Isolated breast myeloid sarcoma: A diagnostic and therapeutic challenge. A case report and literature review

Abstract

Introduction

Myeloid sarcoma is a high-grade hematological malignancy that rarely occurs in the breast as the tumor is generally seen in the ribs, sternum, and orbital bones. We report a case of isolated myeloid sarcoma presenting as a breast mass and reviewed the literature to raise awareness of this disease.

Case presentation

A 20-year-old girl presented with a painless mass located in the upper outer quadrant of the left breast. The patient underwent a bilateral breast US revealing a central retroareolar large hypoechoic solid mass about 55 × 33 mm. A core needle biopsy was performed leading to the suspicion of non-Hodgkin lymphoma. The patient was planned to start CHOP protocol till the final confirmatory pathologic results. She received 4 cycles with a partial response. A new biopsy from the breast mass and IHC revealed the diagnosis of myeloid sarcoma. Bone marrow examination was normocellular with no abnormal deposits. She received 4 cycles HD Cytarabine with a PET CT revealing a complete response. She is prepared for bone marrow transplantation.

Conclusion

Being rare, breast myeloid sarcoma is often misinterpreted as NHL or lobular breast cancer. Oncologists must remain aware of this condition because it frequently co-occurs with or follows AML.

Keywords

breast myeloid sarcoma AML lymphoma chemotherapy

Introduction

Myeloid sarcoma is a rare, high-grade hematological malignancy characterized by an extramedullary tumor mass that is composed of a myeloid blast with effacement of underlying tissue structure. Due to the green color of the myeloperoxidase enzyme, the tumor was originally called chloroma by King in 1893.¹ Myeloid sarcoma rarely occurred in the breast as the tumor was generally seen in the ribs, sternum, and orbital bones.² We report a case of isolated myeloid sarcoma presenting as a breast mass that was misdiagnosed as non-Hodgkin’s lymphoma (NHL) and reviewed literature to raise awareness of this disease.

Case presentation

A 20-year-old girl presented to our hospital with a painless mass in her left breast which had an insidious onset and slowly progressive course. She has no relevant medical or surgical history. The patient also experienced intermittent fever, but no weight loss, and had painless nodules on her face, in the axilla, and under her eyes. There was no mastalgia, nipple discharge, or other swellings. Her aunt had a history of breast cancer. Her menstrual history was insignificant. By examination, there was a mass located in the upper outer quadrant of the left breast. The mass was firm with limited mobility. A general examination of the patient showed normal appearance, body build, and complexion. The patient was cooperative and fully oriented. Vital signs were within normal ranges.

The patient underwent both breast US revealing a central retroareolar large hypoechoic solid mass about 55 × 33 mm with moderate vascularity in the left breast, and another similar smaller area of parenchymal distortion was seen at the right breast with suspicious bilateral axillary and left infraclavicular nodes. Left breast mild skin thickening with mild edema was also noted.

A core needle biopsy was performed, and it was examined in a qualified pathology laboratory outside our center. Microscopic examination revealed tumoral proliferation diffusely arranged with crushing artifacts surrounded with intense cellular fibrous stroma. It showed a positive reaction for LCA while Ki67 showed a high proliferation index. This led to the suspicion of non-Hodgkin lymphoma. Further, IHC was suggested on more tissue cores.

PET-CT (Figure 1) showed FDG-avid bilateral irregular breast masses with a maximum standardized uptake value (SUVmax) of 9.5 on the right breast and 7 on the left. It also described distorted FDG-avid left axillary and subpectoral LNs with SUVmax of 3.5 and 5.5, respectively. No other metabolically active lesions were detected.

Figure 1.

Baseline PET-CT: (a), (b), and (c): Axial post-contrast CT and fused FDG PET/CT images reveal FDG-avid bilateral irregular breast masses with maximum standardized uptake value (SUVmax) of 9.5 on the right breast and 7 on the left, and distorted FDG-avid left axillary and subpectoral LNs with SUVmax of 3.5 and 5.5, respectively. (d): coronal maximum intensity projection (MIP) image reveals no other metabolically active lesions detected.

