Gastrointestinal Myeloid Sarcoma a Case Presentation and Review of the Literature

Pouyan Kheirkhah1, Ana M. Avila-Rodriguez2, Bartlomiej Radzik1 and Carlos Murga-Zamalloa1.

1 Department of Pathology, University of Illinois at Chicago, USA.
2 Department of Internal Medicine, University of Illinois at Chicago, USA.

Correspondence to: Carlos A. Murga-Zamalloa, M.D. Department of Pathology, University of Illinois at Chicago, 840 S Wood Street, 260 CMET, Chicago, IL 60607. Tel: 312-413-3998. E-mail: catto@uic.edu

Published: November 1, 2021
Received: September 7, 2021
Accepted: October 19, 2021
Mediterr J Hematol Infect Dis 2021, 13(1): e2021067 DOI 10.4084/MJHID.2021.067

This is an Open Access article distributed under the terms of the Creative Commons Attribution License
(https://creativecommons.org/licenses/by-nc/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Myeloid sarcomas can be detected in up to 30% of acute myeloid leukemia cases or occur de-novo without bone marrow involvement. The most frequent localization of myeloid sarcomas in the abdominal cavity is the small intestine, and gastric presentations are infrequent, frequently misdiagnosed, and a high level of suspicion should exist when the characteristic histomorphology features are present. The current review features a case report with gastric presentation of myeloid sarcoma in a patient with a diagnosis of acute myeloid leukemia with trisomy 8. In addition, a review of the literature of intestinal-type myeloid sarcomas shows that less than 15% of these cases have been reported in the stomach. The most common molecular aberrancy detected in intestinal myeloid sarcomas is the fusion protein CBFB-MYH11. A review of several large studies demonstrates that the presence of myeloid sarcoma does not constitute an independent prognostic factor. The therapeutic approach will be tailored to the specific genetic abnormalities present, and systemic chemotherapy with hematopoietic stem cell transplant is the most efficient strategy.



Case Presentation

A 60-year-old male with a relevant past medical history of hepatitis C infection, methadone use, and heroin addiction was surgically managed for a toe infection. Persistent leukocytosis was noted despite antibiotic treatment, and a microscopic review of the peripheral blood smear demonstrated circulating blasts with left shift in granulocytes. Bone marrow biopsy evaluation demonstrated 70-80% myeloblasts, and the concurrent flow cytometric analysis show myeloblasts with the expression of CD34, CD117, CD33, CD11c, CD13, and negative for CD56. A diagnosis of acute myeloid leukemia was rendered. Karyotype analysis of the bone marrow aspirate demonstrated trisomy 8 (47, XY, +8[2]/46, XY[18]). Molecular testing demonstrated mutations in SRF2, TET2, and KRAS genes (SRSF2 P95H, TET2 F1901Lfs*4, TET2 S585*, KRAS A146T). During admission, the patient complained of persistent abdominal pain, with coffee-ground emesis and one episode of melena. Computed tomography showed thickening of the gastric wall near the gastroesophageal junction with multiple enlarged lymph nodes. An urgent esophagogastroduodenoscopy revealed a large, firm, ulcerated, and partially circumferential mass in the cardia extending into the fundus, with multiple ulcers within the gastric fundus and proximal duodenum. Histologic evaluation from biopsies of the cardia mass demonstrated dense submucosal aggregates, composed of large cells, with lobated nuclear contours and fine and dispersed chromatin with inconspicuous nucleoli (Figure 1). Immunohistochemical stains demonstrated that the infiltrates  were positive for MPO, CD43, with weak CD68 expression, and negative for CD34, CD117, CD20, CD79a, CD5, CD3 and cyclin D-1 (Figure 1). A diagnosis of myeloid sarcomas was established. The following questions arise from this case: How often is myeloid sarcoma identified in the stomach, and what are the specific histological features that help establish the diagnosis? Do intestinal myeloid sarcomas share common molecular features? What is the prognosis and management of myeloid sarcomas? 
Figure 1 Figure 1. Representative pictures of gastric cardia mass. Each immunostain or tissue stain is indicated within each picture. Abbreviations: Hematoxilin and Eosin stain (H&E). Myeloperoxidase immunostain (MPO). 

