Case Reports. Extranodal Rosai-Dorfman Disease Associated With Increased Numbers of Immunoglobulin G4 Plasma Cells Involving the Colon
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1 Case Reports Extranodal Rosai-Dorfman Disease Associated With Increased Numbers of Immunoglobulin G4 Plasma Cells Involving the Colon Case Report With Literature Review Daniel B. Wimmer, DO; Jae Y. Ro, MD, PhD; Annisa Lewis, MD; Mary R. Schwartz, MD; Richard Caplan, MD; Peter Schwarz, MD; Alberto G. Ayala, MD A 49-year-old woman presented with fever, weight loss, night sweats, hematochezia, and acid reflux symptoms. Two large, firm cecal lesions were seen at colonoscopy, but multiple biopsies were inconclusive. The patient underwent a right hemicolectomy for a clinical diagnosis of colon cancer. Noncaseating granulomatous inflammation with background lymphocytes, plasma cells, and histiocytes exhibiting emperipolesis were identified. With these histologic features and immunoreactivity for S-100 protein and CD68, a diagnosis of Rosai-Dorfman disease was rendered. Other areas had storiform fibrosis admixed with numerous immunoglobulin G4 (IgG4) positive plasma cells. Although a few preliminary reports have noted an increased number of IgG4-positive plasma cells in Rosai- Dorfman disease, the relationship between these 2 conditions is unclear. To our knowledge, this is the first case report of a possible association of colonic Rosai- Dorfman disease with an increased number of IgG4- positive plasma cells. Reviews of colonic Rosai-Dorfman disease and IgG4-related sclerosis are presented to heighten awareness of this rare presentation. (Arch Pathol Lab Med. 2013;137: ; doi: /arpa CR) Rosai-Dorfman disease (RDD), also known as sinus histiocytosis with massive lymphadenopathy, is an uncommon disorder. Rosai-Dorfman disease most often manifests with bilaterally enlarged, painless cervical lymphadenopathy, fever, and leukocytosis. 1 3 The disease process is characterized by dilated lymph node sinuses filled with lymphocytes, plasma cells, and histiocytes. Many of these histiocytes classically exhibit emperipolesis of lymphocytes and plasma cells. The etiology of RDD remains unclear, although it has been regarded as a reactive inflammatory process. Immune deficiency and viral infection (eg, Epstein-Barr virus, parvovirus B19, and human herpesvirus 6) have also been postulated to play a role in the pathogenesis of RDD, although no definitive evidence to support any of these has been found. 1,4 6 Immunoglobulin (Ig) G4 related sclerosing disease is a recently described entity that occurs in a variety of anatomic sites and organ systems. It is characterized by storiform fibrosis with an intense IgG4-positive plasma cell infiltration. 7 9 We report a case of colonic RDD associated with increased numbers of IgG4-positive plasma cells and review the pertinent literature. REPORT OF A CASE A 49-year-old African-American woman presented with night sweats, fever, unintentional weight loss, and hematochezia for more than 1 year. She also complained of abdominal bloating, constipation, nausea, vomiting, and symptoms of acid reflux. The patient denied easy bruising. No lymphadenopathy was noted on physical examination. The patient underwent 2 colonoscopies and was found to have 2 unusual lesions in her cecum (Figure 1, A). Colonic biopsies from multiple sites showed a nonspecific mixed inflammatory infiltrate and areas of focal noncaseating granulomatous inflammation. No evidence of malignancy was found. Accepted for publication August 28, From the Departments of Pathology and Genomic Medicine (Drs Acid-fast bacilli, periodic acid Schiff, and Grocott methenamine Wimmer, Ro, Lewis, M. Schwartz, and Ayala), General Surgery (Dr silver stains were all negative for acid-fast bacilli or fungi. On the Caplan), and Gastroenterology (Dr P. Schwarz), The Methodist basis of a presumptive clinical diagnosis of colon cancer, the patient Hospital, Weill Medical College of Cornell University, Houston, underwent a right hemicolectomy. Texas. Operative findings included hard cecal masses with suspicious The authors have no relevant financial interest in the products or companies described in this article. mesenteric lymph node involvement. The liver had no visible or Reprints: Alberto G. Ayala, MD, Department of Pathology and palpable abnormalities. Frozen section diagnosis of the resected Genomic Medicine, The Methodist Hospital, 6565 Fannin St, M227, bowel was that of granulomatous inflammation with no malignancy. Houston, TX ( aayala@tmhs.org). Arch Pathol Lab Med Vol 137, July 2013 Colonic Rosai-Dorfman With IgG4 Plasma Cells Wimmer et al 999
