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TESTICULAR MYELOID SARCOMA: A SYSTEMATIC REVIEW OF LITERATURE
To review literature for the clinical characteristics, treatment and prognosis of reported cases of testicular myeloid sarcoma (TMS).
The clinical data of TMS patients were reviewed, including their clinical features and treatment, and were evaluated.
A total of 52 cases of TMS were studied. The median age was 42 years old (50 patients’ data) with age range of 0.17 to 79 years. Mostly, unilateral with left side being more common. Treatment methods given included combinations of surgery, chemotherapy and hematopoietic stem cell transplantation. 14 cases were misdiagnosed initially due to histopathological or clinical similarities. Most of the patients were treated with AML like chemotherapy. Rarely, patients were treated only with orchiectomy. Only three cases underwent HSCT for TMS. Majority of the patients died irrespective of treatment protocol followed suggesting the poor prognosis in TMS cases.
The incidence of TMS is low, hence the current data is still immature regarding the guidelines. The existing data is based on the experience with the MS involving the more common sites. As per the current literature, combined chemotherapy regimen of anthracycline and cytarabine combined with HSCT can achieve better clinical efficacy.
Myeloid sarcoma; acute myeloid leukaemia; chemotherapy; testis; chloroma
Granulocytic sarcoma (GS), commonly known as myeloid sarcoma (MS) or chloroma is an extramedullary neoplasm comprised of leukemic granulocytes organized as solid deposits, found either in isolation or in association with leukemias, most commonly in association with acute myeloid leukemia (AML). Rarely, MS is also seen in conjunction with myeloproliferative neoplasms (MPN), myelodysplastic syndrome (MDS) and the blast phase of chronic myelogenous leukemia (CML). MS has been recently been included as a major subgroup in the WHO classification of myeloid neoplasms (2). The American Cancer Society in 2018 reported 9310 newly diagnosed cases of testicular cancer in the United States alone, with a mortality of 5% in total. The majority of testicular malignancies (approximately 85%) occur in the reproductive age group and hence it affects the most functional group of general population (3). Myeloid sarcoma accounts for 2-8% of all cases of AML and 4.5% of all CML cases. Clinically depending on the time of occurrence, MS is categorized into three different groups (Table 1) as follows-  Concurrent, when primary hematological disease and MS is diagnosed at the same time  Isolated, when MS is the sole finding without any evidence of leukemia/MPN etc.  Secondary, when MS develops in a known case of leukemia/MPN signifying either relapse or blast crisis.
While almost any site may be involved in MS, commonly afflicted sites include lymph nodes, skin, orbit and the head and neck region (4–8). However, testes are an uncommon site of involvement in this condition. Large institutional case series of 27 (Suh et al), 61 (Neiman et al) and 92 cases (Pileri et al) have reported incidence of Testicular Myeloid Sarcoma (TMS) of only 4%, 5% and 6.5% respectively (9–11). This paper aims to sensitize readers to keep low threshold for TMS and also discusses the challenges in diagnosis and management.
Search strategy: This systematic review investigated all articles as per the PRISMA guideline for systematic review. All case reports, case series, studies that has been published until December 2018 were investigated. By using the MeSH terms “testis and myeloid sarcoma”, “testis and Chloroma”, ‘testis and granulocytic sarcoma”, we searched the Medline/PubMed, and we also searched google scholar with the above-mentioned terms. We searched the references of all the articles that has been published regarding this.
Selection and inclusion criteria: The relevant literature search was done by two independent and trained researchers. Abstracts of all available articles were examined in order to ensure includability. Articles that were original, included humans, in English, had an abstract, and had a complete report were included in the review. Articles that were incomplete, published in other language, did not have an abstract or convincing clinical detail were excluded. A total of 62 articles were identified over the span of past 40 years [1988 to 2018]. Among these 5 articles were excluded as they were not in English language, 4 articles were excluded as they were incomplete. Hence a total of 53 articles were included in this analysis (Flow diagram 1).
Data extraction: One reviewer independently extracted the data and entered these in a predefined data sheet. Details of demographic, clinical, histopathological, management, follow up and outcome related data were extracted from each of the article. Details of treatment with chemoradiotherapy and/or Stem cell transplant were also obtained.
Data analysis: Extracted data was entered in Microsoft excel version 16. 17 spread sheets. In statistical analysis means and percentages were reported for continuous and categorical variables respectively.