Based on the initial pathology report, the patient was planned to start chemotherapy with cyclophosphamide, doxorubicin, vincristine, and prednisolone (CHOP protocol) till final confirmatory pathologic results. She received 4 cycles with a partial response; she complained of an initial regression followed by recurrent increases in breast mass size before each cycle. After the fourth cycle, PET-CT described a metabolic resolution and morphologic regression of bilateral axillary lymph nodes and breast masses. A new biopsy from the breast mass was recommended to complete IHC (CD20) and to reassure initial pathologic results due to inconsistent response.

Core needle biopsy (Figure 2) revealed breast tissue with partially distorted lobular architecture by dense infiltration of small to medium-sized neoplastic cells. These cells were discohesive mostly infiltrating in patternless arrays and around the ducts. These cells exhibit dense granular chromatin, a high N/C ratio, and little amphophilic cytoplasm. Eosinophilic infiltrate and occasional mitotic figures and apoptotic bodies were detected. IHC (Figure 3) for CD34, MPO, and LCA showed diffuse positivity in neoplastic cells while it showed focal positivity in neoplastic cells for CD 117. CD79a, PAX5, CD20, CD3, and panCK showed a negative reaction in neoplastic cells. IHC for ERG showed a positive reaction, and Ki67 showed a high proliferation index. This led to the diagnosis of myeloid sarcoma.

Figure 2.

Microscopic examination of the tumor: (a) The lobular breast architecture is disturbed by a diffuse infiltrate of mostly round discohesive cellular infiltrate (H&E. ×40). (b) The cells have a mild amount of cytoplasm with hyperchromatic nuclei and a moderate degree of pleomorphism. Scattered eosinophils are seen among the infiltrate (arrow) (H&E. ×200). (c) The infiltrate is seen dissecting between fat cells and again eosinophils are occasional (arrow) (H&E. ×400).

Figure 3.

IHC staining of the tumor cells: (a) Immunohistochemistry revealed a negative reaction for CK with good internal control (IHC × 400). Similarly, negative reaction was encountered for CD20, CD3, and HMB45 (IHC × 100). (b) A diffuse positive nuclear reaction for ERG, diffuse positive membranous reaction for CD 34, and diffuse positive cytoplasmic reaction for myeloperoxidase. Ki67 revealed nuclear reaction in an average of 80% of tumor cells (IHC × 400).

Immunophenotyping (flow test) done on FNAC sample of breast mass was performed. Few myeloblasts could be detected 2.0% expressing CD34, CD117, CD33, CD13, and HLADR but are negative for CD36, CD14, CD64, cCD3, and cCD79a. MPO expression could not be interpreted. Bone marrow examination was done for evaluation of the possibility of concurrent acute myeloid leukemia, and the result was negative showing normocellular bone marrow with no abnormal deposits.

MDT recommended for this patient HD Cytarabine (1.5 mg/m²). She received 4 cycles with follow-up PET CT revealing a complete response with morphologic and metabolic resolution of the breast masses and lymph nodes. She is prepared for bone marrow transplantation.

Discussion

The report described a case of myeloid sarcoma involving the breast with no evidence of bone marrow involvement and therefore considered primary myeloid sarcoma (in the absence of acute or chronic myeloproliferative disorder) with an incidence of two cases per million adults. Myeloid sarcoma (MS) is a tumor mass of myeloblasts or immature myeloid cells occurring in an extramedullary site or the bone.³ The tumor can involve any part of the body, but commonly involved sites include subperiosteal bone structures of the skull, paranasal sinuses, sternum, ribs, vertebrae, and pelvis; lymph nodes and skin are also common sites.³ MS may occur de novo or concurrently with acute myeloid leukemia (AML) or a myeloproliferative disorder.³ The rate of occurrence is approximately 1.4% to 9% of patients with AML.^4,5 MS is frequently mistaken for non-Hodgkin lymphoma (NHL), small round cell tumor (neuroblastoma, rhabdomyosarcoma, Ewing sarcoma/PNET, and medulloblastoma), and undifferentiated carcinoma. The diagnosis is missed in about 50% of cases when immunohistochemistry is not used.⁶ The most commonly suggested diagnosis was that of an NHL⁷ as it is with our case. From the pathological professional point of view, the misdiagnosis of the first biopsy done outside our center can be explained by technical defects. The amount of tissue was scanty, and cells were predominantly crushed with only a few viable ones. Therefore, the cells were mostly appearing as blast-like with no features saying that they were myeloblast. Being more common, NHL was the top differential coming into mind in such a case after the exclusion of lobular carcinoma. IHC for CD 20 also suffered technical defects with much background staining being falsely interpreted by the pathologist as positive. The second biopsy was examined by another expert pathologist who reported the features of myeloid sarcoma confirmed by the IHC profile.