2 Figure 1. Gross pathology of colonic mass. A. Endoscopic image of a large cecal mass protruding into the lumen. B. Gross image of the fungating cecal mass. Figure 2. A. Numerous histiocytes with extensive cytoplasmic emperipolesis (hematoxylin-eosin, 320). B. Histiocytes with extensive cytoplasmic emperipolesis and identifiable plasma cells (hematoxylin-eosin, 310). PATHOLOGIC FINDINGS Gross Pathology The segmental bowel resection included 23 cm of large bowel and 16 cm of ileum. There was an 8.4-cm, tan-red, fungating cecal mass that grossly extended to the muscularis propria (Figure 1, B). Less than 1 cm from this mass was a second 5.4-cm mass that circumferentially involved the ileocecal valve and did not grossly invade into the muscularis propria. Both lesions were firm, were externally tan-red, and had a tan-white cut surface. No hemorrhage or necrosis was seen. There was a firm 6-cm nodule in the pericolic fat that also had a tan-white firm cut surface. Microscopic Evaluation The cecal masses were extensively sampled. The mucosa over the masses was focally ulcerated and had chronic inflammation. Both lesions had xanthogranulomatous inflammation with numerous foamy histiocytes and extensive fibrosis extending into the muscularis propria. Numerous plasma cells and histiocytes were present and were focally admixed with eosinophils. There were numerous large histiocytes containing lymphocytes and plasma cells (ie, emperipolesis) (Figure 2, A and B). Additionally, dense storiform fibrosis and sclerosis were identified in the colonic wall in association with an extensive plasma cell infiltration (Figure 3). Flow cytometric studies were negative for malignancy, and no dysplasia or carcinoma was identified. The margins were free of lesional involvement. The nodule within the pericolic fat was an enlarged lymph node, with reactive germinal centers, architectural distortion, and inflammation similar to that of the colon, including numerous histiocytes with emperipolesis. An additional 20 benign lymph nodes were identified. Sixteen of 21 lymph nodes exhibited at least focal RDD involvement, with numerous histiocytes engulfing lymphocytes, plasma cells, and occasionally neutrophils in their cytoplasm. No malignancy was found. Immunohistochemistry The following immunohistochemical stains were performed: S-100 protein (prediluted, polyclonal; Ventana, 1000 Arch Pathol Lab Med Vol 137, July 2013 Colonic Rosai-Dorfman With IgG4 Plasma Cells Wimmer et al
3 Tucson, Arizona), CD1a (prediluted, clone MTB2; Ventana), CD68 (1:4000, clone KP1; DAKO, Carpinteria, California), IgG (1:40 000, polyclonal; DAKO), and IgG4 (1:200, monoclonal; Zymed, Carlsbad, California). The large histiocytes with emperipolesis were immunoreactive for both S-100 protein (Figure 4, A) and CD68 (Figure 4, B). These cells were negative for CD1a. These immunohistochemical findings, in conjunction with the morphologic features, are diagnostic for RDD of the colon and regional lymph nodes. Additionally, numerous background plasma cells were immunoreactive for IgG (up to 324 plasma cells/high-power field [HPF; 0.24 mm 2 ]) and IgG4 (up to 164 plasma cells/hpf) (Figure 4, C and D). An average of 122 IgG4-positive plasma cells/hpf was present in the 3 densest fields; this accounted for 46% to 51% of the IgG plasma cells. The high number and proportion of IgG4- positive plasma cells, along with the dense storiform fibrosis, was suggestive of a possible IgG4-related sclerosing lesion. Figure 3. Storiform fibrosis associated with an extensive plasmacytic infiltrate (hematoxylin-eosin, 310). Serology With light microscopic and immunohistochemical evidence of a possible IgG4-related sclerosing disease process, stored blood from postoperative day 1 was obtained to Figure 4. Immunohistochemistry of the cecal mass. A. Strong S-100 protein staining of histiocytes (310). B. CD68-positive histiocytes (340). C and D. IgG4 (C) and IgG (D) staining plasma cells (320). IgG4 accounted for 51% of the IgG-positive cells (164 IgG4, 324 IgG). Arch Pathol Lab Med Vol 137, July 2013 Colonic Rosai-Dorfman With IgG4 Plasma Cells Wimmer et al 1001
