Other T-Cell and Natural Killer Cell Lymphomas Involving the Skin

Blastic Plasmacytoid Dendritic Cell Neoplasm

Clinical Features: This tumor has undergone several name changes over recent years; the best known include blastic NK-cell lymphoma and, later, CD4+/CD56+ hematodermic neoplasm. It is now believed that the neoplastic cell of BPDCN is related to a precursor of the plasmacytoid dendritic cell, a cell that is known to produce large amounts of α-interferon.⁴⁶³ It most commonly arises in middle-aged to elderly individuals. Cutaneous nodules often constitute the presenting finding.^464,465 Skin lesions are sometimes described as “rash” or exanthema,^466,467 and in one example the lesions were said to resemble angiosarcoma.⁴⁶⁵ Disseminated disease is often present, with lymphadenopathy, anemia, cytopenia, liver, spleen, and/or bone marrow involvement.^467–470 This is an aggressive lymphoma, with deaths usually occurring several months to 3 years following diagnosis.^469,471

Microscopic Findings: There are dermal infiltrates of medium-sized cells with fine chromatin and lymphoblastic features.464,467 Extension into the subcutis may be seen. Other described features include a perivascular or periadnexal configuration of the infiltrate and admixtures with cells having elongated or distorted features⁴⁷² (Fig. 27-42A and B). Although there is some variability in the reported immunophenotype, neoplastic cells are regularly CD56+, usually CD4+ and CD43+, and negative for surface CD3. They typically express the plasmacytoid dendritic cell antigen CD123 and T-cell leukemia/lymphoma 1,^473,474 and they can also stain with antibodies to MxA, a surrogate marker for interferon-α production.⁴⁷⁵ Tumor cells can also stain for TdT.⁴⁷⁶ T-cell receptor genes are germline.^465,471,477 In contrast to NK/T-cell lymphoma, nasal type, these cases are negative for EBV.^465,467,477

Figure 27-42 Blastic plasmacytoid dendritic cell neoplasm. A, There is a dense, nodular infiltrate extending into the deep dermis and subcutis. The infiltrate surrounds a portion of a hair follicle to the lower right of the figure. B, The neoplastic cells have fine chromatin and lymphoblastic features.

Differential Diagnosis: There can be a morphologic resemblance to other lymphomas and leukemias. In terms of immunohistochemical staining, expression of CD56 can also be seen in extranodal NK/T-cell lymphoma, nasal type, and cutaneous γδ T-cell lymphoma, and TdT expression is characteristic of precursor T-lymphoblastic lymphoma (PTLL). Distinction can be made by the expression of plasmacytoid dendritic antigens in BPDCN and the usual negativity for EBV antigens or EBV-encoded small nuclear RNA, in contrast to the positivity for EBV associated with NK/T-cell lymphoma, nasal type. A recent paper described cutaneous lesions composed of plasmacytoid dendritic cells associated with acute myeloid leukemia. As is the case for the neoplastic cells in BPDCN, the cells in the latter condition express CD123, CD4, and T-cell leukemia/lymphoma 1. Among the microscopic differences, the plasmacytoid dendritic cells associated with myeloid leukemia form aggregates that are demarcated from the leukemic cells; they are small- to medium-sized cells with rounded to oval nuclei and fine chromatin. The cells of BPDCN are morphologically similar but are medium- to large-sized and not associated with leukemic cells. In terms of immunohistochemical differences, the cells of BPDCN are regularly CD56+ and sometimes express TdT, whereas those in lesions associated with myeloid leukemia are CD56− and TdT−.⁴⁷⁸

