Langerhans cell sarcoma (LCS), one of several malignant
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1 REVIEW ARTICLE Langerhans Cell Sarcoma: Case Report and Review of World Literature Ted Zwerdling, MD,* Eric Won, MD,w Lisa Shane, MD,* Ramin Javahara, MD,* and Ronald Jaffe, MDz Summary: Langerhans cell sarcoma is a rare malignancy with only 1 pediatric case (less than 15 y of age) reported. Here, we report the second case of Langerhans cell sarcoma in a child who presented with cord compression. This patient was treated with extensive surgical resection, postoperative chemotherapy, and involved-field radiation therapy. She completed therapy and remains in remission for 27 months. A review and analysis of all 53 cases published in the world literature is provided to help guide physicians treating this disease. Recently discovered genetic mutation involving BRAF is also discussed. Key Words: Langerhans cell sarcoma, pediatric, treatment, world review (J Pediatr Hematol Oncol 2014;36: ) Langerhans cell sarcoma (LCS), one of several malignant histiocytic disorders which also include histiocytic sarcoma and interdigitating dendritic cell sarcoma, is recognized by the World Health Organization (WHO) as a class III histiocytic process involving truly malignant histiocytes. 1,2 This is supported by new evidence of BRAF mutations in some of these tumors. 3,4 LCS differs from class I and II histiocytic disorders based on morphologic characteristics of lesional cellular make-up and is frequently a fatal disease. LCS is very rare and found mostly in adults, when reported. The Histiocyte Society has established classification, diagnostic criteria, evaluation, and suggested treatments for these disorders ( org/). We recently evaluated and treated a pediatric patient diagnosed with LCS who presented with spinal cord compression and continues in complete remission for 27 months. Our goals for this report are: (1) to add information as an aid for other clinicians who may evaluate and treat this disease; (2) to undertake a review of the world literature; and (3) add to new molecular analysis of this tumor which may suggest better diagnostic criteria and allow rationale for treatment. METHODS A literature search was conducted in PubMed under the search term Langerhans Cell Sarcoma. MeSH: Received for publication February 28, 2014; accepted April 30, From the *Miller Children s Hospital, Long Beach; wdepartment of Pediatrics, University of California, Irvine, CA; and zchildren s Hospital of Pittsburgh of UPMC, Pittsburgh, PA. The authors declare no conflict of interest. Reprints: Ted Zwerdling, MD, Miller Children s Hospital, 701 East 28th Street, Suite 202, Long Beach, CA ( tzwerdling@memorialcare.org). Copyright r 2014 by Lippincott Williams & Wilkins Langerhans Cell Sarcoma; pathology, therapy, diagnosis, etiology. BRAF mutational analysis performed at Clarient Inc. (Aliso Viejo, CA) using polymerase chain reaction technique. Immunohistochemical staining was performed using standard techniques according to the manufacturers recommendations. RESULTS Case Report and Clinical Outcome A 7-year-old girl presented to the emergency department with chest pain for 2 weeks and progressive difficulty walking for 3 days. She denied lower extremity pain, fevers, travel, or trauma. The family history was unremarkable and she was taking no medications. In the emergency department, the patient was afebrile and examination found slight tenderness over the right thoracic paraspinal region which increased with movement and decreased sensation (pinprick and touch) in the lower extremities without a sensory line. Weakness involving the lower extremities, hyperactive reflexes, and bilateral Babinski signs were noted. The remainder of her examination, including a retinal examination, was normal. Magnetic resonance imaging of the spine demonstrated a left-sided, extradural soft-tissue mass with bony involvement of T5-T6 vertebral bodies. Initial treatment consisted of steroids, decompression laminectomy, and partial tumor resection. Pathologic evaluation of the resected material was diagnostic of LCS (Fig. 1). With residual tumor present, second surgery, with