Definition and Frequency of Myeloid Sarcoma

Myeloid sarcoma (MS) is defined by the presence of neoplastic extramedullary infiltrates of myeloid precursors at a single or multiple sites, and the term leukemia cutis is reserved for when those infiltrates are present in the skin.[1] The incidence of myeloid sarcoma is variable, it has been reported in 7% to 30% of the cases of acute myeloid leukemia,[2] and this variability will largely depend on the criteria utilized to define extramedullary involvement. The majority of the studies that identified myeloid sarcoma by physical examination and/or imaging studies demonstrated a prevalence in the range of 20% to 30%, in contrast to studies with the only biopsy-proven diagnosis that identified a prevalence of 7-10%.[1-4] Position-electron tomography (PET) has also been utilized, with reported increased sensitivity compared to physical exam or other imaging techniques.[5,6] A single prospective study that compared PET-imaging, clinical examination, and histologic analysis, reported an incidence of 22% with a sensitivity of 77% and specificity of 97% for FDG-PET.[5]
The more frequent localizations of myeloid sarcoma will also depend on the methodology utilized for its detection. Detection by physical examination identifies, as the most frequent sites, the gingiva, spleen, and lymph nodes.[2] When imaging or biopsy studies are utilized during the diagnosis, the most frequently involved sites include the lymph nodes, testis, bone, and soft tissue.[1,7] Some studies do not consider gingival, lymph node, liver, or splenic involvement as myeloid sarcoma, as the hypertrophy identified during physical examination may constitute migration/extravasation of blast precursors and not a truly ‘tumor’ lesion.[5,8,9]
Myeloid sarcoma can occur de-novo without simultaneous bone marrow involvement, and in these instances, the diagnosis may be challenging, as it can be misdiagnosed as lymphoma.[10,11] Moreover, a diagnosis of myeloid sarcoma can precede the occurrence of acute myeloid leukemia, or the occurrence of myeloid sarcoma can be the sole manifestation of relapse. No specific risk factors for myeloid sarcoma are identified; however, surface expression of CD56,[12] and CD11b,[2] and monocytic differentiation[4] are reported to be associated with an increased risk for the presence of extramedullary involvement by leukemia.

Intestinal Myeloid Sarcoma

Involvement of the gastrointestinal tract by myeloid sarcoma is not a common occurrence, and the most involved site is the small intestine. A PubMed search using a combination of the terms’ intestinal’ ‘gastric’ ‘myeloid sarcoma’ and ‘granulocytic sarcoma’ identified 58 individual clinical case reports of myeloid sarcoma localized in the intestinal tract. From the list, only 7 cases were reported to be localized in the gastric compartment (Table 1). The clinical presentation for gastric myeloid sarcoma was characterized by non-specific symptoms, including persistent vague abdominal pain and vomiting. Upper gastrointestinal endoscopy usually revealed thickening of the stomach mucosa with hyperemic lesions and occasional nodularity or tumor-forming lesions. Imaging studies, including computer tomography (CT) scans, often revealed enlarged lymph nodes around the stomach. In the current literature review series, 60% of the cases (n = 50) did not feature synchronous bone marrow involvement by acute leukemia, making the diagnosis more challenging. Importantly, five reported cases featured relapse of acute myeloid leukemia in the form of gastrointestinal myeloid sarcoma, and three of those cases were post stem cell transplantation. 
Table 1 Table 1. Identified reported cases of myeloid sarcoma within the intestinal wall. 

Histologic Evaluation and Differential Diagnosis of Intestinal Myeloid Sarcomas

Myeloid sarcomas are histologically characterized by dense submucosal infiltrates, predominantly composed of large cells with cleaved or slightly folded nuclear contours, variable amounts of cytoplasm, and finely dispersed chromatin.[11] However, similar features can be identified in lymphoid and non-lymphoid neoplasms in the intestinal tract; so, the differential diagnosis includes mature lymphoproliferative neoplasms like diffuse large B-cell lymphoma, the blastoid variant of mantle cell lymphoma, and mature T-cell neoplasms with secondary GI tract involvement or primary to the GI tract. Non-hematolymphoid neoplasms that may show similar morphological features includes poorly differentiated carcinoma and melanoma. The possibility of benign extramedullary hematopoiesis (myeloid metaplasia) should also be included in the differential diagnosis; however, those are characterized by multilineage hematopoietic elements at progressive stages of maturation.
Myeloid sarcoma localized within the intestinal tract is not a frequent presentation and lacks specific clinical symptoms; therefore, the diagnosis may remain elusive unless clinical suspicion and a careful histological analysis exist. A misdiagnosis of myeloid sarcoma is not uncommon,[11,13] one report indicated that 58% (n = 26) of cases were originally diagnosed as lymphoma,[14] and two independent reports demonstrated that 44% (n = 61) and 46% (n = 158) were initially mislabeled as lymphoma.[11,15] Therefore, immunohistochemical stains are required to establish a diagnosis, and a panel that includes myeloid-specific markers (MPO, CD117), should be included with any suspicious infiltrate. The current literature review demonstrates that the majority of the cases within the intestinal tract featured positive expression of either CD34 (91%, n = 36) or CD117 (93%, n = 29), and only a single report was identified with negative expression of both of these markers (Table 1).[16] Importantly, expression of either CD43 (94%, n = 17) and MPO (97%, n = 32) is frequently detected in the tumor cells (Table 1). Aberrant expression of associated lymphoid markers has been reported in cases of myeloid sarcoma, including CD3 and CD79a. The current review for the intestinal presentation of myeloid sarcoma shows that CD3 was positive in a single case,[17] and expression of CD5, CD20, and CD79a was not detected in any of the cases included. The current case report also demonstrated divergent CD34 and CD117 between the bone marrow biopsy and the stomach biopsies, a phenomenon previously described in leukemia cutis.[18]