Precursor T-Lymphoblastic Lymphoma

Clinical Features: This neoplasm is composed of T-lineage lymphoblasts. It is essentially the same disorder as precursor T-lymphoblastic leukemia, the only difference being that the lymphoma presents as a mass lesion with less than 25% lymphoblasts in the marrow.⁴⁷⁹ PTLL primarily occurs in adolescent males. It often presents as a rapidly growing mediastinal mass with pleural effusion. Extranodal sites include the liver, spleen, Waldeyer ring, and the central nervous system as well as the skin. A unique feature of this lymphoma is that, although it represents the vast majority of all lymphoblastic lymphomas, it apparently involves the skin less often than does precursor B-lymphoblastic lymphoma.^480,481 Cutaneous involvement most often consists of one or more tumor nodules, with a propensity to occur in the head and neck regions.^480,482 Responses to therapy are comparable to those of precursor B-lymphoblastic lymphoma.

Microscopic Findings: There is usually a dense, diffuse infiltrate composed of medium-sized lymphoid cells with high nuclear-to-cytoplasmic ratios. These cells display rounded to convoluted nuclei with dispersed to condensed chromatin and inconspicuous nucleoli479,480 (Fig. 27-43). Mitotic figures are readily identified. Scattered macrophages can produce a “starry sky” appearance. Several authors have emphasized that there are few, if any, morphologic differences between PTLL and its B-cell counterpart.⁴⁸¹ Immunohistochemistry confirms the T-cell nature of the process, because tumor cells commonly express CD2, CD3, CD4, CD5, CD7, and/or CD8. Blastic cells may coexpress CD4 and CD8.⁴⁷⁹ As is characteristic of lymphoblastic lymphoma, cells are positive for TdT. Other antigens that are sometimes expressed are CD10, CD79a, and the myeloid markers CD13 and/or CD33.^479,480 Other B-cell markers are negative.⁴⁸⁰ Clonal rearrangement of T-cell receptor genes can be detected. Translocations involve T-cell receptor loci and an assortment of partner genes, including several transcription factors.⁴⁸³

Figure 27-43 Precursor T-lymphoblastic lymphoma. The cells have a high nuclear-to-cytoplasmic ratio. Nuclear chromatin is dispersed to condensed, and nucleoli are inconspicuous.

Differential Diagnosis: The “starry sky” appearance of some examples of PTLL can mimic Burkitt lymphoma or variants of mantle cell lymphoma, both uncommon in skin. However, nuclear TdT positivity confirms the diagnosis of lymphoblastic lymphoma. In contrast to blastic plasmacytoid dendritic cell neoplasm, which can also show TdT positivity, the neoplastic cells of PTLL lack the characteristic markers of plasmacytoid dendritic cells, such as CD123. Differential B-cell and T-cell staining can be used to determine the precise lineage of the neoplastic cells.

Hodgkin Disease (Hodgkin Lymphoma)

Clinical Features

Hodgkin disease is a lymphoma composed of a particular type of atypical cell—the Reed-Sternberg cell (and its variants, such as the lacunar cell)—together with a mixed inflammatory cell infiltrate and, sometimes, stromal changes. This disorder has a bimodal age of incidence, with one peak occurring in early adult life and another in later life. Typically, Hodgkin disease presents with lymphadenopathy, particularly cervical, mediastinal, axillary, para-aortic, or inguinal-femoral.484,485 Intermittent fever, night sweats, weight loss, and anemia can accompany the lymphadenopathy. Treatment involves radiation and chemotherapy. Over the years, there has been progressive improvement in the prognosis, and now cures are possible in many cases. Stage of the disease and associated symptoms are better predictors of outcome than histopathologic type.^343,484,485 The neoplastic cells of Hodgkin disease are believed to most often arise from a germinal center B cell,⁴⁸⁶ but T-cell derivation is also possible.^306,487 EBV is detected in a number of cases and may play a pathogenetic role, particularly in patients who are immunosuppressed.⁴⁸⁵

