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Background
MALTomas stand for mucosal associated lymphoid tissue. These are the extra-nodal equivalent of monocytoid (marginal zone) B-cell lymphomas occurring in lymphoid organs such as the lymph node. These lymphomas arise in numerous extranodal sites such as the stomach, salivary gland and thyroid, most of which lack native lymphoid tissue but acquire MALT in close association with chronic inflammation or autoimmune processes. MALT lymphomas appear to have similar clinical, pathological and molecular features regardless of organs of origin.
OUTLINE
PATHOGENESIS CHARACTERIZATION BCL10
MALT1 and BCL10 aberrations in MALT lymphomas and their effect on the expression of BCL10 in the tumour cells.
Sagaert X, Laurent M, Baens M, Wlodarska I, De Wolf-Peeters C.
1Division of Morphology and Molecular Pathology, Katholieke Universiteit Leuven, Leuven, Belgium.
Mod Pathol. 2006 Feb;19(2):225-32. Abstract quote
Among the genetic abnormalities reported to occur in mucosa-associated lymphoid tissue (MALT) lymphomas, the three translocations t(11;18)(q21;q21), t(1;14)(p22;q32) and t(14;18)(q32;q21) are of particular interest because they appear to be specific for, or at least closely related to this type of B-cell non-Hodgkin's lymphoma. These translocations affect the MALT1 (18q21) and BCL10 (1p22) genes.
We retrieved 77 consecutive biopsies of MALT lymphomas (documented with frozen material) over a 10-year period and investigated these cases for the presence of these three translocations with fluorescence in situ hybridisation, along with the immunohistochemical analysis of the intracellular localisation of the BCL10 protein. The above-listed translocations occurred mutually exclusive and were detected in 10, 1 and 3% of the cases, respectively (the latter incidence being much lower than in the previously reported studies by one single group). These genetic rearrangements corresponded well with the aberrant subcellular localisation of the BCL10 protein as found by immunohistochemistry: t(11;18)(q21;q21) and (1;14)(p22;q32) were marked by a, respectively, moderate to strong nuclear BCL10 staining pattern while t(14;18)(q32;q21)-positive MALT lymphomas were characterised by a perinuclear BCL10 staining pattern.
This study further supports the close interaction between the MALT1 and BCL10 proteins in the pathogenesis of MALT lymphomas and may indicate that BCL10 immunohistochemistry is a simple technique to identify those MALT lymphoma cases with an underlying genetic aberration.Novel translocation of the BCL10 gene in a case of mucosa associated lymphoid tissue lymphoma.
Achuthan R, Bell SM, Leek JP, Roberts P, Horgan K, Markham AF, Selby PJ, MacLennan KA.
Molecular Medicine Unit, University of Leeds, Clinical Sciences Building, St. James's University Hospital, Leeds, United Kingdom.
Genes Chromosomes Cancer 2000 Dec;29(4):347-9 Abstract quote
Interest has focused on a recently identified gene, BCL10, thought to play an important role in the genesis of extranodal, marginal zone (MALT) lymphomas. This gene belongs to a family containing caspase recruitment domains (CARD), that are involved in the apoptotic pathway. Translocations of the BCL10 gene to the immunoglobulin heavy chain locus at 14q32 have been described.
We report herein a case of MALT lymphoma showing t(1; 2)(p22; p12). The translocation was shown to involve the BCL10 gene and the immunoglobulin kappa light chain locus by fluorescence in situ hybridization.
CHROMOSOMAL ABNORMALITIES
Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester MN.
Several balanced translocations have been identified in extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) but there are few data regarding their frequency in different anatomic sites or the frequency of translocations involving BCL6 or kappa or lambda immunoglobulin light chain genes (IGK or IGL), particularly in patients from geographic regions other than Europe and Japan.