the goal of complete resection, was attempted. Additional tumor was removed in a piecemeal manner and it was unclear if the resection margins contained malignant cells. An extensive reconstruction of the operative site was performed with bone grafting and stabilization. Further evaluations including computed tomography (CT) scan, bilateral bone marrow aspirations and biopsies, and Tc 99 radionuclide bone scan were negative for metastatic disease. The patient then went on to receive chemotherapy (Table 1). Five months into chemotherapy, a small area of residual mass at the primary site showed slight PET/CT activity. This was biopsied and found to be fibrous tissue without evidence of LCS. Healing of the bone graft was found about 10 months into therapy and repeat metastatic evaluation was negative. Fourteen months after diagnosis and with continued healing of the bone graft, using intensity-modulated radiation therapy techniques, 4500 cgy, in 25 fractions, was delivered to the primary site of tumor. Subsequently, 2 additional courses of Maintenance Therapy completed approximately 17 months of treatment. End-of-treatment evaluations included PET/CT scan, cross-sectional imaging, and J Pediatr Hematol Oncol Volume 36, Number 6, August
2 Zwerdling et al J Pediatr Hematol Oncol Volume 36, Number 6, August 2014 FIGURE 1. Hematoxylin and eosin staining of primary tumor (A: 20; B: 100). bilateral bone marrow aspirates and biopsies, did not demonstrate disease. Pathologic Findings Soft tissue and bone measuring 1 cm in largest dimension were evaluated for histology from the primary tumor site. The neoplasm consisted of a uniform population of cells with enlarged, moderately pleomorphic nuclei, and occasional multinucleated cells. The degree of nuclear pleomorphism was atypical for Langerhans cell histiocytosis. Mitotic activity was over 20 mitoses in 10 hpf (Ki-67 of 10% to 30%, Fig. 2) and atypical, pyknotic nuclei were common with areas of tumor necrosis scattered throughout the neoplasm. The tumor invaded the bone and cartilage. Tissue was evaluated by electron microscopy and tumor cells identified by nuclear configuration and abundant cytoplasm. The tumor showed occasional cells with blunted pseudopodium, scattered numerous large lysosomes, and an electron-dense cytoplasm with ribosomes and occasional small profiles of rough endoplasmic reticulum. No intermediate-type filamentous whorls or Birbeck granules were identified. There were no features to suggest neuritic processes nor other features of a primitive neural TABLE 1. Treatment Schema Surgery Surgical resection2 Induction Vincristine, IV, 2 mg/m 2 1 dose Adriamycin, IV, 40 mg/m 2 1 dose (S Adriamycin 320 mg/m 2 ) Prednisone, PO, 40 mg/m 2 /d7d Cyclophosphamide, IV, 1000 mg/m 2 1 dose with mesna 400 mg/m 2 2 doses Cycles repeated every 3 wk, 9 Maintenance I Vincristine, IV, 2 mg/m 2 1 dose Prednisone, PO, 40 mg/m 2 /d7 d (held last 2 cycles) Cyclophosphamide, IV, 1000 mg/m 2 2 doses with mesna 400 mg/m 2 4 doses Cycles of chemotherapy repeated every 4 wk, 7 Radiation 4500 cgy to local site of disease Vincristine, IV, 2 mg/m 2 X 1 dose, weekly X 6. Maintenance II Vincristine, IV, 2 mg/m 2 1 dose Cyclophosphamide, IV, 1000 mg/m 2 2 doses with mesna 400 mg/m 2 4 doses Cycles of chemotherapy repeated every 4 wk, 2 nor glial tumor. Immunohistochemical results are shown in Table 2 and Figure 2. Tumor tissue was subjected to analysis for BRAF and found to harbor a known mutation (V600E). Literature Review and Discussion Tables 3 and 4 summarize 53 collected cases of LCS as published in the world literature as of January (We are also aware of 4 other cases involving children aged 2, 7, 15, and 18 years and 2 others in adults aged 22 and 31, but have insufficient information about these cases. These cases were reviewed by one of us (R.J.) and have never been published. However, attempts to gather additional information beyond the diagnosis were unsuccessful, and therefore, not included in our analysis.) Approximately 53% were reported to involve a single-site/single-organ. For patients with single-site/single-organ disease, 11 (39%) were reported to be in remission, as opposed to 5 of 25 