Cutaneous manifestations are found in about 25% of all patients with Hodgkin disease. Nonspecific skin lesions are most common and may precede the diagnosis by months or years. Among the most common are pruritus, Addisonian hyperpigmentation, acquired ichthyosis, infectious complications such as herpes zoster, and erythroderma.⁴⁸⁴ Specific cutaneous infiltrates of Hodgkin disease are uncommon, with reported incidences ranging from 0.5% to 7.5%.^485,488,489 They consist of papules, plaques, nodules, or larger tumors that sometimes ulcerate.⁴⁹⁰ Rarely, exfoliative dermatitis accompanying Hodgkin disease shows specific histopathologic features. Bullous lesions have also been described,⁴⁹¹ and rare examples of granulomatous slack skin have been reported in Hodgkin disease.^488,490 Most often, the mechanism of skin involvement is via retrograde lymphatic spread distal to involved lymph nodes.^489,492 Other, less common mechanisms include direct extension from an underlying nodal focus and hematogenous dissemination. In some cases, specific skin lesions are noted at the time of first presentation of the disease, with node involvement being detected either simultaneously or shortly thereafter.^489,492,493 Hodgkin disease has been preceded by lymphomatoid papulosis^306,494 and accompanied or followed by mycosis fungoides.^306,495 Usually, the finding of specific cutaneous lesions indicates stage IV disease and carries an adverse prognosis.^489,496

However, there may also be rare instances of primary cutaneous Hodgkin disease.⁴⁸⁹ Lesions have most often been isolated cutaneous or subcutaneous nodules,^289,497,498 but there have also been papules or nodules that have undergone spontaneous involution.³¹⁸ Diagnosis of primary cutaneous Hodgkin disease requires identification of typical histopathologic and immunohistochemical features together with a negative workup for systemic disease.^318,497 Primary cutaneous Hodgkin disease may have a more favorable prognosis than does secondary cutaneous involvement arising in established disease. In fact, some examples of primary cutaneous disease persist in the skin for years without systemic findings.³¹⁸ Nevertheless, typical nodal involvement may eventually occur, at intervals ranging from several months to 6 years following the diagnosis of cutaneous disease.^318,497,498

Microscopic Findings

As in lymph nodes and other tissues, a diagnosis of cutaneous involvement by Hodgkin disease rests on the finding of atypical cells with the characteristics of Reed-Sternberg cells. This often occurs in the setting of a polymorphous infiltrate that may include lymphocytes, macrophages, neutrophils, and eosinophils.318,490,493 The Hodgkin cell features lightly basophilic cytoplasm and a large rounded nucleus with a single prominent acidophilic nucleolus. The Reed-Sternberg cell possesses a bilobed nucleus, each lobe containing a prominent acidophilic nucleolus⁴⁸⁵ (Fig. 27-44A and B). A lacunar cell has also been described in cutaneous lesions; this is a Hodgkin or Reed-Sternberg cell with retraction of the cytoplasmic membrane, giving the impression that the cell resides in a space or lacuna.^485,490 The lesional configurations in skin can mimic those of the established nodal subtypes of the disease, and accordingly, nodular sclerosis, mixed cellularity, and lymphocyte-depleted forms have been observed in skin.^489,490,492 The cutaneous pattern frequently reflects that in the involved lymph nodes,⁴⁹⁰ and in one study, the cutaneous pattern was always in the same or a prognostically worse histopathologic category when compared to that displayed in the proximal nodal focus of disease.⁴⁸⁹

Figure 27-44 Hodgkin disease. A, Low-power view of a cutaneous nodule that showed a mixed cellularity configuration. This was the first detected lesion of Hodgkin disease in this patient; a proximal nodal focus of disease was found subsequently. B, A typical Reed-Sternberg cell is shown.