Recurrent Cytogenetic Abnormalities in Intestinal Myeloid Sarcomas

The previous series indicated that trisomy 8 is commonly detected in cases of myeloid sarcoma[19] and leukemia cutis,[20] and the presence of chromosome 8 abnormalities are associated with worse responses to initial therapies and worse overall clinical outcomes.[21,22] Unlike the current case, the literature review did not identify any previous report of abdominal myeloid sarcoma with trisomy 8. Previous reports demonstrated a higher prevalence for abdominal localization of myeloid sarcomas that are positive for the CBFB-MYH11 fusion.[23] The largest series to date included 13 cases of myeloid sarcoma with an abdominal presentation, and 11 (85%) of those cases were positive for CBFB-MYH11 fusion protein.[23] The same report included an additional number of 22 cases that were identified from reported cases in the literature, and 20 (92%) of those cases were positive for CBFB-MYH11 fusion protein.[23] The current review of the literature identified 11 additional cases of intestinal myeloid sarcoma[17,24-33] that evaluated for genetic abnormalities by either cytogenetic or molecular testing, and the most common chromosomal rearrangement was inv(16) in 27% (3/11) of the cases (Table 2).
Table 2 Table 2. Identified reported cases with available molecular studies (not included in Dalland et al. reference # 12). References for the studies included: (13-23).

Prognosis of Myeloid Sarcoma

Poor outcomes with negative trends in the overall survival and event-free survival sarcoma have been associated with a diagnosis of myeloid sarcoma.[7,22] However, when adjusted to age and cytogenetic risk, myeloid sarcoma is not identified as an independent prognostic factor for overall survival,[2,4,34] and the overall 5-year survival rate for patients with concomitant myeloid sarcoma is no different from those without it.[1] A retrospective study that evaluated the clinical outcomes of 84 patients with acute myeloid leukemia (AML) patients positive for t(8;21)(AML1/ETO) included eight patients with extramedullary involvement with significant worst responses to initial induction chemotherapy. However, half of the patients with extramedullary involvement featured CNS leukemic infiltration,[21] and additional studies did not identify myeloid sarcoma as an adverse prognostic factor in this subset of cases.[4]

Management of Myeloid Sarcoma

The treatment of myeloid sarcoma will depend on the form of presentation and whether this occurs at the initial diagnosis or at relapse.[1] In the current era of targeted therapies, the consensus is to tailor the therapeutic approach based on the tumor’s genetic profile, and therefore molecular and cytogenetic testing are required to formulate the treatment strategies.[35]
As a rare condition, the lack of randomized controlled trials limits the treatment strategies for isolated myeloid sarcoma without bone marrow involvement. Retrospective series have demonstrated that delayed or localized therapy alone will almost always progress to AML.[1,35] Remission-type induction chemotherapy regimens have also been used in isolated myeloid sarcoma, demonstrating a decrease in the rate of progression and an increase in overall survival.[35,36] The role of hematopoietic stem cell transplantation (HSCT) following induction therapy is supported by retrospective studies, which indicate that allogeneic HSCT is associated with a 5-year overall survival rate of 48% and leukemia-free survival of 36%.[37] Localized radiation therapy (RT) has also been considered as consolidation treatment for isolated MS.[38]
Systemic treatment is the first-line option for myeloid sarcoma with concurrent marrow involvement at diagnosis. First-line treatments for gastrointestinal myeloid sarcoma usually include conventional induction chemotherapy with a combination of cytarabine and anthracycline agents.[39,40] Unfortunately, there have been no randomized trials comparing the different types of chemotherapy regimens and assessing the optimal AML remission-induction chemotherapy regimens in the setting of myeloid sarcoma with marrow involvement. However, autologous and allogeneic HSCT are usually considered as treatment intensification based on the superior outcomes with the use of HSCT in several retrospective studies.[37,38]
Isolated myeloid sarcoma at relapse is rare and usually precedes marrow relapse. For relapse after chemotherapy alone, strategies such as relapse-type chemotherapy regimens and localized radiation therapy (RT) are recommended.[1] Isolated myeloid sarcoma after HSCT can present as the first manifestation of relapse but has rarely been described, and currently, there is no established standardized management. The therapeutic strategies include donor lymphocyte infusion, tapering of immunosuppression, or enrollment in clinical trials.[41] Concomitant MS and marrow relapse are usually treated with reinduction chemotherapy taking into account the possibility of HSCT or RT.[38] In the setting of marrow and myeloid sarcoma relapse after HSCT, the survival is poor and investigational agents or palliative care measures must be considered.[1]
Finally, noncontrolled anecdotal reports have described the use of highly targeted therapies as a treatment strategy for myeloid sarcoma. For example, the humanized anti-CD33 monoclonal antibody has been associated with good responses.[35,36] In addition, tyrosine kinase inhibitors have also shown promising results in a patient with myeloid sarcoma associated with FIP1L1- PDGFRA fusion gene and eosinophilia.[42]

Conclusions

Myeloid sarcoma can occur in up to 30% of newly diagnosed acute myeloid leukemia. According to the site presentation, it is usually identified by physical examination and imaging studies, and a confirmatory biopsy will be required in a proportion of the cases. Histology analysis shows overlapping morphology with mature lymphoproliferative neoplasms, and immunohistochemical analysis is required to establish the diagnosis. The most common site within the intestinal tract is the small intestine, and the expression of CD34, MPO, and CD117 are the most sensitive and specific markers. The aberrant fusion protein CBFB-MYH11 is the most predominant cytogenetic abnormality detected in intestinal myeloid sarcoma. A diagnosis of myeloid sarcoma does not appear to render a worse prognosis in comparison with patients that do not feature extramedullary disease. The clinical management of myeloid sarcoma will largely depend on the timing of the presentation and the underlying genetic landscape of the tumor.