with multisite/multiorgan disease (20%). Patients presenting with multisite/multiorgan disease fared very poorly with 64% dead and another 16% either alive with disease or without follow-up. It is likely that many of the patients reported as alive with disease eventually died from the process. For patients who presented with single-site/single-disease, lymph nodes, and skin were most frequently reported, similar to patients with multisite/multiorgan disease. Initiation of therapy and the actual treatment details are poorly reported precluding comparisons. Details of surgery, especially related to the intent to remove all known disease and the subsequent evaluation of resection margins for disease are absent in most of the cases reported to date. Less information regarding radiation therapy is given. Tables 5 and 6 summarizes treatment-related outcome as described for reported cases. Although all patients had lesional biopsy for diagnostic purposes, 43 (81%) went on to receive other treatments with either surgery only (n = 5), radiation only (n = 2), chemotherapy only (n = 19), or multimodality therapy (n = 17). Ten patients were either not treated or case reports did not so state. Three patients received liver (n = 1) or stem cell transplants. Two cases reported by Chung et al 43 are not included in this analysis. In case 1, there is a lack of Ki-67 reporting and while the text described sarcomatous changes the CD1a illustration is poor and not convincingly membranous. They also describe widespread disease without any masses and no results of the bone marrow evaluation are given r 2014 Lippincott Williams & Wilkins
3 J Pediatr Hematol Oncol Volume 36, Number 6, August 2014 Langerhans Cell Sarcoma CD1a (20X) CD207 (20X) S100 (20X) Ki-67 (20X) FIGURE 2. Immunohistologic reactivity of primary tumor. The second case is incompletely documented and without any illustrations. Langerhans cells are primarily charged with antigen recognition, processing, and presentation to T cells. First identified in 1868 using gold chloride staining technique, they were assumed to be of nerve origin based on morphology. It is now known, they are derived from fetal liverderived monocytes which populate the outer layer of the TABLE 2. Immunohistologic Results Positively Reactive Immunostaining CEA (perinuclear, 10% of cells) CD1a (diffuse cytoplasmic, membranous) CD43 (diffuse, membranous) CD68 (perinuclear) INI-1 (strong, diffuse nuclear positivity)* Ki-67 60%-70% of tumor nuclei PGP 9.4 (faint, membranous) S-100 (diffuse, cytoplasmic, nuclear) Vimentin (diffuse, intense cytoplasmic) CD207 *Normal (expected). Nonreactive Immunostaining Synaptophysin EMA GFAP CD99, myeloperoxidase AE-1/AE-3 Myogenin, desmin CD34, CD117, CD3, CD15, CD20, CD21, CD23, CD30, CD35, CD45, CD56 HMB-45 Melan-A, tyrosine hydroxylase epidermis before birth. 44 During inflammatory states, they may be replaced by blood-derived Gr-1 Hi monocytes. Other data support the separate ontogeny from other dendritic cells such as flt-3 independence, and required IL ,46 Malignant Langerhans cells must be distinguished from class I histiocytes and include such morphologic features as increased nuclear:cytoplasmic ratio, nuclear pleomorphism, and bizarre mitoses. Specific immunostaining is required for the accurate diagnosis of Langerhans cell neoplasms and may include CD4, CD1a, S-100, and/or the electron microscopic identification of Birbeck granules. Alternatively, Birbeck granules may also be identified by CD207 reactivity (Langerin). CD207 appears to recognize a c-type lectin, found on Birbeck granules, but the pattern of staining clearly shows more than just the granule itself. This lectin participates in internalizing antigen and allows processing of antigen for presentation to T cells. However, Birbeck granules many not be observed in all cases of LCS. 12 In reviewing the literature, it is apparent that LCS may arise de novo or be observed in other disorders. Several cases have been reported in myeloproliferative syndromes, other histiocytic disorders, B-lineage leukemia, follicular lymphoma, dermal lentigines, and after liver transplantation. Several authors provided details about chemotherapy given to these patients. Most used CHOP but several reports of MAID (mesna, doxorubicin, ifosphamide, dacarbazine) and other agents appear in the literature. 8,10,37 In addition, Keklik et al, 47 attempted to use 2-CDA for a primary tumor in the nasopharynx. However, new disease r 2014 Lippincott Williams & Wilkins 421