The neoplastic cells in Hodgkin’s disease are CD30+, CD15+ and CD45−.318,490,497,498 A substantial minority of the cells expresses CD20 with varying levels of intensity.⁴⁸⁵ However, T-cell antigens have been expressed on Reed-Sternberg cells in some cases.⁴⁹⁹ EBV-encoded latent membrane protein is sometimes detected.⁴⁸⁵ Overexpression of cytokines and their receptors by the neoplastic cells may account for the admixture of inflammatory cells so often observed in Hodgkin disease.⁴⁸⁵ Immunoglobulin gene rearrangements are found in most cases, but there are rare cases in which T-cell receptor gene rearrangements have been detected.⁴⁸⁷ Most often, gene rearrangements are detected in isolated Reed-Sternberg cells rather than in whole-tissue specimens.

Differential Diagnosis

Cutaneous lesions with heavy mixed infiltrates could be confused with a variety of inflammatory dermatoses, unless the typical cells of Hodgkin disease are identified. Of course, this is less likely to be a problem when there is a known history of nodal or systemic disease. The neoplastic cells of Hodgkin disease closely resemble the atypical cells of type A lymphomatoid papulosis. Lymphomatoid papulosis can precede the onset of Hodgkin disease, and rare cases of primary cutaneous Hodgkin disease present with self-healing papulonodular lesions that are close clinical mimics of lymphomatoid papulosis. Although the atypical cells of lymphomatoid papulosis are also CD30+, they are usually CD15− and CD45+, in contrast with Hodgkin and Reed-Sternberg cells. CD30+ ALCL can also resemble Hodgkin disease. However, the polymorphous inflammatory infiltrate of Hodgkin disease is distinctive.³¹⁸ Also, in contrast to ALCL, the neoplastic cells of Hodgkin disease are positive for B-cell–specific activator protein and are negative for epithelial membrane antigen and the ALK protein.^485,500 The latter two staining results help make a distinction from systemic ALCL. Although the neoplastic cells in primary cutaneous CD30+ large-cell lymphoma are also typically negative for epithelial membrane antigen and ALK, those cells are usually positive for CD4.²⁰⁹ Positivity for EBV latent membrane protein also favors Hodgkin disease in this context.⁴⁸⁵ A distinction from anaplastic large B-cell lymphoma may not always be possible, but this is not likely to be a major issue in cases of cutaneous Hodgkin disease, particularly when all the clinical and histopathologic features are taken into account. Recently, Cho and colleagues reported an example of cutaneous nodules occurring in a man with classic Hodgkin lymphoma. As in a lymph node biopsy, the Reed-Sternberg and Hodgkin cells showed weak PAX5 positivity and weak focal Oct-2 positivity and were negative for BOB.1. These results are consistent with Hodgkin lymphoma and argue against T-cell lymphoma (in which all three markers are absent) and other non-Hodgkin B-cell lymphomas (in which all three markers are strongly expressed).^501–503

Leukemia Cutis

Clinical Features

Cutaneous involvement in the leukemias can be categorized as specific leukemic infiltrates and nonspecific manifestations. This section will focus on specific lesions of leukemia cutis. However, nonspecific lesions can be sources of clinical confusion with true leukemic infiltrates, complications related to leukemias (e.g., purpura due to thrombocytopenia, cutaneous infection due to immunosuppression), or closely linked reactive processes. Examples of the latter conditions include generalized pruritus, Sweet syndrome, pyoderma gangrenosum,⁵⁰⁴ and drug eruptions.⁵⁰⁵ More recently, there have been reports of arthropod bite–like reactions in patients with leukemias and lymphomas⁵⁰⁶ (Fig. 27-45).

Figure 27-45 Arthropod bite–like reaction in a patient with leukemia. Findings include spongiotic intraepidermal vesicles and a wedge-shaped dermal infiltrate containing numerous eosinophils. Leukemic cells were not identified in the sections.