References   

  1. Bakst RL, Tallman MS, Douer D, Yahalom J. How I treat extramedullary acute myeloid leukemia. Blood. 2011;118(14):3785-93. https://doi.org/10.1182/blood-2011-04-347229 PMid:21795742
  2. Ganzel C, Manola J, Douer D, Rowe JM, Fernandez HF, Paietta EM, et al. Extramedullary Disease in Adult Acute Myeloid Leukemia Is Common but Lacks Independent Significance: Analysis of Patients in ECOG-ACRIN Cancer Research Group Trials, 1980-2008. J Clin Oncol. 2016;34(29):3544-53. https://doi.org/10.1200/JCO.2016.67.5892 PMid:27573652 PMCid:PMC5074349
  3. Avni B, Rund D, Levin M, Grisariu S, Ben-Yehuda D, Bar-Cohen S, et al. Clinical implications of acute myeloid leukemia presenting as myeloid sarcoma. Hematol Oncol. 2012;30(1):34-40. https://doi.org/10.1002/hon.994 PMid:21638303
  4. Fianchi L, Quattrone M, Criscuolo M, Bellesi S, Dragonetti G, Maraglino AME, et al. Extramedullary Involvement in Acute Myeloid Leukemia. A Single Center Ten Years' Experience. Mediterr J Hematol Infect Dis. 2021;13(1):e2021030. https://doi.org/10.4084/MJHID.2021.030 PMid:34007418 PMCid:PMC8114885
  5. Stolzel F, Luer T, Lock S, Parmentier S, Kuithan F, Kramer M, et al. The prevalence of extramedullary acute myeloid leukemia detected by (18)FDG-PET/CT: final results from the prospective PETAML trial. Haematologica. 2020;105(6):1552-8. https://doi.org/10.3324/haematol.2019.223032 PMid:31467130 PMCid:PMC7271590
  6. Cribe AS, Steenhof M, Marcher CW, Petersen H, Frederiksen H, Friis LS. Extramedullary disease in patients with acute myeloid leukemia assessed by 18F-FDG PET. Eur J Haematol. 2013;90(4):273-8. https://doi.org/10.1111/ejh.12085 PMid:23470093
  7. Paydas S, Zorludemir S, Ergin M. Granulocytic sarcoma: 32 cases and review of the literature. Leuk Lymphoma. 2006;47(12):2527-41. https://doi.org/10.1080/10428190600967196 PMid:17169797
  8. Kobayashi R, Tawa A, Hanada R, Horibe K, Tsuchida M, Tsukimoto I, et al. Extramedullary infiltration at diagnosis and prognosis in children with acute myelogenous leukemia. Pediatr Blood Cancer. 2007;48(4):393-8. https://doi.org/10.1002/pbc.20824 PMid:16550530
  9. Muss HB, Moloney WC. Chloroma and other myeloblastic tumors. Blood. 1973;42(5):721-8. https://doi.org/10.1182/blood.V42.5.721.721
  10. Yamauchi K, Yasuda M. Comparison in treatments of nonleukemic granulocytic sarcoma: report of two cases and a review of 72 cases in the literature. Cancer. 2002;94(6):1739-46. https://doi.org/10.1002/cncr.10399 PMid:11920536
  11. Neiman RS, Barcos M, Berard C, Bonner H, Mann R, Rydell RE, et al. Granulocytic sarcoma: a clinicopathologic study of 61 biopsied cases. Cancer. 1981;48(6):1426-37. https://doi.org/10.1002/1097-0142(19810915)48:6<1426::AID-CNCR2820480626>3.0.CO;2-G
  12. Chang H, Brandwein J, Yi QL, Chun K, Patterson B, Brien B. Extramedullary infiltrates of AML are associated with CD56 expression, 11q23 abnormalities and inferior clinical outcome. Leuk Res. 2004;28(10):1007-11. https://doi.org/10.1016/j.leukres.2004.01.006 PMid:15289011
  13. Hagen PA, Singh C, Hart M, Blaes AH. Differential Diagnosis of Isolated Myeloid Sarcoma: A Case Report and Review of the Literature. Hematol Rep. 2015;7(2):5709. https://doi.org/10.4081/hr.2015.5709 PMid:26330997 PMCid:PMC4508548
  14. Menasce LP, Banerjee SS, Beckett E, Harris M. Extra-medullary myeloid tumour (granulocytic sarcoma) is often misdiagnosed: a study of 26 cases. Histopathology. 1999;34(5):391-8. https://doi.org/10.1046/j.1365-2559.1999.00651.x PMid:10231412
  15. Byrd JC, Edenfield WJ, Shields DJ, Dawson NA. Extramedullary myeloid cell tumors in acute nonlymphocytic leukemia: a clinical review. J Clin Oncol. 1995;13(7):1800-16. https://doi.org/10.1200/JCO.1995.13.7.1800 PMid:7602369
  16. Kim NR, Lee WK, Lee JI, Cho HY. Multiple Jejunal Myeloid Sarcomas Presenting with Intestinal Obstruction in a Non-leukemic Patient: A Case Report with Ultrastructural Observations. Korean J Pathol. 2012;46(6):590-4. https://doi.org/10.4132/KoreanJPathol.2012.46.6.590 PMid:23323112 PMCid:PMC3540339