4 Zwerdling et al J Pediatr Hematol Oncol Volume 36, Number 6, August 2014 TABLE 3. Single-Site/Single-Organ Cases References Age (y) Sex Site Therapy Outcomes M Flank mass Surgery M Skin Surgery M Skin Surgery Liver transplant F Lymph node M Lymph node Marrow transplant M Skin Surgery M Lymph node M Skin Unknown M Skin Myeloid leukemia Stem cell transplant M Bone M Lung Surgery F Lymph node with disease F Skin Surgery with disease F Bone Surgery with disease M Lymph node with disease F Skin Surgery with disease F Skin Surgery Died at 14 mo M Lymph node Died at 7 mo F Skin Died of disease M Lymph node Died at 1 mo Lymph node Unknown Dead F Bone Surgery Dead 10 mo M Lymph node None Dead 3 mo M Skin Surgery Not available M Lung Not available F Skin Not available Not available M Lymph node Unknown No data F Lymph node chronic leukemia Hospice care No data was detected and treatment was changed to etoposide, ARA-C, cis-platin, and methylprednisolone without success. for class I histiocytic disorders may consist of cyclosporine, prednisone, etoposide, and vinblastine, but only 1 report has been published for LCS. 47 Some authors have suggested chemotherapy used for sarcomas treatment is suited for LCS and this was the approach used when treating our patient. 40 However, reviewing the poor outcomes should raise concern about its efficacy, even in the setting of single-site/single-organ disease. Our initial impetus for this review was an attempt to design a treatment plan for this young patient reported. With the few patients reported, and virtually no data for young patients, we were left trying approaches which have proved successful for treating sarcomas in children and young adults. We therefore began therapy with aggressive surgical resection at the primary tumor site, returning the patient to the operating theater after definitive diagnosis and staging evaluation. The location of tumor, with extension near the spinal cord did not allow for a wide surgical excision with negative margins. However, this approach did result in additional tumor removal during a second surgical procedure. With little data to choose chemotherapy, we decided on CHOP based on historical considerations and the fact that some of the drugs have been used to treat other histiocytic disorders. Once a cumulative dose of anthracycline equaled 320 mg/m 2,we eliminated further doxorubicin, and continued therapy with vincristine, prednisone, and cyclophosphamide. One limitation of this approach was the possibility that steroids were slowing bone engraftment and healing at the site of surgical reconstruction. We felt it important to have adequate bone healing before initiating radiation therapy because of the long-term consequences related to bone graft demise. Therefore, 2 months before initiating local radiation therapy, prednisone was also discontinued. Furthermore, the extensive surgical grafting and possible slowing of bone healing by steroid therapy delayed local control measures. Most sarcoma therapy recommendations begin local control earlier in the course of therapy. Indeed, we were concerned that delaying radiotherapy might allow local recurrence and performed a PET/CT scan about 5 months into treatment. A site of modest activity near the r 2014 Lippincott Williams & Wilkins