One hundred thirty-three paraffin-embedded North American primary MALT lymphoma specimens from diverse anatomic sites were studied by fluorescence in situ hybridization (FISH) using probes for API2-MALT1, IGH-MALT1, IGH-BCL10, IGH-FOXP1, IGH, +/- centromeres 3, 7, 12, and 18, and a subset (n=74) were analyzed using FISH probes for IGK, IGL, and BCL6. Translocations were mutually exclusive and were detected in 26% of cases (17% API2-MALT1, 5% IGH-MALT1, 3% IGH-unknown translocation partner, and 1% IGH-BCL10). Aneuploidy was associated with IGH-MALT1 and IGH-BCL10 but only rarely with API2-MALT1. There was striking site specificity, with API2-MALT1 showing a marked predilection for lung and intestine, and IGH-MALT1 and IGH-BCL10 occurring almost exclusively in lung. Twenty-three percent of translocation-negative primary MALT lymphomas from diverse sites showed complete/partial trisomy 18. No MALT lymphomas with translocations involving IGK, IGL, BCL6, or FOXP1 were identified.
This FISH panel detected cytogenetic abnormalities in half of all MALT lymphomas, and translocations arose preferentially in MALT lymphomas of the lung and gastrointestinal tract.
Differences in incidence and anatomic site specificity of translocations between North American and non-North American cases may reflect geographic variability of infectious or other etiologic factors.CYCLIN DEPENDENT KINASES
Methylation analysis of cyclin-dependent kinase inhibitor genes in primary gastrointestinal lymphomas.Go JH.
Department of Pathology, Dankook University College of Medicine, Cheonan, Korea. e stomach and intestine.
Mod Pathol. 2003 Aug;16(8):752-5. Abstract quote The CIP/KIP family of cyclin-dependent kinase inhibitors may act as tumor suppressors.
To assess promoter hypermethylation as a potential underlying mechanism for loss of expression, methylation-specific polymerase chain reaction for p21 and p27 genes was performed in 13 gastric low-grade mucosa-associated lymphoid tissue (MALT) lymphomas, 13 gastric high-grade B-cell lymphomas, and 14 intestinal diffuse large B-cell lymphomas. p21 and p27 genes were unmethylated in normal Peyer's patch and tonsillar tissues. Promoter hypermethylation of p21 gene was detected only in some gastric low-grade MALT lymphomas (4/13, 31%). All gastric and intestinal high-grade lymphomas revealed unmethylated status of p21 gene. p27 gene was unmethylated in all cases of low- and high-grade gastrointestinal lymphomas.
These results suggest that p21 promoter methylation is involved in some low-grade MALT lymphomagenesis in stomach and seems to be an early event in the gastric lymphomagenesis. And promoter methylation is not the underlying mechanism for loss of p27 protein expression in the malignant lymphomas of the stomach and intestine.
TOXOPLASMA GONDII Detection of Toxoplasma Gondii DNA in Primary Intraocular B-Cell Lymphoma
De Fen Shen, Ph.D., Carl P. Herbort, M.D., Nadine Tuaillon, Ph.D., Ronald R. Buggage, M.D., Charles E. Egwuagu, Ph.D. and Chi-Chao Chan, M.D.
Laboratory of Immunology (DFSNT, RRB, CEE, C-CC), National Eye Institute, National Institutes of Health, Bethesda, Maryland; and University of Lausanne and Uveitis & External Diseases (CPH), Eye Center La Source, Lausanne, Switzerland
Mod Pathol 2001;14:995-999 Abstract quote
We analyzed 10 cases of primary intraocular lymphoma using microdissection and PCR. Tumor and normal cells were microdissected from ocular tissue on slides and subjected to PCR for genes from Toxoplasma gondii, EBV, and HHV-8.
We detected Toxoplasma gondii, not HHV-8 or EBV, DNA in the lymphoma but not in normal cells of two cases that resembled ocular toxoplasmosis clinically.
We speculate that Toxoplasma gondii may play a role in some forms of primary intraocular B-cell lymphoma.
HISTOLOGICAL TYPES CHARACTERIZATION EYE Clinical, Histopathological, and Immunogenetic Analysis of Ocular Adnexal Lymphoproliferative Disorders: Characterization of MALT Lymphoma and Reactive Lymphoid Hyperplasia
Tomohiko Mannami, M.D., Tadashi Yoshino, M.D., Ph.D., Koichi Oshima, M.D., Ph.D., Sumie Takase, M.D., Eisaku Kondo, M.D., Ph.D., Nobuya Ohara, M.D., Ph.D., Hideki Nakagawa, M.D., Ph.D., Hiroshi Ohtsuki, M.D., Ph.D., Mine Harada, M.D., Ph.D. and Tadaatsu Akagi, M.D., Ph.D.