  17. Gajendra S, Gogia A, Das P, Gupta R, Tanwar P. Acute myeloid leukemia presenting as "bowel upset": a case report. J Clin Diagn Res. 2014;8(7):FD09-10.
  18. Benet C, Gomez A, Aguilar C, Delattre C, Vergier B, Beylot-Barry M, et al. Histologic and immunohistologic characterization of skin localization of myeloid disorders: a study of 173 cases. Am J Clin Pathol. 2011;135(2):278-90. https://doi.org/10.1309/AJCPFMNYCVPDEND0 PMid:21228369  
  19. Al-Khateeb H, Badheeb A, Haddad H, Marei L, Abbasi S. Myeloid sarcoma: clinicopathologic, cytogenetic, and outcome analysis of 21 adult patients. Leuk Res Treatment. 2011;2011:523168. https://doi.org/10.4061/2011/523168 PMid:23213544 PMCid:PMC3505919
  20. Sen F, Zhang XX, Prieto VG, Shea CR, Qumsiyeh MB. Increased incidence of trisomy 8 in acute myeloid leukemia with skin infiltration (leukemia cutis). Diagn Mol Pathol. 2000;9(4):190-4. https://doi.org/10.1097/00019606-200012000-00003 PMid:11129442
  21. Byrd JC, Weiss RB, Arthur DC, Lawrence D, Baer MR, Davey F, et al. Extramedullary leukemia adversely affects hematologic complete remission rate and overall survival in patients with t(8;21)(q22;q22): results from Cancer and Leukemia Group B 8461. J Clin Oncol. 1997;15(2):466-75. https://doi.org/10.1200/JCO.1997.15.2.466 PMid:9053467
  22. Shan M, Lu Y, Yang M, Wang P, Lu S, Zhang L, et al. Characteristics and transplant outcome of myeloid sarcoma: a single-institute study. Int J Hematol. 2021;113(5):682-92. https://doi.org/10.1007/s12185-021-03081-2 PMid:33511548
  23. Dalland JC, Meyer R, Ketterling RP, Reichard KK. Myeloid Sarcoma With CBFB-MYH11 Fusion (inv(16) or t(16;16)) Prevails in the Abdomen. Am J Clin Pathol. 2020;153(3):333-41. https://doi.org/10.1093/ajcp/aqz168 PMid:31671434
  24. Antic D, Elezovic I, Bogdanovic A, Vukovic NS, Pavlovic A, Jovanovic MP, et al. Isolated myeloid sarcoma of the gastrointestinal tract. Intern Med. 2010;49(9):853-6. https://doi.org/10.2169/internalmedicine.49.2874 PMid:20453407
  25. Derenzini E, Paolini S, Martinelli G, Campidelli C, Grazi GL, Calabrese C, et al. Extramedullary myeloid tumour of the stomach and duodenum presenting without acute myeloblastic leukemia: a diagnostic and therapeutic challenge. Leuk Lymphoma. 2008;49(1):159-62. https://doi.org/10.1080/10428190701704621 PMid:18203027
  26. El H, II, Easler JJ, Ceppa EP, Shahda S. Myeloid sarcoma of the sigmoid colon: An unusual presentation of a rare condition. Dig Liver Dis. 2017;49(11):1280. https://doi.org/10.1016/j.dld.2017.05.012 PMid:28606757
  27. Goor O, Goor Y, Konikoff F, Trejo L, Naparstak E. Common malignancies with uncommon sites of presentation: case 3. Epigastric distress caused by a duodenal polyp: a rare presentation of acute leukemia. J Clin Oncol. 2003;21(23):4458-9. https://doi.org/10.1200/JCO.2003.03.188 PMid:14645438
  28. Jeong SH, Han JH, Jeong SY, Kang SY, Lee HW, Choi JH, et al. A case of donor-derived granulocytic sarcoma after allogeneic hematopoietic stem cell transplantation. Korean J Hematol. 2010;45(1):70-2. https://doi.org/10.5045/kjh.2010.45.1.70 PMid:21120167 PMCid:PMC2982999
  29. Le Beau MM, Larson RA, Bitter MA, Vardiman JW, Golomb HM, Rowley JD. Association of an inversion of chromosome 16 with abnormal marrow eosinophils in acute myelomonocytic leukemia. A unique cytogenetic-clinicopathological association. N Engl J Med. 1983;309(11):630-6. https://doi.org/10.1056/NEJM198309153091103 PMid:6577285
  30. Mrad K, Abid L, Driss M, Ben Abid H, Ben Romdhane K. Granulocytic sarcoma of the small intestine in a child without leukemia: report of a case with cytologic findings and immunophenotyping pitfalls. Acta Cytol. 2004;48(5):641-4. https://doi.org/10.1159/000326435 PMid:15471256
  31. Narayan P, Murthy V, Su M, Woel R, Grossman IR, Chamberlain RS. Primary myeloid sarcoma masquerading as an obstructing duodenal carcinoma. Case Rep Hematol. 2012;2012:490438. https://doi.org/10.1155/2012/490438 PMid:23243527 PMCid:PMC3517833