Specific cutaneous lesions have been reported in most of the leukemias. These include acute myeloid leukemias (M1–M3 in the French-American-British [FAB] classification), acute myelomonocytic leukemia (M4), acute monocytic leukemia (M5), acute erythroleukemia (M6), acute lymphoblastic leukemia, chronic myelogenous leukemia, chronic myelomonocytic leukemia, chronic lymphocytic leukemia, adult T-cell leukemia, T-cell prolymphocytic leukemia (formerly T-cell chronic lymphocytic leukemia), and hairy cell leukemia.⁵⁰⁷ The author has already discussed the lymphomatous counterparts of acute lymphoblastic leukemia (precursor B-lymphoblastic lymphoma), ATLL, and precursor T-lymphoblastic leukemia/lymphoma. Aggressive NK cell leukemia will be considered briefly; although it may represent the leukemic form of extranodal NK/T-cell lymphoma, nasal type, this has not been established with certainty.⁵⁰⁸

The frequency of specific lesions of leukemia cutis varies, depending on the type of leukemia. Cutaneous involvement is common in monocytic leukemia, occurring in about 10% to 50% of cases.⁵⁰⁹ It is also relatively frequent in chronic lymphocytic leukemia, particularly in T-cell subtypes, such as T-cell chronic lymphocytic leukemia⁵⁰⁷ and T-cell large granular lymphocytic leukemia.^510,511 Specific skin lesions are less common in other varieties, such as acute lymphoblastic leukemia, myeloid leukemias, and hairy cell leukemia.^507,512,513 Lesions of leukemia cutis are most often papules and nodules. Plaques, ulcers, and purpuric lesions also occur.^509,514,515 Unusual manifestations include erythroderma^507,516 and bullous lesions.⁵¹⁵ Pigmentary changes have been associated with leukemia cutis; both hyperpigmented and vitiligo-like lesions have been described.^517,518 Gingival hypertrophy is associated with monocytic and myelomonocytic leukemias. The chloroma (granulocytic sarcoma), a green to greenish-gray tumor, is a characteristic if uncommon lesion associated with acute myeloid leukemia. Its greenish color is due to the presence of high concentrations of myeloperoxidase in infiltrating myeloblasts.⁵⁰⁹ Lesions appearing at arterial and venous puncture sites have been reported in acute promyelocytic leukemia (M3).⁵¹⁹

There is a strong association between specific lesions of leukemia cutis and involvement of other extramedullary sites.520,521 The appearance of cutaneous lesions of leukemia is associated with a poor prognosis.^515,521 Aleukemic leukemia cutis refers to the occurrence of leukemic skin lesions prior to detection of peripheral blood or bone marrow involvement. Although uncommon, there are numerous reports of this phenomenon, most of which involve cases of acute monocytic or myelomonocytic leukemia,^522–524 but also in acute lymphoblastic leukemia.⁵²⁵

Microscopic Findings

Most varieties of leukemia cutis feature dense dermal infiltrates of atypical cells with infiltration between collagen bundles.⁵²⁶ A grenz zone separating the infiltrate from the overlying epidermis is frequently described in the non–T-cell leukemias.^507,527 The atypical cells often display a perivascular and/or periadnexal distribution.^507,513 Infiltration and destruction of adnexal structures, vessels, nerves, and muscle are seen, particularly in myeloid, monocytic, and myelomonocytic leukemias^507,526 (Fig. 27-46). Examples of “leukemic vasculitis” have been described, in which infiltration of vessels by atypical cells may be associated with destruction of vessels walls and fibrin deposition.^528–530 A Kaposi sarcoma–like pattern has been reported in myeloid leukemias, in which myeloblasts appear to line slitlike, blood-filled spaces.⁵²⁷ The cells of chronic lymphocytic leukemia can also appear in other types of cutaneous lesions, where they can be recognized in varying sized clusters of monotonous, small- to medium-sized cells⁵³¹ (Fig. 27-47A and B). Recognition of the cytologic characteristics of the cells can be important in refining the diagnosis. Formerly described T-cell variants of chronic lymphocytic leukemia were reported to show epidermotropism.⁵⁰⁷ However, a recent series of cases of T-cell prolymphocytic leukemia (the current term that encompasses T-cell chronic lymphocytic leukemia) showed that dermal infiltrates were angiocentric rather than epidermotropic, composed of cells with irregular nuclei, small nucleoli, and rims of eosinophilic cytoplasm^531a (Fig. 27-48A and B). The myeloblasts of acute myeloid leukemias are large cells with round to oval nuclei, fine to coarse (when minimally differentiated) chromatin, and scant basophilic cytoplasm (Fig. 27-49). Chronic myeloid leukemia features a much more varied cell population, including atypical myelocytes, metamyelocytes, eosinophil precursors, and mature neutrophils. In monocytic leukemias, monocytoid forms have indented nuclei with fine to lacy chromatin and one or more distinct nucleoli. In acute lymphoblastic leukemia, the cells are medium to large with fine to reticulated chromatin and scant to moderate amounts of cytoplasm (Fig. 27-50); in comparison, the lymphocytes are smaller and relatively mature in appearance in chronic lymphocytic leukemia. In hairy cell leukemia, the characteristic cytoplasmic projections are not seen in routinely processed skin specimens; tissue imprints are required to see them.⁵⁰⁷ Furthermore, fresh specimens are necessary to demonstrate staining with tartrate-resistant acid phosphatase.⁵³²