4 Colonic Rosai-Dorfman Disease Cases Case No. Source, y Age, y/sex Race Clinical Presentation 1 Nathwani et al, /F AA 6 months hematochezia; anemia 2 Long et al, /M White Fever, abdominal pain, constipation 3 Chen et al, /F AA Vomiting, stomach pain, low back pain 4 Lauwers et al, /M AA Right lower quadrant mass 5 Lauwers et al, /F White Abdominal pain 6 Lauwers et al, /F White Colonic mass 7 Lauwers et al, /F AA Incidental rectal mass on routine colonoscopy 8 Alatassi et al, /F NA Hematochezia and rectal mass 9 Shukla et al, /F NA Persistent ileocecal mass S/P chemotherapy 10 Anders et al, /F NA Hematochezia and constipation 11 Present study, /F AA Abdominal pain, bleeding per rectum, nausea, vomiting, weight changes Abbreviations: AA, African American; Hx, history; NA, not available; RDD, Rosai-Dorfman disease; S/P, status post. a Indicates a diagnosis made after slide review on previous tissue for a patient presenting with a rectal mass RDD lesion. determine the IgG and IgG4 serum levels and establish the IgG4:IgG ratio (approved by the Methodist Hospital Research Institute Institutional Review Board: IRB ). Duplicate testing on the serum demonstrated that the IgG4 subpopulation (33 and 37 mg/dl, respectively; reference range, 7 89 mg/dl) accounted for approximately 3% of the total IgG population (1040 and 1210 mg/dl, respectively; reference range, mg/dl). No preoperative serum was available for examination. COMMENT The pathogenesis of RDD is unclear. Immune deficiency, viral infection, and autoimmune mechanisms have all been proposed as possible etiologies of this disorder. 1,4 6 Classically, RDD primarily involves lymph nodes of the head and neck areas. 1 3 Definitive treatment for RDD has not yet been determined, and there is evidence that exclusive nodal involvement may not require therapy, as this manifestation often spontaneously remits. 2,10 13 Extranodal involvement was initially thought to be uncommon, but some reports suggest extranodal involvement occurs in up to 40% of RDD cases. 1,10,12 The most commonly involved extranodal sites include the skin, salivary gland, orbit, eyelid, and upper respiratory tract, but isolated cases have been reported in the colon. 1,10 16 Rosai-Dorfman disease with extranodal involvement, including colonic involvement, may require active intervention including surgical debulking, radiation therapy, or a combination of the two. 14 Gastrointestinal involvement represents less than 1% of extranodal presentations, and colonic involvement by RDD is an even rarer presentation, with only 10 cases previously reported in the English literature. 1,10 16 Based on the published cases, intestinal RDD appears to have a predilection for the ileocecal area and the distal colon. To the best of our knowledge, there are no previously reported cases of intestinal RDD proximal to the jejunum. Key clinical and pathologic features of the reported cases of colonic RDD, including our case, are summarized in the Table. These 11 patients ranged in age from 4 to 79, with a mean age of 44 years. Of the reported cases, there were 9 females and 2 males. Of the patients whose race was provided, 5 were African American and 3 were White. Four patients with colonic RDD, including our patient, had more than 1 lesion. Two cases, including ours, involved the cecum or ileocecum. 13 Two cases involved the appendix, 10 2 had lesions in the colon not otherwise specified, 10,14 1 in the descending colon, 11 2 in the sigmoid colon, and 3 in the rectum. 10,12,15 The presenting symptoms varied and included fever, hematochezia, abdominal pain, and an abdominal mass. A few cases were reported to be asymptomatic and had RDD discovered incidentally (ie, during a routine colonoscopy and appendectomy). Preoperative diagnoses included cancerous relapse, 13 sarcoidosis, 16 diverticulitis, 11 and probable colon cancer (present case). It is noteworthy that of the documented colonic RDD cases, none were recognized preoperatively. Patients with nodal RDD often develop a good response to therapy or even spontaneous remission. 1 However, patients with extranodal Rosai-Dorfman disease have been identified as having an increased risk of developing recurrent lesions and enduring a more aggressive clinical course. 16 Though the intestinal tract is one of the least commonly affected organ systems, approximately 20% of patients with intestinal manifestations of RDD ultimately succumb to complications from the disease. 10,15 Several investigators have discussed a possible association between RDD and IgG4-related sclerosing disease Immunoglobulin G4-related sclerosing disease is a recently described entity that may occur in a variety of anatomic sites. The mechanism of IgG4 sclerosis is not fully understood, nor is there a consensus on diagnostic criteria. 7 9,21 23 Some studies have even noted variability of 1002 Arch Pathol Lab Med Vol 137, July 2013 Colonic Rosai-Dorfman With IgG4 Plasma Cells Wimmer et al