  32. Sun R, Samie AA, Theilmann L. A patient with a tumor of the ileocecal valve. Gastroenterology. 2011;141(6):1977, 2278. https://doi.org/10.1053/j.gastro.2010.11.046 PMid:22033185
  33. Toubai T, Kondo Y, Ogawa T, Imai A, Kobayashi N, Ogasawara M, et al. A case of leukemia of the appendix presenting as acute appendicitis. Acta Haematol. 2003;109(4):199-201. https://doi.org/10.1159/000070971 PMid:12853694
  34. Shimizu H, Saitoh T, Hatsumi N, Takada S, Yokohama A, Handa H, et al. Clinical significance of granulocytic sarcoma in adult patients with acute myeloid leukemia. Cancer Sci. 2012;103(8):1513-7. https://doi.org/10.1111/j.1349-7006.2012.02324.x PMid:22568487 PMCid:PMC7659365
  35. Almond LM, Charalampakis M, Ford SJ, Gourevitch D, Desai A. Myeloid Sarcoma: Presentation, Diagnosis, and Treatment. Clin Lymphoma Myeloma Leuk. 2017;17(5):263-7. https://doi.org/10.1016/j.clml.2017.02.027 PMid:28342811
  36. Ibrahim M, Chen R, Vegel A, Panse K, Bhyravabhotla K, Harris K, et al. Treatment of myeloid sarcoma without bone marrow involvement with gemtuzumab ozogamicin-containing regimen. Leuk Res. 2021;106:106583. https://doi.org/10.1016/j.leukres.2021.106583 PMid:33906021
  37. Chevallier P, Labopin M, Cornelissen J, Socie G, Rocha V, Mohty M, et al. Allogeneic hematopoietic stem cell transplantation for isolated and leukemic myeloid sarcoma in adults: a report from the Acute Leukemia Working Party of the European group for Blood and Marrow Transplantation. Haematologica. 2011;96(9):1391-4. https://doi.org/10.3324/haematol.2011.041418 PMid:21685467 PMCid:PMC3166114
  38. Chen WY, Wang CW, Chang CH, Liu HH, Lan KH, Tang JL, et al. Clinicopathologic features and responses to radiotherapy of myeloid sarcoma. Radiat Oncol. 2013;8:245. https://doi.org/10.1186/1748-717X-8-245 PMid:24148102 PMCid:PMC4016483
  39. Xavier SG, Fagundes EM, Hassan R, Bacchi C, Conchon M, Tabak DG, et al. Granulocytic sarcoma of the small intestine with CBFbeta/MYH11 fusion gene: report of an aleukaemic case and review of the literature. Leuk Res. 2003;27(11):1063-6. https://doi.org/10.1016/S0145-2126(03)00070-5
  40. Zhang XH, Zhang R, Li Y. Granulocytic sarcoma of abdomen in acute myeloid leukemia patient with inv(16) and t(6;17) abnormal chromosome: case report and review of literature. Leuk Res. 2010;34(7):958-61. https://doi.org/10.1016/j.leukres.2010.01.009 PMid:20116851
  41. Wada A, Kobayashi N, Asanuma S, Matsuoka S, Kosugi M, Fujii S, et al. Repeated donor lymphocyte infusions overcome a myeloid sarcoma of the stomach resulting from a relapse of acute myeloid leukemia after allogeneic cell transplantation in long-term survival of more than 10 years. Int J Hematol. 2011;93(1):118-22. https://doi.org/10.1007/s12185-010-0737-z PMid:21181316
  42. Vedy D, Muehlematter D, Rausch T, Stalder M, Jotterand M, Spertini O. Acute myeloid leukemia with myeloid sarcoma and eosinophilia: prolonged remission and molecular response to imatinib. J Clin Oncol. 2010;28(3):e33-5. https://doi.org/10.1200/JCO.2009.23.6976 PMid:19901109
  43. Gadage V, Zutshi G, Menon S, Shet T, Gupta S. Gastric myeloid sarcoma--a report of two cases addressing diagnostic issues. Indian J Pathol Microbiol. 2011;54(4):832-5.
  44. Huang XL, Tao J, Li JZ, Chen XL, Chen JN, Shao CK, et al. Gastric myeloid sarcoma without acute myeloblastic leukemia. World J Gastroenterol. 2015;21(7):2242-8. https://doi.org/10.3748/wjg.v21.i7.2242 PMid:25717265 PMCid:PMC4326167
  45. Kini S, Amarapurkar A, Balasubramanian M. Small Intestinal Obstruction with Intussusception due to Acute Myeloid Leukemia: A Case Report. Case Rep Gastrointest Med. 2012;2012:425358. https://doi.org/10.1155/2012/425358 PMid:22928122 PMCid:PMC3426187
  46. Koehler M. Granulocytic sarcoma of the stomach. Gastrointest Endosc. 1998;48(2):190. https://doi.org/10.1016/S0016-5107(98)70162-2