Figure 27-46 Myelomonocytic leukemia. There is a dense dermal infiltrate, separated from the epidermis by a grenz zone of uninvolved connective tissue. The leukemic cells insinuate between collagen bundles and also permeate vessels and adnexal epithelia.

Figure 27-47 Chronic lymphocytic leukemia. Aggregates of small, monotonous-appearing lymphoid cells are found adjacent to islands of basal cell carcinoma (A). Higher power view (B) shows the cytologic detail of these cells. The cells of chronic lymphocytic leukemia frequently stain positively for CD20 (C) and CD43 (D).

Figure 27-48 T-cell prolymphocytic leukemia. A, Dermal cellular aggregates are angiocentric rather than epidermotropic. B, The cells have irregularly contoured nuclei, small nucleoli, and rims of eosinophilic cytoplasm.

Figure 27-49 Acute myeloid leukemia. The myeloblasts are large cells with round to oval nuclei.

Figure 27-50 Acute lymphoblastic leukemia. In this particular preparation, the cells show fine chromatin and generally scant amounts of cytoplasm.

Histochemistry and immunohistochemistry can be of great help in reaching a specific diagnosis of the type of leukemia cutis. Among the most useful stains in formalin-fixed, paraffin-embedded tissues are chloroacetate esterase (Leder stain; CAE) and immunohistochemical stains for myeloperoxidase (MPO), lysozyme, and CD20, CD30, CD43, CD45, CD45RO, and CD68. The Leder stain (CAE) typically decorates only myelocytes and mature granulocytes (mast cells also stain with this method), and therefore earlier myeloid precursors require recognition through other means. Several detailed schemes have been provided for the use of immunohistochemical stains in the workup of atypical dermal infiltrates for possible leukemia cutis.507,533 Cells of myeloid leukemias express lysozyme and (within the limits specified above) CAE. MPO positivity is found in myeloid and myelomonocytic leukemias. Monocytic and myelomonocytic leukemias are CD43+ and CD68+.^534–536 In the algorithm proposed by Cronin and associates, atypical CD3− and CD20− infiltrates can be stained for CD43, MPO, CD68, CD56, and CD117 as a means of separating myeloid leukemia cutis from other entities such as BPDCN, mast cell sarcoma, and other lymphoproliferative disorders.⁵³³ This will be discussed further (see “Differential Diagnosis”). In acute lymphoblastic leukemia, the usual profile is CD19+, CD20+ (variable), CD79a+, CD10+, and HLA-DR+. As a practical matter in formalin-fixed skin specimens, the most noteworthy immunohistochemical finding is that neoplastic cells are weakly positive or negative for CD20 and, among the other common lymphocyte markers, may only express CD45.⁵⁰⁷ In paraffin-embedded tissues, the cells of chronic lymphocytic leukemia frequently express CD20 and CD43 (see Fig. 27-47C and D).