5 J Pediatr Hematol Oncol Volume 36, Number 6, August 2014 Langerhans Cell Sarcoma TABLE 4. Multisite/Multiorgan Disease Cases References Age (y) Sex Initial Sites Therapy Outcomes M Lymph nodes, skin M Lymph nodes, skin F Gall bladder, lymph nodes Surgery 4 This study 7 F Bone marrow, soft tissue Surgery F Lymph nodes Chronic myeloid leukemia M Skin, lymph nodes, lung with disease F Skin, neck mass, lung Surgery with disease M Lymph nodes, lung, rib with disease F Lymph nodes, skin Dead at 2 mo M Mediastinum, liver, spleen None Dead at 3 wk F Skin, lymph nodes, lung Dead at 2 y F Skin, lymph nodes, lung, spleen Dead M Lymph nodes, lung, rib Dead M Spleen, skin, lymph nodes, bone marrow Dead at 9 y M Bone marrow, lung, lymph nodes, liver Dead F Lymph nodes, liver, spleen Dead at 10 mo M Mediastinum, lung Dead at 4 mo 18 37? Skin, lymph nodes, lung Dead at 5 mo M Spleen, skin Dead at 10 mo F Skin, bone marrow Unknown Dead at 3 mo M Skin, neck Surgery Dead 3 mo F Lymph nodes Unknown Dead at 2 d M Subcutaneous Dead at 1 y M Lung, lymph nodes, bone marrow Not available Not available M Lymph nodes Dead at 7 mo primary tumor location was uncovered. Very little data are available to assess the role of PET/CT in this disease, 41 so it was felt additional information would be of importance. Therefore, a CT-guided biopsy was performed. The tissue obtained did not show any evidence of tumor and chemotherapy proceeded for an additional 11 to 12 months. The rarity of LCS is likely to preclude any uniform clinical trials. However, the true incidence of LCS is unknown and it may be misdiagnosed as one of the other histiocytic disorders or even a granulocytic sarcoma. If the published reports regarding age distribution are accurate, many individuals may never receive therapy, especially for older patients where CHOP or other chemotherapy would be poorly tolerated. Recent reports of mutations in BRAF merit consideration and comment. BRAF, a serine/threonine protein TABLE 5. Treatment-related Outcome Treatment Number Dead With Disease Unknown Surgery only Radiation only only Multimodality Unknown/ none Total kinase, is recruited by activated RAS and transported to the cell membrane where it is then activated. 3,27,48 Activated BRAF then activates MEK and eventually regulates gene expression via ERK. Mutations in the glycine-rich loop/ activation segment may lead to destabilization of inactive protein and result in a constitutively activated form of BRAF, which may increase MEK-ERK signaling by up to 700-fold. 49 Many tumors have been described to have activating mutations in BRAF including melanoma, thyroid cancer, hairy cell leukemia, and sarcomas. A recent report by Chen et al, 27 describes an activating BRAF mutation in LCS, the same mutation observed in our patient. Few other genetic abnormalities are known to exist in LCS tumors and given the poor outcome for these patients, we suggest BRAF testing be performed for future patients. Although this mutation has been reported in other histiocytic disorders and is not specific for LCS, it may help to distinguish this disorder from other tumors. Introduction of vemurafenib, a BRAF inhibitor, may allow rational exploitation of this mutation for treatment purposes, especially in older individuals where combined modality therapy is expected to be poorly tolerated. 42,50 In summary, we report a young patient diagnosed with LCS. This is a highly aggressive neoplasm and patients who present with multisite/multiorgan disease are unlikely to benefit long-term from currently employed treatments. The best approach to treatment is unknown but some patients, especially with single-site/site-organ disease, may benefit from aggressive surgery, chemotherapy, and additional r 2014 Lippincott Williams & Wilkins 423
6 Zwerdling et al J Pediatr Hematol Oncol Volume 36, Number 6, August 2014 TABLE 6. Disease Outcome by Site Disease Total (%) (%) With Disease (%) Dead (%) Other (%) Single-site/single-organ 28 (100) 11 (39) 5 (18) 7 (25) 5 (18) Multisites/multiorgans 25 (100) 5 (25) 3 (12) 16 (64) 1 (4) local control with radiation. Tumor evaluation for BRAF mutations may allow better diagnosis, therapeutic options, and should be studied in this disease. REFERENCES 1. International Classification of Diseases for Oncology, 3rd Edition (ICD-O-3). C Available at: who.int/classifications/icd/en/. 2. Swerdlow SH, Campo E, Harris NL, et al. World Health Organization Classification of Tumours: Pathology and Genetics of Tumours of Hematopoietic and Lymphoid Tissues. Lyon, France: IARC Press; Badalian-Very G, Vergilio JA, Fleming M, et al. Pathogenesis of Langerhans cell histiocytosis. Annu Rev Pathol. 2013;8: Subbiha V, Subbiah IM. 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