  47. Sekaran A, Darisetty S, Lakhtakia S, Ramchandani M, Reddy DN. Granulocytic Sarcoma of the Stomach Presenting as Dysphagia during Pregnancy. Case Rep Gastrointest Med. 2011;2011:627549. https://doi.org/10.1155/2011/627549 PMid:22606423 PMCid:PMC3350040
  48. Yu T, Xu G, Xu X, Yang J, Ding L. Myeloid sarcoma derived from the gastrointestinal tract: A case report and review of the literature. Oncol Lett. 2016;11(6):4155-9. https://doi.org/10.3892/ol.2016.4517 PMid:27313759 PMCid:PMC4888104
  49. Choi ER, Ko YH, Kim SJ, Jang JH, Kim K, Kang WK, et al. Gastric recurrence of extramedullary granulocytic sarcoma after allogeneic stem cell transplantation for acute myeloid leukemia. J Clin Oncol. 2010;28(4):e54-5. https://doi.org/10.1200/JCO.2009.23.7560 PMid:19917867
  50. Jalil Ur R, Shinawi M, Aslam M, Kelta M. Acute myeloid leukemia post-allogeneic peripheral stem cell transplant with gastric chloroma. Ann Saudi Med. 2011;31(6):658-60. https://doi.org/10.4103/0256-4947.81805 PMid:21727746 PMCid:PMC3221145
  51. Pasricha TS, Abraczinskas D. Gastrointestinal Myeloid Sarcoma. N Engl J Med. 2020;383(9):858. https://doi.org/10.1056/NEJMicm2001235 PMid:32846064
  52. Alvarez P, Navascues CA, Ordieres C, Pipa M, Vega IF, Granero P, et al. Granulocytic sarcoma of the small bowel, greater omentum and peritoneum associated with a CBFbeta/MYH11 fusion and inv(16) (p13q22): a case report. Int Arch Med. 2011;4(1):3. https://doi.org/10.1186/1755-7682-4-3 PMid:21255400 PMCid:PMC3032668
  53. Chen YI, Paci P, Michel RP, Bessissow T. Myeloid sarcoma of the duodenum: a rare cause of bowel obstruction and gastrointestinal bleeding. Endoscopy. 2015;47 Suppl 1 UCTN:E181-2. https://doi.org/10.1055/s-0034-1391502
  54. Cicilet S, Tom FK, Philip B, Biswas A. Primary myeloid sarcoma of small bowel. BMJ Case Rep. 2017;2017. https://doi.org/10.1136/bcr-2017-220503 PMid:28596206 PMCid:PMC5535183
  55. Fukushima M, Ono Y, Imai Y. Granulocytic sarcoma of the small intestine in a patient with chronic myelomonocytic leukemia. Dig Endosc. 2014;26(6):757-8. https://doi.org/10.1111/den.12381 PMid:25251682
  56. Ghafoor T, Zaidi A, Al Nassir I. Granulocytic sarcoma of the small intestine: an unusual presentation of acute myelogenous leukaemia. J Pak Med Assoc. 2010;60(2):133-5.
  57. He T, Guo Y, Wang C, Yan J, Zhang M, Xu W, et al. A primary myeloid sarcoma involving the small intestine and mesentery: case report and literature review. Int J Clin Exp Pathol. 2018;11(8):4158-62.
  58. Hotta K, Kunieda K. Granulocytic sarcoma of the jejunum diagnosed by biopsies during double-balloon endoscopy before treatment (with video). Dig Endosc. 2013;25(4):468. https://doi.org/10.1111/den.12107 PMid:23621465
  59. Huang B, You P, Zhu P, Du Z, Wu B, Xu X, et al. Isolated duodenal myeloid sarcoma associated with the CBFbeta/MYH11 fusion gene followed by acute myeloid leukemia progression: A case report and literature review. Oncol Lett. 2014;8(3):1261-4. https://doi.org/10.3892/ol.2014.2313 PMid:25120702 PMCid:PMC4114609
  60. Kitagawa Y, Sameshima Y, Shiozaki H, Ogawa S, Masuda A, Mori SI, et al. Isolated granulocytic sarcoma of the small intestine successfully treated with chemotherapy and bone marrow transplantation. Int J Hematol. 2008;87(4):410-3. https://doi.org/10.1007/s12185-008-0067-6 PMid:18365139
  61. Kumar B, Bommana V, Irani F, Kasmani R, Mian A, Mahajan K. An uncommon cause of small bowel obstruction: isolated primary granulocytic sarcoma. QJM. 2009;102(7):491-3. https://doi.org/10.1093/qjmed/hcp051 PMid:19433489
  62. Lee EY, Leung AY, Anthony MP, Loong F, Khong PL. Utility of 18F-FDG PET/CT in identifying terminal ileal myeloid sarcoma in an asymptomatic patient. Am J Hematol. 2011;86(12):1036-7. https://doi.org/10.1002/ajh.22077 PMid:21800353
  63. Li X, Huang C, Li Y. Obstructive jaundice caused by myeloid sarcoma in duodenal ampulla. Dig Liver Dis. 2019;51(2):321. https://doi.org/10.1016/j.dld.2018.08.004 PMid:30253977
  64. Lim SW, Lee HL, Lee KN, Jun DW, Kim IY, Kim E, et al. A Case of Myeloid Sarcoma of Intestine. Korean J Gastroenterol. 2016;68(3):148-51. https://doi.org/10.4166/kjg.2016.68.3.148 PMid:27646584