It is worth mentioning that the breast is a very uncommon site for myeloid sarcoma. A summary of the previously reported cases is presented in Table 1. A high index of suspicion based on histological findings especially the interspersed eosinophilic infiltrate and IHC will be helpful to avoid misdiagnosis as neither lymphoma nor lobular carcinoma. Based on a study that included six male and seven female patients with an age range of 25 to 72 years (mean, 49.3 years) and a male-to-female ratio of 1:1.2, MS de novo occurred in 4/13 (31%) of cases examined, the most sensitive immunohistochemical markers were CD43, and lysozyme present in all cases with MS (13/13, 100%). All de novo MS showed a normal karyotype, monoblastic differentiation, and lack of CD34 in contrast to our case in which it was positive for CD34. The most common chromosomal abnormalities in MS associated with a hematopoietic disorder were trisomy 8 and inv (16) (2/11, 18%).

Table 1.

Summary of all previously reported cases.

#	Author/year	Sex/age	Clinical presentation	Misdiagnosis	Radiology result	IHC	Treatment modalities	Follow-up	Progression to AML
1	Rizwan et al. (2012)	M/56	Right breast enlargement	Misdiagnosed as CML	CT: large chest wall mass eroding 5–6 ribs	positive for MPO lysozyme, CD43, and CD34	Gleevec, radiotherapy, planned for AML chemotherapy	Hip fracture, he passed away 5 days post-surgery due to pulmonary embolism	Not mentioned
			Skin color changes	Or myelodysplastic syndrome	Bone scan: bone uptake in femur and skull
			Mild hip and thigh pain	Or myelodysplastic syndrome	Bone scan: bone uptake in femur and skull
2	X. Huang et al. (2015)	F/58	Enlarged, painless, and palpable mass in the left breast for 1 year	No	Mammogram: a single, irregular, poorly defined mass without calcification	Positive for MPO and CD68, but negative for ER, PR, Her-2, and p120	Lumpectomy and three cycles of consolidation chemotherapy (cytarabine and idarubicin)	No local recurrence was identified in the breast 1 year later	Already diagnosed with AML-M6 2 years earlier
2	X. Huang et al. (2015)	F/58		No	MRI: ill‐defined inhomogeneous hyperintense mass				Already diagnosed with AML-M6 2 years earlier
3	Shaikh and Kayani (2015)	F 28	Painless lump in left breast noticed over 2 years, approximately 7 × 6 cm	No	Ultrasound: hypoechoic area measuring approximately 6 cm in diameter	Positive for LCA, CD34, CD117, CD43, and MPO; negative for CK AE1/AE3	Not treated	Patient died 1.5 years after myeloid sarcoma diagnosis	Most probably, yet not proven
4	Ozsoy et al. (2016)	F/21	Bilateral painless palpable breast masses, increased in size over 4 months	Initially suspected hematolymphoid neoplasm	US: multiple hypoechoic solid masses with increased vascularity	Positive for CD34, CD43, CD99, Tdt, and BCL-2, weak-to-moderate positive for CD79a and CD117, focal positivity for MPO, and variable positivity for CD68	Chemotherapy with cytarabine and idarubicin regime	2 years disease-free	No
5	Zhai et al. (2018)	F/34	Palpable, painless, hard mass in the right breast	Breast cancer versus lymphoma	Mammogram: 2.5 × 2.4 cm mass with irregular margins and 1.4 × 1.1 cm mass in the IOQ	Strongly positive for MPO, CD43, and LCA	Lumpectomy received 4 cycles of consolidation chemotherapy with idarubicin	1.5 years disease-free	No
5	Zhai et al. (2018)	F/34	Palpable, painless, hard mass in the right breast	Frozen section examination: poorly differentiated malignant tumor	Ultrasound: hypoechoic lobulated mass (3.7 × 2.6 cm) in the UOQ and another mass (1.8×1.1 cm) below the nipple	Strongly positive for MPO, CD43, and LCA		1.5 years disease-free	No
6	Gomaa et al. (2018)	F/29	A painless left breast lump for 3 months.	Initially suspected hamartoma	US: a well-defined mass in the left UOQ, likely hamartoma. Mammogram: single, irregular, poorly defined mass without calcification	Positive for LCA, MPO, CD68, CD34, and CD117	Radiotherapy and chemotherapy	6 months disease-free	No