5 Extended Preoperative Diagnosis Site of Involvement Other Clinical Data NA Multiple nodules within 25 cm from the NA anal verge Sigmoiditis and colonic diverticulitis Descending colon Hx of myelodysplasia. Widespread nodal and extranodal RDD developed and the patient died 2 years after surgery. Fibroblastic proliferation with mixed inflammatory cells without evidence of malignancy Colon with involvement of other pelvic organs A second debulking surgery was attempted but did not succeed in removing the entire lesion. The patient developed hydronephrosis from compression by the mass and subsequently had a nephrectomy. NA Appendix Cervical and mesenteric lymph nodes involved. NA Appendix Corneal RDD diagnosed 5 years previously. NA Colon Peritoneal involvement. NA Rectum NA NA Rectum, sigmoid colon, a abdominal, a Numerous previous abdominal surgeries. and pelvic mass a Recurrent Hodgkin lymphoma Ileum and cecum Remote Hx of Hodgkin lymphoma with relapse including the cervical and ileocecal lymph nodes and bone marrow. Possible sarcoidosis Sigmoid colon Remote Hx of mediastinal lymphadenopathy believed to be sarcoid. Presumptive colon cancer Cecum and ileocecal valve IgG4 manifestations among different organ systems. 7 Essential histologic features include storiform fibrosis and an IgG4-positive plasma cell infiltrate, although these findings are neither specific nor diagnostic for this entity. Several processes may elevate the number of IgG4-positive plasma cells; therefore, it is important to note that an absolute increase in IgG4-positive plasma cells alone is insufficient to diagnose IgG4-related disease. Proposed characteristic morphologic features include an increased number of IgG4-positive plasma cells (more than 50/HPF), an increase in the ratio of IgG4:IgG plasma cells of greater than 40%, and obliterative phlebitis. 7 9,21 23 There is often an associated eosinophilic and lymphoplasmacytic infiltrate. 7 9,21 23 Serum levels of immunoglobulin, including IgG4 and IgG, may be increased. 7 9,21 23 The sclerotic lesions can be severe and extremely damaging to the involved tissue. 9 Lymph node involvement may manifest as a Castleman-like disease. A dramatic response to steroid therapy remains the cornerstone to disease management. 7 9,21 23 Our case has several characteristic features of IgG4 sclerosing disease. 7,21 23 The colonic lesion had dense storiform fibrosis and sclerosis with inflammation, a rich lymphoplasmacytic infiltrate with a focal admixture of eosinophils, and up to 324 IgG plasma cells/hpf. Many of these plasma cell dense foci had a significant IgG4-positive plasma cell subpopulation (up to 164 IgG4-positive plasma cells/hpf), accounting for 46% to 51% of the IgG-positive plasma cells. No obliterative phlebitis was seen in our case, but the incidence of this finding is known to vary tremendously among different organ systems; one large study identifies its presence in 56% to 85% of diagnosed cases depending on the system involved. 7 The serum IgG4 subpopulation was well below the threshold typically regarded as abnormal. However, more than one-third of patients with IgG4-related disease may have a normal serum level. 7 9,21 23 Moreover, because the serum was collected postoperatively, this value may not be a true representation of the patient s IgG4 subpopulation before surgery. Since our patient s initial diagnosis of RDD with increased IgG4-positive plasma cells 2 years ago, she has developed several additional lesions, suggestive of a systemic disease process. Masses of the breast, buttock, mediastinum, and pleura have all been resected. Rosai-Dorfman disease and granulomatous inflammation similar to our initial case have been identified. Additionally, a dense lymphoplasmacytic infiltrate with storiform fibrosis and sclerosis also appears within the tissue. Rosai-Dorfman disease rarely presents with colonic lesions. It can clinically mimic cancer, and recognition of this entity thus has important implications for the appropriate clinical management of patients. When extensive histiocytic infiltration is seen in the colon, RDD should be considered. Immunohistochemical evaluation of S-100 protein and CD68 expression can confirm the diagnosis of RDD. There have been no previous reports of colonic RDD with increased numbers of IgG4-positive plasma cells. Our patient s recurrent, multifocal