A total of 53 cases reviewed from literature were included in our study cohort. Patient characteristics including age, side of involvement, presenting features with treatment and outcome were manually abstracted for analysis and are shown in Table 1. Out of 53 cases, an interesting case of TMS was reported in a hermaphrodite (case no. 39) (12). Our study cohort had the median age of 42 years (51 patient’s data) with age range of 0.17 to 79 years. Mostly, testicular involvement was unilateral with left sided involvement being commoner than the right. Most common pattern of testicular involvement was left only (18 cases) followed by right only (14 cases) followed by bilateral (5 cases). In 5 cases, TMS was unilateral to begin with followed bilateral involvement. No data of side of involvement was available in 10 cases. Our review showed that the most common presenting complaint or symptom described were scrotal swelling, scrotal mass, overlying skin discoloration and testicular pain (case no 12, 25 and 52). In two cases, a testicular mass was detected incidentally during an evaluation for left arm paresis (case 15) and ileal mass (case no 24) respectively.
4 out of the 47 cases with available records in our study, were initially misdiagnosed as epididymitis, orchitis and spermatocele. 10 of the 47 cases were diagnosed as lymphoma (10, all non-Hodgkin’s lymphoma) and plasmacytoma (1). 7 cases of the misdiagnosed NHL even received chemotherapy (case no 13, 14, 19, 23, 24, 44 and 47). Patients who were misdiagnosed, received treatment on a variety of chemotherapeutic regimens like RCHOP, CHOP, VEMP and CVP. With introduction of flowcytometry and advancement in staining techniques, the incidence of misinterpretation during microscopic examination have gone down significantly.
Other sites of involvement by leukemic infiltrates
We noted that in few of the reviewed patients, MS also involved parts other than testes. In 14 patients, we found one or sites of MS involvement including the skin (case nos 15,16,17,18,24,27,28), ileum (case no 22,24), orbit (case no 33), lymph nodes (case nos 14,27,29,32), peritoneum (case no 15) retina (case no 33), psoas (case no 27), forearm (case nos 18, 44), nasolabial fold (case no 47) and stomach (case no 15). Three patients (case nos 4,7 and 29) had retroperitoneal lymphadenopathy related hydroureteronephrosis. The impending organ dysfunction can be prevented with timely intervention.
Stratification of TMS cases
By analyzing the clinical data, we were able to divide the cases into three clinical settings as mentioned above in introduction section. We found 6 concurrent (C) TMS cases, 23 isolated (I) TMS cases and 17 secondary (S) TMS cases. In four patients (case no-17,18,48,49), no data was available to categories the patient into one of these three groups. In patients with S TMS and C TMS, the underlying diseases were AML (11 cases), CML (4 cases), CMML (3 cases), APML (3), MDS (2). Time duration of diagnosis of primary malignancy to the development of TMS is mentioned in Table 1 wherever the data was available.
Various treatment modalities using different therapeutic regimens including various combinations of chemotherapy, radiotherapy, HSCT and experimental therapy. Table 2 outlines the various regimens implemented for the treatment of TMS by various authors. As evident as well, there is a lack of protocol driven therapeutic guidelines for treatment of TMS. Table 2 also mentions patient treatment follow-up details. We were unable to gather follow-up data for 10 out of the 53? cases due to lack of information. 1 patient was lost to follow-up. In 17 out of the remaining 42 cases, patients were reported to be disease-free following treatment. Analysis showed that 20 patients were deceased at follow-up. The remaining patients were living either with disease or undergoing treatment (Case nos 11, 26, 28, 29, 30, 34). 2 cases died from causes unrelated to TMS or hematological disease.
Amongst the cases with available data, 9 cases of TMS were treated with orchiectomy only without chemotherapy or radiotherapy. Details of their follow-up are outlined in table X. case 27 (died due to progression of disease), case 30 (relapsed on other side after an year), case 31(NED till last f/u of 17 months), case 35 (lost to follow up), case 37 (NED till last f/u of 7 yrs.), case 46 (systemic and CNS relapse after 9 months), Case 47 (systemic relapse in 6 months), case 48 (details not available) and case 53 (NED till last f/u of 13 months). <Maybe a line about the standard guidelines and what it changed in the discussion.>
In this study, we investigated a series of TMS cases with regards to clinical presentation, treatment and outcomes. Goyal et al reviewed ten years (2004-2013) of data from the National Cancer Database (NCDB) and found 746 registered patients with a new diagnosis of extramedullary MS (13). Of these, 43 cases (5.8%) were found to be cases of MS with gonadal involvement. In that study, median age of MS in general was 59 years (range, 41-73) at presentation. They mentioned 43 cases of MS (5.8%) involving reproductive organ without mentioning TMS in isolation. Median age of this subcategory was 51 years which is almost a decade younger than of MS as a whole (13). In our review of TMS cases, median age was 42 years. This highlights an important fact in that MS resulting in gonadal involvement is seem to occur at an earlier mean age which means affecting the reproductive ae group.