  65. Martinelli G, Ottaviani E, Testoni N, Visani G, Pagliani G, Tura S. Molecular analysis of granulocytic sarcoma: a single center experience. Haematologica. 1999;84(4):380-2.
  66. McKenna M, Arnold C, Catherwood MA, Humphreys MW, Cuthbert RJ, Bueso-Ramos C, et al. Myeloid sarcoma of the small bowel associated with a CBFbeta/MYH11 fusion and inv(16)(p13q22): a case report. J Clin Pathol. 2009;62(8):757-9. https://doi.org/10.1136/jcp.2008.063669 PMid:19638550
  67. Meireles LC, Lagos AC, Marques I, Serejo F, Velosa J. Myeloid sarcoma of gastrointestinal tract: A rare cause of obstruction. Rev Esp Enferm Dig. 2015;107(5):326-7.
  68. Mizumoto R, Tsujie M, Wakasa T, Kitani K, Manabe H, Fukuda S, et al. Isolated myeloid sarcoma presenting with small bowel obstruction: a case report. Surg Case Rep. 2020;6(1):2. https://doi.org/10.1186/s40792-019-0759-6 PMid:31900687 PMCid:PMC6942080
  69. Morel F, Herry A, Le Bris MJ, Le Calvez G, Marion V, Berthou C, et al. Isolated granulocytic sarcoma followed by acute myelogenous leukemia type FAB-M2 associated with inversion 16 and trisomies 9 and 22. Leukemia. 2002;16(12):2458-9. https://doi.org/10.1038/sj.leu.2402593 PMid:12454755
  70. Nemesio RA, Costa B, Abrantes C, Leite JS. Myeloid sarcoma of the small intestine in a patient without overt acute myeloid leukaemia: a challenging diagnosis of a rare condition. BMJ Case Rep. 2018;2018. https://doi.org/10.1136/bcr-2017-222718 PMid:29848520 PMCid:PMC5976126
  71. Ono K, Mikami Y, Hosoe N. Primary granulocytic sarcoma of the small intestine diagnosed by single-balloon enteroscopy: A case report. Dig Endosc. 2020;32(3):436. https://doi.org/10.1111/den.13611 PMid:31858650
  72. Palanivelu C, Rangarajan M, Senthilkumar R, Annapoorni S. Laparoscopic management of an obstructing granulocytic sarcoma of the jejunum causing intussusception in a nonleukemic patient: report of a case. Surg Today. 2009;39(7):606-9. https://doi.org/10.1007/s00595-007-3807-y PMid:19562450
  73. Russell SJ, Giles FJ, Thompson DS, Scanlon DJ, Walker H, Richards JD. Granulocytic sarcoma of the small intestine preceding acute myelomonocytic leukemia with abnormal eosinophils and inv(16). Cancer Genet Cytogenet. 1988;35(2):231-5. https://doi.org/10.1016/0165-4608(88)90245-2
  74. Wang P, Li Q, Zhang L, Ji H, Zhang CZ, Wang B. A myeloid sarcoma involving the small intestine, kidneys, mesentery, and mesenteric lymph nodes: A case report and literature review. Medicine (Baltimore). 2017;96(42):e7934. https://doi.org/10.1097/MD.0000000000007934 PMid:29049187 PMCid:PMC5662353
  75. Wong SW, Lai CK, Lee KF, Lai PB. Granulocytic sarcoma of the small bowel causing intestinal obstruction. Hong Kong Med J. 2005;11(3):204-6.
  76. Yoldas T, Erol V, Demir B, Hoscoskun C. A rare cause of mechanical obstruction: Intestinal myeloid sarcoma. Ulus Cerrahi Derg. 2014;30(3):176-8. https://doi.org/10.5152/UCD.2013.31 PMid:25931908 PMCid:PMC4379854
  77. Evans C, Rosenfeld CS, Winkelstein A, Shadduck RK, Pataki KI, Oldham FB. Perforation of an unsuspected cecal granulocytic sarcoma during therapy with granulocyte-macrophage colony-stimulating factor. N Engl J Med. 1990;322(5):337-8. https://doi.org/10.1056/NEJM199002013220517 PMid:2404207
  78. Gupta S, Chawla I, Singh V, Singh K. Granulocytic sarcoma (chloroma) presenting as colo-colic intussusception in a 16-year-old boy: an unusual presentation. BMJ Case Rep. 2014;2014. https://doi.org/10.1136/bcr-2014-206138 PMid:25150243 PMCid:PMC4154025
  79. Kaila V, Desai A. An Unusual Cause of Postpolypectomy Bleeding. Gastroenterology. 2020;159(4):e3-e5. https://doi.org/10.1053/j.gastro.2020.02.063 PMid:32205169
  80. Rodriguez EA, Lopez MA, Valluri K, Wang D, Fischer A, Perdomo T. Acute appendicitis secondary to acute promyelocytic leukemia. Am J Case Rep. 2015;16:73-6. https://doi.org/10.12659/AJCR.892760 PMid:25666852 PMCid:PMC4327184

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