6	Gomaa et al. (2018)	F/29	A painless left breast lump for 3 months.	Initially suspected hamartoma	MRI: suggestive of hamartoma	Positive for LCA, MPO, CD68, CD34, and CD117	Radiotherapy and chemotherapy	6 months disease-free	No
7	Hengyu Wu, Lei Liu, Lei Gu. Yonghui Luo (2019)	F/42	Palpable right breast mass present for 4 months	Invasive breast carcinoma based on frozen section	US: irregular, ill-defined margin hypoechoic area	Positive for MPO, LCA, BCL-2, C-myc, and Ki-67 60%.	Right mastectomy and sentinel lymph node biopsy, 2 cycles of IA chemotherapy (inhibition and cytosine arabinoside.) Then HA regimen chemotherapy (Homoharringtonine and cytosine arabinoside)	1-year disease-free	No
					Mammogram: a mass without calcification in the outer quadrant of the right breast	Negative ER, PR, cerbB2, CK5/6, ECad, CK, P120, CD20, PAX5, CD3, CD5, BCL-6, CD10, and MUM-1
					MRI: mass over the outer quadrant of the right breast coalescing with axillary lymph nodes
8	Kim and Kim (2019)	F/24	A painless lump in UOQ of the right breast was noticed 2 days earlier	No	US: 4.3 cm oval heterogeneous mass with posterior enchantment in the UOQ of the right breast	Focal positive MPO	N/A	N/A	Already diagnosed with AML 18 months earlier
9	Khoshnaw et al. (2019)	F/30	Bilateral breast pain and tenderness 8 weeks after bone marrow remission	Initial diagnosis was likely focused on mastitis or breast cancer	US: Oval-shaped, heterogeneous masses in both breasts	Positive for CD117, CD45, Ki67 negative for CD34, ER, PR, HER2, E-cadherin, AE1, and AE3	Received FLAG-IDA chemotherapy	Did not achieve complete remission, died due to disease progression	She was already diagnosed with AML-M1
9	Khoshnaw et al. (2019)	F/30			MRI: multiple round-shaped masses with a mild, irregular outline		Received FLAG-IDA chemotherapy		She was already diagnosed with AML-M1
10	Baveja et al. (2020)	F/13	Painless lump in the LOQ of the right breast noticed 2 days prior	No	N/A	Strongly positive for MPO, CD43, CD56, CD68, LCA, and CD99; intermediate to weak for CD117 and TdT; negative for lymphoid B and T cell markers	FLAG-IDA (Fludarabine, Daunorubicin, and Cytosar)	N/A	Known patient of AML
11	Huang et al. (2021)	F/34	Painless palpable breast masses, rapidly increasing in size	No	Ultrasound and MRI: multiple well-defined hypoechoic oval lesions in bilateral breasts, and hypoechoic nodules in both axillae	Positive for MPO, CD34, CD43, CD68, CD117, and Ki67	Interleukin-2 (IL-2) + decitabine + thalidomide regimen once, the azacitidine + cytarabine + IL-2 regimen twice, the methotrexate (MTX) regimen once, then MA (MTX + cytarabine) regimen once, and 11 doses of 50 mg intrathecal cytarabine	The patient died of intracranial invasion of AML, brain herniation, and respiratory failure	Already diagnosed with AML-M4
12	Amiraian et al. (2022)	F/63	Rapidly enlarging palpable breast masses over 2 weeks	No	Mammogram and ultrasound: multiple high-density, irregular masses in both breasts	Positive for: CD33 and CD43	Plans were made for salvage chemotherapy and consideration of allog-BMT	The patient died before starting treatment	Already diagnosed with AML
12	Amiraian et al. (2022)	F/63	Rapidly enlarging palpable breast masses over 2 weeks	No		Negative for MPO, lysozyme, CD3, and pan-CK		The patient died before starting treatment	Already diagnosed with AML
13	Chun et al. (2024)	F/50	Erythematous, painful breast mass with central necrosis in the UOQ of right breast	No	US: an 8.8 cm mass with mixed solid echogenic and cystic anechoic components	Positive for CD68KP1, CD45, CD33, Cyclin D1, and CD4, with weak positivity for MPO. Negative for CD34, CD3, CD20, CD79a, CD14, CD117, and TdT	Neoadjuvant radiotherapy and chemotherapy (cytarabine and daunorubicin), followed by right mastectomy	Disease-free for 8 months	Not mentioned
13	Chun et al. (2024)	F/50		No	CT: 11.7 × 8.9 cm mass in the right breast with axillary lymphadenopathy			(but developed local recurrent phyllodes)	Not mentioned