Clinically, TMS usually presents as scrotal masses which is the usual finding for all testicular pathologies. Most common clinical presentation described by the authors were scrotal swelling, mass, acute testicular pain (case no 1), overlying scrotal skin discoloration. There is one exceptional case of development of TMS in ovotestis in a true hermaphrodite who presented for evaluation of mass below umbilicus (12). Acute testicular pain as the one of the presentations of TMS was reported by three authors (case no 12,25,52) (14,15). This could be misleading and confusing with other acute testicular pathologies like testicular torsion and Fournier’s gangrene. Hence, ED physicians must be aware of this atypical presentation of MS. In the non-leukemic patients, a median of 5 months (range: 2-44 months) elapsed between the diagnosis of MS and acute leukemia. Our review revealed that TMS developed more frequently unilaterally and on the left side.
MS is primarily associated with AML, FAB M2. Isolated MS without concurrent leukemic disease warrants aggressive therapy as the vast majority of non-leukemic patients in such settings ultimately develop frank systemic disease within one year. Breccia et al in their study of 12 cases of MS found the median survival time from diagnosis in MS to be only 7 months (range: 1-49 months). There was one exception where the patient did well for 49 months after bone marrow transplantation. The testes are considered pharmacological sanctuaries that enable survival of leukemic cells as a result of poor penetration by anti-cancer drugs. Many autopsy-based studies in the past have suggested that microscopic testicular involvement by leukemic infiltrates is commoner in acute leukemias when compared to chronic leukemias and lymphomas (16). Amongst acute leukemias, ALL is more commonly associated with isolated testicular relapse rather than AML (17). Although it is difficult to predict which patients have a higher propensity to develop MS, studies have found monocytic morphology (FAB M4 and M5), t(8;21), inv (16) and 11q23 mutations to be risk factors (18). Furman et al in their autopsy series reported 45% of patients with AML FAB M4 and M5 subtype, and 12-30% with other FAB subtypes to be have had microscopic testicular leukemic infiltrates (19).
Prognosis wise, the literature review revealed a divided opinion regarding the impact of MS on the prognosis of leukemia. While Park et al suggested MS to be associated with a poor outcome, others like Dusenbery et al have reported better prognosis (20,21). Contrary in conclusion to the study by Goyal et al, a study of 92 cases of MS by Pileri et al found that clinical aggressiveness of MS was not found to be associated with primary hematological disease, demographics or cytogenetics (11,13). An interesting observation was noted in the median overall survival (OS) by Goyal et al in their review of 746 MS patients registered with NCBD. They found that median OS was best (>30 months) in MS involving reproductive and digestive systems as opposed to involvement of head, neck, kidney, retroperitoneum, skin, kidney, bladder (15-30months), nervous system, bone, cardiac or mediastinum (<15months). The most likely explanation for the good prognosis in MS of the reproductive and digestive system was linked to early symptom onset and detection (13). In our review of TMS cases, median survival could not be studied due to variable reporting of timepoints for survival analysis.
A histological diagnosis of TMS is very challenging especially in the absence of any history of associated malignancies, minimal myeloid cell lineage precursors and Auer rods in the histopathological specimen. Due to morphological similarities, MS can be confused with other malignancies such as DLBCL, plasmacytomas and other high-grade neoplasms. Incidence wise, testicular lymphoma and plasmacytomas are much more common than TMS (1). A clinical distinction from lymphoma becomes difficult in cases where MS has a higher percentage of blast cells. As suggested in our review, due to this diagnostic confounder, the diagnosis was not only delayed but the treatment as well as a result was compromised. This fact becomes especially important in cases of isolated TMS where there is no history of leukemia to guide pathologists to suspect MS in a given case. Similarly, confusion with epididymitis, orchitis and other testicular conditions can also delay diagnosis. Ferry et al in their paper suggested the following subtle findings that favors a diagnosis of MS over lymphoma viz. smaller cell size, a more evenly distributed chromatin, rounded or indented nuclei instead of sharp angulation and the presence of eosinophilic myelocytes or eosinophilic precursors. Histochemical stains for chloroacetate esterase, myeloperoxidase and lysozyme also help confirm the diagnosis of MS (1). Similarly, flow cytometry can also confirm the diagnosis. MS cells are negative for B and T–cell associated antigens and positive for CD13, CD68 (markers for monocytic/macrophagic cells) and CD117 (markers for myeloid differentiation) (22). Misdiagnosing TMS with other malignancies, can significantly delay diagnosis and result in both inadequate and incorrect management. Therefore, it is prudent to suspect and rule out TMS during the work-up of testicular lymphomas or plasmacytomas.