Second Department of Internal Medicine (TMMH), Department of Pathology (TY, ST, EK, NO, TA), and Department of Ophthalmology (KO, HN, HO), Okayama University Medical School, Okayama, Japan.
Mod Pathol 2001;14:641-649 Abstract quote
Malignant lymphomas and reactive lymphoid hyperplasia (RLH) in the ocular adnexa are sometimes difficult to differentiate morphologically and have often been categorized together as a lymphoproliferative disorder. Immunogenotypic characters of these diseases have not yet been well clarified.
This study included 76 cases of ocular adnexal lymphoproliferative disorders. These consisted of 52 cases of malignant lymphoma (43 primary and 9 secondary), 22 of RLH, and 2 borderline cases. There were slightly more male than female subjects. Diagnoses were based on morphology and immunophenotypic characteristics. Clonalities were detected by means of polymerase chain reaction (PCR), and immunoglobulin heavy-chain variable region (VH) genes were sequenced in 10 cases of mucosa-associated lymphoid tissue (MALT) lymphoma. MALT lymphoma constituted 86% (37 cases) of the primary lymphomas. MALT lymphomas were more indolent, more rarely disseminated, and had a lower death rate than the other primary lymphomas. Two patients exhibited coexistence of MALT and diffuse large B-cell lymphoma.
The average age of patients with RLH was 5.5 years younger than that of those with MALT lymphoma. One of the cases of RLH later progressed to malignant lymphoma. B-cell clonality was detected by PCR in 57%, 55%, and 0% of primary lymphomas, MALT lymphomas and RLHs, respectively. Sequencing of VH genes revealed that the VH3 family was the most commonly expressed germline VH family (70%) and that DP-63, DP-54 and DP-47 genes were frequently found in the MALT lymphomas examined. PCR analysis was useful for differentiation between MALT lymphoma and RLH.
Sequence analysis of VH genes showed that an autoimmune mechanism may be involved in the lymphomagenesis of ocular adnexal MALT lymphoma.
KIDNEY
- Low-grade mucosa-associated lymphoid tissue lymphoma involving the kidney: report of 3 cases and review of the literature.
Qiu L, Unger PD, Dillon RW, Strauchen JA.
Department of Pathology, Mount Sinai Medical Center, New York, NY 10029, USA.
Arch Pathol Lab Med. 2006 Jan;130(1):86-9. Abstract quote
Low-grade B-cell lymphoma of mucosa-associated lymphoid tissue involving the kidney is rare.
We report a series of 3 cases. The first case occurred in an 83-year-old woman who presented with back pain. The second case was a 53-year-old man with a history of sarcoidosis who was found, in the course of evaluation of sarcoidosis, to have a right renal mass. The third case occurred in a 72-year-old man who had a history of periorbital mucosa-associated lymphoid tissue lymphoma and had been treated with surgery and radiation 1 year prior to this presentation.
Histologically, all 3 patients showed infiltrate of uniform small-to-medium-sized lymphocytes with irregular nuclear contours and abundant cytoplasm resembling centrocytes or monocytoid lymphoid cells. The first patient received chemotherapy without complications. The second patient underwent a partial nephrectomy and was asymptomatic at the subsequent follow-up.
The third patient developed a pulmonary embolism following nephrectomy, and further follow-up is not available.