A leukemia-associated surface antigen, JL1, appears to stain examples of both lymphoblastic and acute myelogenous leukemia and does not stain other cutaneous lesions or normal tissues. Despite this degree of specificity, JL1 appears to have limited sensitivity; it was positive in about two thirds of cases of acute lymphoblastic leukemia/lymphoma and one third of cases of acute myelogenous leukemia.⁵³⁷ CD99, representing the E21/MIC2 gene product, is regularly positive in skin lesions of acute lymphoblastic leukemia and in a high percentage of those of acute myeloid leukemia.⁵³⁸ In a case of aggressive NK cell leukemia involving the skin, the neoplastic cells were CD2+, CD8+, CD56+, TIA-1+, and granzyme B+; positive for EBV by in situ hybridization; and CD3−, CD4−, CD16−, and CD57−.⁵³⁹ In T-cell large granular lymphocytic leukemia, the infiltrating cells are CD3+, CD4−, and CD8+, and EBV infection may again be demonstrable.⁵¹⁰

Differential Diagnosis

The presence of atypical cutaneous infiltrates with the morphologic changes outlined above should suggest the possibility of leukemia cutis. A more detailed clinical and laboratory investigation should then follow; specific diagnosis depends on findings in bone marrow and peripheral blood. In the case of aleukemia cutis, close clinical follow-up is indicated to detect early development of systemic disease. A distinction from cutaneous lymphoma can be a major challenge, but it should be recognized that a number of these disorders (e.g., ATLL, acute lymphoblastic leukemia/precursor B-lymphoblastic lymphoma) actually have both leukemic and nonleukemic phases. Diagnosis may also be challenging when there are only a few atypical cells obscured by a dense, reactive infiltrate, as has been described in some lesions resembling Sweet syndrome or pyoderma gangrenosum.⁵²⁷ Regarding immunohistochemical staining, myeloid leukemia cutis is a likely diagnosis when CD3−/CD20− infiltrates are found to be CD43+/MPO+ or CD43+/MPO−/ CD68+/CD56−/CD117−.⁵³³ Examples that are CD56+ can be distinguished from BPDCN by using stains for CD4 and CD123, which are positive in the latter disorder (CD4 may also be positive in myeloid leukemias with monocytic differentiation); those that prove to be CD117+ can be distinguished from mast cell sarcoma by staining for tryptase or microphthalmia transcription factor, each of which stains mast cells but not myeloid cells.^533,540 S-100 positivity has been reported in rare examples of myeloid leukemia cutis, and in one recent case this was associated with cytophagic activity.⁵⁴¹ Such a result could lead to an erroneous diagnosis of melanoma, Rosai-Dorfman disease, or phagocytic activity associated with a lymphoid neoplasm, thus emphasizing the need for use of immunohistochemical panels as well as clinicopathologic correlation.

Extramedullary Hematopoiesis

Clinical Features

Cutaneous hematopoiesis normally occurs in the 8-cm stage embryo and ceases by 34 to 38 weeks’ gestation.⁵⁴² After this stage, cutaneous hematopoiesis is distinctly unusual, arising principally in two settings: (1) in neonates, associated with abnormalities that have begun in utero, and (2) in adults, usually associated with myelofibrosis and often following splenectomy.⁵⁴³

