalignant tissue[5]asshown in Figure 1. They showed that SRS had an equal or greater sensitivity than The main difficulty with PET alone is the lack of an CT for imaging of MCC [36]. anatomical reference frame. eTh hybrid of FDG-PET and Nevertheless, more recent studies observed a limited the morphological data of CT have potential to improve sensitivity of SRS as well as a high rate of false positive specicfi ity of PET [ 2]. and negative results [37–39]. Guiltera presented their 7- Several studies in FDG-PET and PET-CT supported year experience with 20 patients with MCC. In particular, the eeff ctiveness in detecting locoregional nodal and distant sensitivity of 78% and specificity of 96% for SRS of Merkel metastatic disease and subsequently staging in patients with cell carcinoma could be observed [38]. MCC [2, 42–47]. A comparison between SRS, CT and MRI showed that tis- Unfortunately, only few data are available comparing sue SRS is less aeff cted by inflammation, edema, granulation FDG-PET and PET-CT with the gold standard of histo- tissue at surgically pretreated or irradiated sites [5]. However, pathologic nodal evaluation and other imaging tools in MCC there is a significantly limited value in organs showing a patients. physiological uptake of radiolabelled octreotide such as liver, In a study comparing FDG-PET-CT, MRI, bone scan, and adrenal glands, pancreas, thyroid gland, and spleen [5, 37]. computerized tomography in 11 patients, the authors could This causes a low tumor-to-background ratio, which hampers show that FDG-PET has a sensitivity of 92% and specificity detection of metastasis near organs with a high physiological of 100%, and in 3 patients FDG-PET-CT allowed a more uptake of the tracer [37]. Further, other systemic diseases precise anatomic localization of lesions [42]. Furthermore, such as sarcoidosis, tuberculosis, Wegener’s granulomatosis, Concannon et al. found, in a retrospective study of 18 non-Hodgkin lymphoma, or Hodgkin’s disease have also led patients with MCC who underwent FDG-PET-CT imaging, to false positive SRS results [37, 40]. that FDG-PET-CT resulted in altered staging in 33% of Unfortunately, a limited use of SRS in diagnostic evalua- patients and in changes in disease management in 43% of the tion of Merkel cell carcinoma. eTh refore many authors do not patients [36]. However, a retrospective study in 15 patients recommend SRS for routine imaging [37, 38]. showed a signicfi ant advantage of FDG-PET-CT compared to clinical examination in 46% of patients, whereas sensitivity, 7. Positron Emission Tomography specicfi ity,andpositiveandnegativepredictivevaluewerethe same for PET-CT and CT, respectively [48]. (PET) and Positron Emission Computed In a retrospective study, Peloschek and colleagues Tomography (PET-CT) described that FDG-PET has a sensitivity of 85,7% and a Within the last years nuclear medicine, especially PET and specicfi ity of 96,2% compared to a sensitivity of 95,5% and PET-CT, has gained importance in diagnostic imaging of specicfi ity of 89,1% for conventional imaging methods [ 2]. Merkel cell carcinoma. Since MCC is a rapid growing tumor, In another study, Grewal et al. reported the sensitivity and it is expected that tumor cells have an increased glycolysis [2]. specicfi ity of FDG-PET in MCC as 79% to 92% [ 49]. 4 Journal of Skin Cancer The most significant drawback of this technique is the needle biopsy of Merkel cell carcinoma. Deni fi tive diagnosis fact that in some cases metabolic trapping can be nonspecific is difficult but possible and accurate with FNA [ 19, 20]. andinaddition to tumorcells it canalsobefound in sitesof In oncologic patients with suspected distant metas- inflammation or infection [ 50]. In case of brain metastases tases FDG-PET, CT or MRI imaging should be performed. FDG-PET scanning is significantly hampered due to the Somatostatin receptor scintigraphy is no longer recom- high metabolic rate. Subsequently high cerebral background mended for routine imaging of Merkel cell carcinoma, as impairs detection of metastatic lesions in the brain [51]. studies showed a high rate of false-positive or false-negative Furthermore, some authors describe a failure of FDG-PET- results in detection of Merkel cell carcinomas and metastatic CT in detection of lymph nodes micrometastases and distant disease [37]. metastatic disease [29, 48]. As Merkel cell carcinoma has a high rate of distant metas- tasis, PET scan has a particular value in imaging and staging workup. 