LARYNX Hodgkin-like transformation of a marginal zone B-cell lymphoma of the larynx
Eric K. Fung, MD
Thomas S. Neuhauser, MD
Lester D.R. Thompson, MDAnn Diagn Pathol 6: 61-66, 2002. Abstract quote
Primary larynx lymphomas, specifically of the mucosa-associated lymphoid tissue, are a rare but documented phenomenon. Transformation of any type of lymphoma that has the presence of Reed-Sternberg cells is unusual in lymph nodes and exceptional in extranodal sites.Herein, we report the first case (to the best of our knowledge in a review of the English literature [MEDLINE 1966-2001]) in which both of these unusual findings are present; that is, an extranodal marginal zone B-cell lymphoma of laryngeal mucosa-associated lymphoid tissue with Hodgkin-like transformation. The patient is a 78-year-old man who presented with intermittent shortness of breath, progressive dysphagia, and intermittent hoarseness. On examination, a large mass of the left supraglottic larynx was identified with a “ball-valve” effect into the laryngeal inlet with inspiration. Examination of the neck showed no palpable masses.
Histologic examination of the incisional biopsy showed replacement of the submucosa by sheets of atypical monocytoid B cells (CD20+, CD79a+, lambda+, CD3–) characterized by nuclear atypia, mitotic activity, plasmacytoid differentiation, and restricted for lambda light chains. Dutcher bodies were easily identified. Interspersed throughout the neoplastic lymphoid population were numerous Reed-Sternberg cells and variants immunoreactive for CD30 and CD15 and nonreactive for CD45RB.
The patient was treated with 44 cGy to the neck and larynx and was alive and free of disease at last contact, 2.6 years after the original presentation.
LUNG Primary Lung Small B-Cell Lymphoma versus Lymphoid Hyperplasia Evaluation of Diagnostic Criteria in 26 Cases
Hugues Bégueret, M.D. ; Béatrice Vergier, M.D. ; Marie Parrens, M.D. ; Philippe Lehours, M.D. ; François Laurent, M.D. ; Jean-Marc Vernejoux, M.D. ; Pierre Dubus, M.D. , Ph.D. ; Jean-François Velly, M.D. ; Francis Mégraud, M.D. , Ph.D. ; André Taytard, M.D. ; Jean-Philippe Merlio, M.D. , Ph.D. ; Antoine de Mascarel, M.D.
From the Department of Pathology and Molecular Biology (H.B., B.V., M.P., P.D., J.-P.M., A.d.M.), Université de Bordeaux, and the Departments of Radiology (F.L.), Pulmonary Pathology (J.-M.V., A.T.), and Thoracic Surgery (J.-F.V.), Hôpital du Haut-Lévêque, Pessac, France; and the Department of Bacteriology (P.L., F.M.), Hôpital Pellegrin, Bordeaux, France
Am J Surg Pathol 2002;26:76-81 Abstract quote
Primary lung non-Hodgkin's lymphoma is a rare neoplasm mostly represented by low-grade B-cell lymphomas of mucosa-associated lymphoid tissue. Their diagnostic criteria are now well defined on surgical specimens, but pathologists may experience difficulties in distinguishing them on exiguous biopsies from benign lymphoid hyperplasia and other lymphomas.
Therefore, we examined a series of 26 lung lymphoid lesions to further define the pathologic features of either lymphoma or lymphoid hyperplasia on small specimens. We observed 16 primary lung non-Hodgkin's lymphomas with a large predominance of low-grade mucosa-associated lymphoid tissue-type lymphomas (87.5%, n = 14). There were no autoimmune disorders, but three patients had a concomitant infectious disease (hepatitis C virus and Helicobacter pylori gastritis). One patient presented with a synchronous pulmonary adenocarcinoma. As well as the classical mucosa-associated lymphoid tissue cellular infiltrate, immunohistochemical characterization of the 14 mucosa-associated lymphoid tissue-type lymphomas revealed the CD20+/CD43+ centrocyte-like cell phenotype in 10 cases (71.5%).
Although the lymphoepithelial lesions observed in all lymphomatous cases have been reported in lung lymphoid hyperplasia, the determination of B-cell CD20+/CD43+ phenotype of the intraepithelial lymphocytes highly increased the specificity of lymphoepithelial lesions. A monoclonal immunoglobulin heavy chain gene rearrangement was present in 71.4% of the mucosa-associated lymphoid tissue-type lymphoma specimens. Investigation of H. pylori by polymerase chain reaction detection was negative, even for the two cases associated with H. pylori gastritis.