Neonatal hematopoiesis has been associated with congenital viral infections, particularly rubella, cytomegalovirus, and coxsackie virus B2, as well as in twin transfusion syndrome, Rh-hemolytic disease of the newborn, and hereditary spherocytosis.542,544–546 It has also been reported in diffuse hemangiomatosis in a newborn.⁵⁴⁷ In cases not associated with hemangiomas, the cutaneous eruption consists of petechiae, purpuric macules, papules, and plaques, and ecchymotic lesions; the more purpuric of these are often referred to as “blueberry muffin” lesions.^542,548 The head, neck, and trunk are mainly involved.⁵⁴² The prognosis depends on the underlying condition and its resulting complications. Skin lesions tend to fade within 3 to 6 weeks after birth.⁵⁴²

Most adults reported with cutaneous extramedullary hematopoiesis have had myelofibrosis,543,549,550 but sporadic cases have also been associated with agnogenic myeloid metaplasia, polycythemia vera, and chronic myelogenous leukemia.⁵⁵¹ Lesions consist of erythematous to purpuric papulonodules.^549,552,553 A case with bilateral leg ulcers has also been described.⁵⁵⁴ Head and neck, trunk, and extremities have all been involved. Again, prognosis depends on the course of the underlying disease. Responses have been reported to hydroxyurea^543,555 and electron beam therapy.⁵⁴³

Microscopic Findings

An infiltrate of varying intensity is found in the dermis and subcutis, both in a perivascular and interstitial distribution. It includes varying combinations of myeloid and erythroid elements as well as megakaryocytes. Myeloid cells in different stages of maturation are present; in some reports, there has been an increase in cells of eosinophil lineage.549,552 Nucleated erythrocytes are often observed⁵⁴² (Fig. 27-51). Megakaryocytes are large, atypical cells with pale eosinophilic cytoplasm and multiple or multilobated nuclei.^552,555 The neonatal cases frequently display only erythrocyte precursors, and myeloid cells are only occasionally present; for this reason, the term cutaneous erythropoiesis is sometimes applied to lesions in newborns.⁵⁴² All three hematopoietic elements are present in some adult cases,^550,553 but some reports have indicated a lack of erythrocyte precursors.⁵⁵² Fibroblasts often accompany the process. Reticulin can be shown to surround megakaryocytes with Wilder or other methods.⁵⁵²

Figure 27-51 Extramedullary hematopoiesis. Nucleated erythrocytes are apparent in this section.

Granulocytes stain red with chloroacetate esterase (Leder stain; CAE) and also stain positively for MAC387. Megakaryocytes and scattered fibroblast-like cells are positive for factor XIIIa, and megakaryocytes also express factor VIII–related antigen.⁵⁵² Fine cytologic details of cells of erythroid and myeloid lineage can be viewed ultrastructurally.⁵⁴⁸

Recently, mutation of the Janus kinase-2 gene (JAK2 V617F) was identified within lesions of cutaneous myelofibrosis, demonstrating that such lesions represent metastases and not simply “reactive” extramedullary hematopoiesis.⁵⁵⁶ In another study, Kawakami and coworkers found that transforming growth factor-beta (TGF-β) was overexpressed in the hematopoietic cells and dermal fibroblasts of cutaneous extramedullary hematopoiesis in a patient with myelofibrosis who eventually succumbed to bone marrow failure. A high titer of TGF-β was also found in the patient’s plasma. It was postulated that this peptide might have played a role in the promotion of extramedullary hematopoiesis and the myelofibrosis that occurred in this patient.⁵⁵⁷

Differential Diagnosis

In neonates, the microscopic features of cutaneous extramedullary hematopoiesis provide a clue to an underlying systemic condition, particularly a congenital infection or hematologic abnormality. In adults, extramedullary hematopoiesis can be difficult to differentiate from chronic myelogenous leukemia. This is a particular problem in myelofibrosis-associated extramedullary hematopoiesis, which has a number of features in common with chronic myelogenous leukemia. However, myelofibrosis is not associated with the Philadelphia chromosome.⁵⁵² Furthermore, erythroid precursors are of help in the recognition of extramedullary hematopoiesis, and the finding of megakaryocytes can also aid in the distinction between this disorder and chronic myelogenous leukemia.^552,555

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