Because NHL and MS have comparable morphologies and express several leukocyte antigens, like CD43 and CD45, an incomplete workup could be deceptive. In our study, lobular carcinoma was excluded based on negativity for CK and EMA. Additionally, B-cell and T-cell lymphomas were also excluded by negative stains for CD20, Pax 5, CD79a, and CD3, respectively. Moreover, the positive reaction for myeloblastic markers including CD34, CD117, MPO, and ERG was valuable in excluding other differentials as blastic NK cell lymphoma. Burkitt lymphoma could be excluded by negative immunoreactivity for B-cell-associated antigens, and lack of t (8;14) or t(2;8), and t(8;22) translocations.^8–12

Primary MS yields an unfavorable prognosis if not treated and 88% of the cases tend to progress to AML within 1 year; therefore, follow-up is mandatory^7,13 with bone marrow biopsies and a complete blood picture.^14,15

The disease’s rarity and the lack of randomized clinical studies restrict treatment options. The various subsets, such as isolated versus synchronous MS, newly diagnosed, relapsing, and after allogeneic hematopoietic stem cell transplantation (allo-HSCT) situations, all have an impact on the therapeutic decision. The most reasonable approach is to treat using systemic AML procedures because almost all MS patients eventually acquire AML. The size and location of MS (skin, CNS, or other regions) as well as the unique characteristics of the patient, such as age, performance status (PS), and comorbidities, also influence the choice of therapeutic approaches. Variable therapeutic techniques, such as immunotherapies, hematopoietic stem cell transplantation, targeted treatments, and local therapy, can be employed in light of all these aspects.

Regarding regional therapy, since local symptoms can occur in up to 70% of MS patients, local treatment offers prompt relief. Few reports in this area support the use of surgery before the start of systemic treatment. Conversely, a surgical excision biopsy could be helpful in some situations where the diagnosis is challenging. However, an aggressive surgical strategy is not recommended because MS seems to be extremely sensitive to ionizing radiation. Patients with isolated MS should be evaluated for involved field RT, which is advised for all patients with MS who are not responding well to systemic therapy.¹⁶ A large retrospective analysis of 71 patients (covering studies completed from 1990 to 2014) found no advantage of combination therapy, despite one trial⁴ suggesting that combining radiation with chemotherapy may enhance survival.¹⁷ Overall, RT was recommended in the following scenarios by the recently published Guidelines From the International Lymphoma Radiation Oncology Group: (i) for patients with isolated MS and inadequate response to chemotherapy; (ii) with isolated recurrence after allo-HSCT; and (iii) for palliation of symptomatic vital structure compression.¹⁸