SALIVARY GLAND Extranodal marginal-zone B-cell lymphoma of the salivary gland
Susan L. Abbondanzo, MD
From the Department of Hematopathology, Armed Forces Institute of Pathology, Washington, DC.
Ann Diagn Pathol 5: 246-254, 2001 Abstract quote
Primary non-Hodgkin's lymphoma of the salivary gland is an uncommon tumor that most often occurs in the parotid gland. The most common subtype is marginal-zone B-cell lymphoma, extranodal, mucosa-associated lymphoid tissue type. This subtype has recently been included in the Revised European-American Classification of Lymphoid Neoplasms, as well as in the upcoming World Health Organization classification of hematopoietic and lymphoid neoplasms.
This low-grade lymphoma usually arises in a background of benign lymphoepithelial lesion or myoepithelial sialadenitis that is associated with the autoimmune disease Sjögren's syndrome. It occasionally develops in patients who do not have a history of autoimmune disease. When mucosa-associated lymphoid tissue lymphoma occurs in the salivary gland, as in other extranodal sites such as the stomach, it is usually an indolent neoplasm that tends to remain localized for long periods of time, even without treatment. Eventually, however, the tumor may disseminate or transform to a higher grade. The histologic distinction of myoepithelial sialadenitis from low-grade B-cell mucosa-associated lymphoid tissue lymphoma can be a difficult diagnostic challenge and many of these lesions continue to be ambiguously diagnosed as “pseudolymphoma.” Immunophenotypic or flow cytometric analysis may be useful in showing an aberrant phenotype or immunoglobulin light-chain restriction, which helps to support a diagnosis of malignant lymphoma in most cases. Molecular genetic analysis for immunoglobulin gene rearrangements also may be useful in showing monoclonality, although the exact significance of this finding in some cases remains controversial.
STOMACH THYMUS GLAND Mucosa-Associated Lymphoid Tissue of the Thymus Hyperplasia vs Lymphoma
Marie Parrens, MD
Pierre Dubus, MD, PhD
Marie Danjoux, MD
Jacques Jougon, MD
Pierre Brousset, MD, PhD
Jean-François Velly, MD
Antoine de Mascarel, MD
and Jean P. Merlio, MD, PhDAm J Clin Pathol 2002;117:51-56 Abstract quote
In the thymus, the relationship between lymphofollicular hyperplasia and mucosa-associated lymphoid tissue (MALT)-type lymphoma is uncertain.
We analyzed 14 cases with a diagnosis of thymic follicular hyperplasia in patients with connective tissue disease (n = 2), myasthenia gravis (n = 11), or both (n = 1). In 11 cases, well-defined reactive lymphoid follicles were surrounded by a continuous layer of medullary epithelial cells. A polyclonal rearrangement of the immunoglobulin heavy chain gene (IgH) was observed. In 3 cases, ill-defined lymphoid follicles with sheets of centrocytic-like B cells disrupting the medullary cytokeratin epithelial network were observed on certain sections. These cells expressed the phenotypic features of memory B cells with CD20, CD79a, and bcl-2 positivity and CD5, CD10, CD23, and bcl-6 negativity, and a monoclonal rearrangement of the IgH gene was detected.
Appropriate sampling, cytokeratin staining, and molecular analyses may help to identify early MALT-type lymphoma developing in the setting of thymic lymphofollicular hyperplasia.
THYROID GLAND Malignant Lymphoma of the Thyroid Gland A Clinicopathologic Study of 108 Cases
Gregory A. Derringer, M.D.; Lester D. R. Thompson, M.D.; R. Allen Frommelt, Ph.D.; Karen E. Bijwaard, M.S.; Clara S. Heffess, M.D., COL, MC, USA; Susan L. Abbondanzo, M.D.
From the Departments of Hematopathology (G.A.D., S.L.A.), Endocrine and Otorhinolaryngic-Head & Neck Pathology (L.D.R.T., C.S.H.), Cellular Pathology (K.E.B.), and Department of Epidemiology, Repository and Research Services (R.A.F.), Armed Forces Institute of Pathology, Washington, DC, U.S.A.