The literature on genomic alterations in MS is lacking and mostly limited to individual case reports. As depicted in our review, most of the reports lacked data on cytogenetics (Table 1). The challenge is especially daunting in cases of isolated TMS where, by the time the diagnosis is confirmed, a fresh sample is unavailable for performing karyotype studies. Recently, studies have found significant clinical utility in using chromosomal microarray analysis (CMA) using formalin-fixed paraffin-embedded (FFPE) tissues for detecting important genetic abnormalities in MS (23). It is important to understand the cytogenetic perturbations in AML patients during follow-up bone marrow examinations which may be of benefit in predicting future MS.
Radiologically, ultrasonography (USG) is usually the first modality of imaging when testicular enlargement is endorsed. Although none of the imaging findings are specific for MS, USG findings such as hypo-echogenicity, septations, increased vascularity with blood vessels arranged in palisading or basket pattern are commonly seen but not specific to TMS (24).
Currently available treatment options
Due to a lack of randomized prospective trials, there is no consensus on treatment of MS. In the past, attempts at localized treatment for focal or isolated MS have failed with the majority (88-100%) progressing to frank AML when compared with systemic chemotherapy (25,26). Hence, at present, the current National Comprehensive Cancer Network (NCCN) guidelines recommend that patients with MS be treated with AML-type chemotherapeutic protocols (27). Similarly, there is sparse data to address the type of chemotherapeutic regimens to use for MS. There are many different opinions in the medical community regarding the therapeutic management of MS. The available treatment modalities include chemotherapy, HSCT, radiotherapy (RT) and surgery. Isolated MS has superior event free survival (EFS) and OS compared to AML Not to forget about the correct diagnosis of TMS in association with APML, especially in the microgranular variant due to the fact that retinoids and arsenic compounds are well established treatment strategies with excellent outcome (28,29).
Although RT is often used in MS, there is no OS benefit. Reports by Tsimberidou et al, Kan et al and many others have not found any benefit in EFS with the use of RT (26). Role of RT is complementary to more definitive therapies. In case of TMS, almost all cases undergo orchiectomy. RT can be used as a therapeutic modality in localized MS, along with chemotherapy with the aim of consolidating induction; treating MS lesions that persist even after chemotherapy; treating limited focal recurrences after chemotherapy or HSCT; reducing large MS masses with the aim of relieving compression symptoms and mass effect. In case of TMS, we still do not have any concrete data supporting the use of RT. Rawal et al (case no. 25) used prophylactic RT (2600-cGy) along with chemotherapy and intrathecal methotrexate with favorable outcomes (14).
Hypomethylating agents are increasingly being used in the treatment of AML/MDS, especially as bridging therapy in old deconditioned patients (15). Data regarding utility in cases of MS (including TMS) is still immature and limited to case reports. Niscola et al reported a partial response with decitabine therapy in a case of multiple extramedullary MS developed after essential thrombocytopenia transformation (30). Similarly, prolonged partial response with 5-azacytidine in a case with tonsillar and cervical nodal MS was reported by Katagiri et al (31). In our review, we found only one patient (case no 6) who was treated with hypomethylating agents (32). Unfortunately, patient died secondary to IgM-aCL-mediated hyper coagulopathy.
Hematopoietic stem cell transportation
There is no randomized data supporting the role of HSCT in MS. However, recent retrospective studies have shown OS benefit in MS patients undergoing HSCT (11,33). Due to the relative rarity of TMS and the paucity of published reports with only 3 cases having received HSCT in our review, we lack data to analyze the significance of outcomes. All three cases were disease free till the last ate of follow up indicating that HSCT is the definitive treatment in TMS.
Rarely, there have been instances where patients with isolated and localized TMS, have a disease-free survival after initial management with chemotherapy. However, in general, such patients if not treated with HSCT, tend to develop frank systemic disease within a few months of MS diagnosis. An interesting observation by Choi et al in their review of 62 MS patients suggested that MS cases were found to have more mutations of the RTK-RAS pathway genes (26). Similarly, Chen et al found a higher percentage of MS cases with c-Kit reactivity (35). Recently, newer agents like FLT3 inhibitors, DNA methyltransferase inhibitors and farnesyl-transferase inhibitors in the treatment of AML and other myeloid malignancies are topics of research (33). These observations pave the way for future studies aimed at further elucidating their therapeutic and prognostic implications when used in the treatment of MS. Understanding the genetic profile of MS subtypes will expand the horizon of therapeutic options with novel targeted therapies.
Our data stresses the importance of an accurate and prompt identification of this rare form of AML and suggests that, even in patients with isolated MS, the early administration of AML-like intensive chemotherapy followed by bone marrow transplantation might reduce the risk of subsequent systemic disease. Clinical and histopathological recognition of MS remains a problem. Only by maintaining a high degree of suspicion will clinicians and pathologists be able to recognize this tumor in the majority of cases. Cytogenetic analysis should be part of the diagnostic and prognostic work-up to determine the best treatment strategy.
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