Given that the majority of patients (71–100%) treated with localized therapies (surgery and/or radiation) progress to AML at a median of 4–6 months, the role of induction chemotherapy in MS is supported by multiple studies, even in isolated cases.^4,19–22 Systemic chemotherapy has also been demonstrated to improve overall survival and slow down the development of MS to AML in isolated cases. Furthermore, patients treated with systemic chemotherapy had a longer time to progression to AML than patients treated with local radiation or surgery.²³ “7 + 3” therapy, which consists of 7 days of cytarabine (Ara-C) and 3 days of idarubicin (4-demethoxydaunorubicin), is the most widely used induction regimen.²⁴ To assess the effectiveness of the treatment, a bone marrow aspirate and biopsy should be carried out 14–21 days following the initiation of induction therapy.¹⁶

There are currently no approved treatment plans for MS; patients who qualify for intensive therapy are often treated with regimens based on anthracyclines and cytarabine.^4,20,25

Hypomethylating drugs (HMA) such as azacitidine (5-azacytidine)^4,16–19 and decitabine (5-aza-2′-deoxycytidine)^26–30 have been found to cause clinical remissions in individuals not eligible for intensive therapy but to varying degrees in a small number of studies. Since 2017, some treatments—alone or in combination with chemotherapy—have received regulatory approval. These include CPX-351, a liposomal formulation of daunorubicin and cytarabine at a fixed 5:1 molar ratio; kinase inhibitors, such as sorafenib, midostaurin and ivosidenib, enasidenib, and gilteritinib (IDH1 and IDH2 inhibitors, respectively); venetoclax, a BCL2 inhibitor; and glasdegib, an inhibitor of the transmembrane protein smoothened (SMO) involved in the Hedgehog signaling pathway.³¹ Only a few numbers of these therapies’ effectiveness in treating MS have been documented; these are primarily case studies.

In patients with solitary MS or simultaneous AML and MS, there are currently no controlled prospective clinical trials assessing the role of allo-HSCT as post-remission therapy.²⁵ More precisely, because of the low number of cases and variability in presentation, consolidation with allo-HSCT has not been sufficiently investigated in the context of isolated MS.³² When these patients get high-dose cytarabine (HiDAC) in addition to anthracycline/anthracenedione-based induction therapy, they usually respond well to chemotherapy and have a high complete remission rate.^16,30

Molecular biology analysis and cytogenetics can be utilized to risk stratify patients for a more individualized treatment plan, according to recent research.³³ Because of this, it’s critical to closely examine the distinctive clinical, radiological, and pathologic findings when diagnosing individual MS cases.^24,34–45

Conclusion

Breast myeloid sarcoma is an exceptionally rare disease that can be easily misdiagnosed as NHL or lobular breast carcinoma. Oncologists’ awareness of such a disease is important as it usually is associated with or followed by AML. Early anticipation of this correlation is important to help proceed with the necessary investigations and subsequent treatment in the early stages, which include chemotherapy, BMT, and local therapy. Molecular biology analysis and cytogenetics can be utilized to risk-stratify patients for a more individualized treatment plan.

Statements and declarations

Footnotes

Author contributions

All authors have read and approved the manuscript. HM, ND, DS, GY, and NM: data collection and editing; OH: editing and revision; SA: conceptualization and supervision; GAS: preparation and editing of the radiology part; RN: preparation and editing of the pathology part; MA: preparation and editing of the medical oncology part.

Conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

All procedures performed in the study involving human participants followed the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This is a case report in which ethical-specific approval can be waived as per the institutional policy at Mansoura Faculty of Medicine IRB

ORCID iDs

Hala E Mahfouz

Noor Dheya

Dalia S Khalifa

Gihan Y Abdelhalim

Nur Alia Maisara

Omar Hamdy

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