disease with some characteristic histologic findings (ie, significantly increased number and proportion of IgG4-positive plasma cells with stromal storiform fibrosis) suggests a possible relationship between colonic RDD and the increased number of IgG4-positive plasma cells. Although there are indications that a close relationship between RDD and IgG4 sclerosing inflammation may exist, a definitive link between RDD and IgG4 positivity has yet to be established. To the best of our knowledge, this is the first report of a possible association of colonic RDD and increased number of IgG4-positive plasma cells. References 1. Gaitonde S. Multifocal, extranodal sinus histiocytosis with massive lymphadenopathy: an overview. Arch Pathol Lab Med. 2007;131(7): Foucar E, Rosai J, Dorfman R. Sinus histiocytosis with massive lymphadenopathy (Rosai-Dorfman disease): review of the entity. Semin Diagn Pathol. 1990; 7(1): Arch Pathol Lab Med Vol 137, July 2013 Colonic Rosai-Dorfman With IgG4 Plasma Cells Wimmer et al 1003
6 3. Rosai J, Dorfman RF. Sinus histiocytosis with massive lymphadenopathy: a newly recognized benign clinicopathological entity. Arch Pathol. 1969;87(1): Levine PH, Jahan N, Murari M, Manak M, Jaffe ES. Detection of human herpesvirus 6 in tissues involved by sinus histiocytosis with massive lymphadenopathy (Rosai-Dorfman disease). J Infect Dis. 1992;166(2): Tsang WY, Yip TT, Chan JK. The Rosai-Dorfman disease histiocytes are not infected by Epstein-Barr virus. Histopathology. 1994;25(1): Mehraein Y, Wagner M, Remberger K, et al. Parvovirus B19 detected in Rosai-Dorfman disease in nodal and extranodal manifestations. J Clin Pathol. 2006;59(12): Zen Y, Nakanuma Y. IgG4-related disease: a cross-sectional study of 114 cases. Am J Surg Pathol. 2010;34(12): Kamisawa T, Okamoto A. IgG4-related sclerosing disease. World J Gastroenterol. 2008;14(25): Sato Y, Notohara K, Kojima M, Takata K, Masaki Y, Yoshino T. IgG4-related disease: historical overview and pathology of hematological disorders. Pathol Int. 2010;60(4): Lauwers GY, Perez-Atayde A, Dorfman RF, Rosai J. The digestive system manifestations of Rosai-Dorfman disease (sinus histiocytosis with massive lymphadenopathy): review of 11 cases. Hum Pathol. 2000;31(3): Long E, Lassalle S, Cheikh-Rouhou R, Hofman V, Lacour JP, Hofman P. Intestinal occlusion caused by Rosai-Dorfman disease mimicking colonic diverticulitis. Pathol Res Pract. 2007;203(4): Nathwani RA, Kenyon L, Kowalski T. Rosai-Dorfman disease of the colon. Gastrointest Endosc. 2008;68(1): Shukla D, Veillon DM, Abreo F, Cotelingam JD. Pathologic quiz case: a 55- year-old woman with a history of treated Hodgkin disease and a persistent abdominal mass: extranodal gastrointestinal Rosai-Dorfman disease. Arch Pathol Lab Med. 2003;127(11): Chen H, Sun J, Aftab L, Sands A. Extranodal Rosai-Dorfman disease involving colon a case report with review of the literature. N Am J Med Sci. 2010;3(3): Alatassi H, Ray MB, Galandiuk S, Sahoo S. Rosai-Dorfman disease of the gastrointestinal tract: report of a case and review of the literature. Int J Surg Pathol. 2006;14(1): Anders RA, Keith JN, Hart J. Rosai-Dorfman disease presenting in the gastrointestinal tract. Arch Pathol Lab Med. 2003;127(2):E74 E Kuo TT, Chen TC, Lee LY, Lu PH. IgG4-positive plasma cells in cutaneous Rosai-Dorfman disease: an additional immunohistochemical feature and possible relationship to IgG4-related sclerosing disease. J Cutan Pathol. 2009;36(10): Richter JT, Strange RG, Jr., Fisher SI, Miller DV, Delvecchio DM. Extranodal Rosai-Dorfman disease presenting as a cardiac mass in an adult: report of a unique case and lack of relationship to IgG4-related sclerosing lesions. Hum Pathol. 2009;41(2): Roberts SS, Attanoos RL. IgG4þ Rosai-Dorfman disease of the lung. Histopathology. 2010;56(5): Chen TD, Lee L. Rosai-Dorfman disease presenting in the parotid gland with features of IgG4-related sclerosing disease. Arch Otolaryngol Head Neck Surg. 2011;137(7): Dhall D, Suriawinata AA, Tang LH, Shia J, Klimstra DS. Use of immunohistochemistry for IgG4 in the distinction of autoimmune pancreatitis from peritumoral pancreatitis. Hum Pathol. 2010;41(5): Cheuk W, Chan JK. IgG4-related sclerosing disease: a critical appraisal of an evolving clinicopathologic entity. Adv Anat Pathol. 2010;17(5): Stone JH, Zen Y, Deshpande V. IgG4-related disease. N Engl J Med. 2012; 366(6): Arch Pathol Lab Med Vol 137, July 2013 Colonic Rosai-Dorfman With IgG4 Plasma Cells Wimmer et al
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