7.1. Alternative Tracers. Biogenic amines are enhanced and MRI has a particular value in assessing so-ft tissue accumulated in neuroendocrine tumors and are an alterna- involvement, whereas CT is used for imaging of thorax and tive PET tracer for MCC to visualize malignant tissue [2]. A abdomen. Three months and 1 year aer ft treatment, FDG-PET case report described that, due to the less intense uptake of should be repeated for follow-up imaging. Moreover, fusion F-DOPA, it is more accurate in diagnosis of brain metas- of FDG-PETwithCTorMRI wouldimprove specicfi ity of tases F-DOPA compared to FDG-PET and is as accurate PET analysis [2]. in detection of more extracranial metastases [45]. However, Colgan et al. reported that the use of FDG-PET when Peloschek et al. showed in a study, superior value of FDG-PET compared with traditional computed tomography is signif- in detection of malignant sites of MCC, showing two false 18 icantly more sensitive and equally specicfi than FDG-PET negative regions in F-DOPA-PET [2]. Furthermore, diffuse alone in evaluation of regional lymph node basins in primary 18 18 F-DOPA uptake was F-DOPA seen in a region pretreated MCC [29]. with surgery and F-DOPA irradiation, which was similar to The role of FDG-PET-CT in management of MCC that in FDG-PET that hampers the idea of a benetfi of F- remains to be a matter of debate. However, PET-CT has DOPA. uTh s, F-DOPA-PET cannot be recommended for been showntohaveapotentialhighimpactofstaging and diagnostic imaging F-DOPA in Merkel cell carcinoma [2]. management of MCC patients with stage I and II disease [43]. To date, there is still no imaging algorithm for Merkel 7.2. Follow-Up Imaging. Aeft r treatment of primary lesions of cell carcinoma. Due to the rarity of Merkel cell carcinoma MCC, a close monitoring is required. imaging, findings have been reported only in small trials For follow-up imaging, we would suggest a routine chest and case reports. On the basis of the existing literature, X-rayaswellasacomputed tomography of theheadand we would recommend FDG-PET CT as rst fi line imag- neck region 3 months after therapy. Every year after therapy, ingofMerkelcellcarcinoma.Itisanoninvasiveimaging a chest X-ray, CT and MRI of the head and neck region technique that has potential to detect occult lesions big- are recommended. 6, 9, 15, 18, 21, and 30 months after ger than 5–8 mm in minimal diameter [48]thatare not therapy a cervical ultrasonography and a chest X-ray should detectable by other imaging techniques. We suggest that be performed. Becauseofthe lowcostofsonography, it has further diagnostic imaging should be obtained depending on a high value in routine follow-up imaging of Merkel cell the results of lymph node involvement and distant metas- carcinoma [2]. Chest X-ray is a routine imaging technique tases. to evaluate possible pulmonary involvement. Peloschek et al. However, in case of negative lymph node involvement, we recommend repetition of FDG-PET 3 months and 1 year aeft r would recommend sentinel lymph node mapping with subse- treatment [2]. quently performing an ipsilateral neck dissection to confirm lymph node status histopathologically. In our opinion, due to the low morbidity of a neck dissection, it has a high diagnostic 8. Discussion and preventive value. eTh key task of imaging in patients with Merkel cell carci- In summary, Merkel cell carcinoma is a highly aggressive noma is staging at the initial presentation and post-therapeu- skin cancer with a high rate of metastasis and mortality. 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