Am J Surg Pathol 2000;24:623-639 Abstract quote
We report a retrospective clinicopathologic study of 108 primary thyroid gland lymphomas (PTLs), classified using the REAL and proposed WHO classification schemes.
The patients included 79 women and 29 men, with an average age of 64.3 years. All patients presented with a thyroid mass. The PTLs were classified as marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT) or MZBL (n = 30), diffuse large B-cell lymphoma (DLBCL) with MZBL (n = 36), DLBCL without MZBL (n = 41), and follicle center lymphoma (FCL; n = 1). Excluding the FCL, features of lymphomas of MALT-type were identified in all groups, despite a follicular architecture in 23% of cases. Lymphocytic thyroiditis (LT) was identified in 94%. Ninety-one percent of patients presented with stage IE or IIE disease, whereas 69% had perithyroidal soft tissue infiltration.
All patients were treated with surgical excision followed by adjuvant therapy (76%): chemotherapy (15%), radiation (19%), or a combination of radiation and chemotherapy (42%). Disease-specific survival was 82% at last follow up (mean, 82.8 mos) and 79% at 5 years. Statistically, stages greater than IE, presence of DLBCL, rapid clinical growth, abundant apoptosis, presence of vascular invasion, high mitotic rate, and infiltration of the perithyroidal soft tissue were significantly associated with death with disease. No patients with MZBL or stage IE disease died with disease.
In summary, PTLs typically occur in middle-to older-aged individuals as a thyroid mass, with a predilection for females. Despite their histologic heterogeneity and frequent simulation of other lymphoma subtypes, virtually all PTLs are lymphomas of MALT-type arising in the setting of LT. Mixed DLBCL and MZBL are common.
Overall, PTLs have a favorable outcome with appropriate therapy, but prognosis depends on both clinical stage and histology. MZBL and stage IE tumors have an excellent prognosis, whereas tumors with a large cell component or DLBCL or stage greater than IE have the greatest potential for a poor outcome.
CHARACTERIZATION POSITIVE CD20
Many distorted meshworks of CD21+ follicular dendritic cells corresponding to reactive folliclesNEGATIVE CD3
CD5BCL10 expression in normal and neoplastic lymphoid tissue. Nuclear localization in MALT lymphoma.
Ye H, Dogan A, Karran L, Willis TG, Chen L, Wlodarska I, Dyer MJ, Isaacson PG, Du MQ.
Department of Histopathology, Royal Free and University College Medical School, London, United Kingdom.
Am J Pathol 2000 Oct;157(4):1147-54 Abstract quote
BCL10 is an apoptotic regulatory molecule identified through its direct involvement in t(1;14)(p22;q32) of mucosa-associated lymphoid tissue (MALT) lymphoma.
We examined BCL10 protein expression in various normal tissues and B-cell lymphomas by immunohistochemistry of formalin-fixed and paraffin-embedded tissues using mouse BCL10 monoclonal antibodies. BCL10 protein was expressed in lymphoid tissue but not in 21 various other tissues with the exception of breast. In normal B-cell follicles, the protein was expressed abundantly in the germinal center B cells, moderately in the marginal zone, but only weakly in the mantle zone B cells.
Irrespective of their stage of B-cell maturation, BCL10 was predominantly expressed in the cytoplasm. In contrast, each of the four MALT lymphomas with t(1;14)(p22;q32) showed strong BCL10 expression in both the nucleus and cytoplasm. Twenty of 36 (55%) MALT lymphomas lacking the translocation exhibited BCL10 expression in both the nucleus and cytoplasm although at a much lower level, whereas the remaining 16 cases displayed only cytoplasmic BCL10. Unlike MALT lymphoma, both follicular and mantle cell lymphomas generally displayed BCL10 expression compatible to their normal cell counterparts.
Our results show differential expression of BCL10 protein among various B-cell populations of the B-cell follicle, indicating its importance in B-cell maturation. The subcellular localization of BCL10 was frequently altered in MALT lymphoma in comparison with its normal cell counterparts, suggesting that ectopic BCL10 expression may be important in the development of this type of tumor.
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