Immunoglobulin G4 related Disease in Genitourinary Organs: An Emerging Fibroinflammatory Entity Often Misdiagnosed Preoperatively as Cancer
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1 EUROPEAN UROLOGY 64 (2013) available at journal homepage: Platinum Opinion Editorial Immunoglobulin G4 related Disease in Genitourinary Organs: An Emerging Fibroinflammatory Entity Often Misdiagnosed Preoperatively as Cancer Rodolfo Montironi a,y, *, Marina Scarpelli a,y, Liang Cheng b, Antonio Lopez-Beltran c, Maurizio Burattini d, Ziya Kirkali e, Francesco Montorsi f a Section of Pathological Anatomy, Polytechnic University of the Marche Region, School of Medicine, United Hospitals, Ancona, Italy; b Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, IN, USA; c Department of Surgery, Cordoba University Medical School, Cordoba, Spain; d Unit of Internal Medicine, Carlo Urbani Hospital, Jesi, Italy; e Departments of Urology, School of Medicine, Dokuz Eylül University, Izmir, Turkey; f Department of Urology, University Vita-Salute, Scientific Institute H San Raffaele, Milan, Italy 1. What is immunoglobulin G4? [(Fig._1)TD$FIG] Immunoglobulin G4 (IgG4) is the least common of the four subclasses of immunoglobulin G (IgG), namely IgG1, IgG2, IgG3, and IgG4, normally constituting only 3% to 6% of the entire IgG fraction. The major differences among the subclasses lie in the composition and structure of the hinge region that has significant effects on the antigen binding and effector functions of the immunoglobulin molecules, resulting in different functional characteristics of each IgG subclass. For instance, IgG4, in contrast to the other IgG subclasses, does not activate complement and has a low affinity for target antigens. IgG4 is a T-helper 2 (Th2) cell-dependent isotype. Despite uncertainties about its normal function, IgG4 seems to play a significant role in allergic reactions, such as atopic eczema, bronchial asthma, and bullous skin lesions [1]. IgG4 has not attracted the attention of pathologists and clinicians until the recent recognition of the syndrome of IgG4-related disease (IgG4-RD), a fibroinflammatory condition with a marked propensity to present as mass-forming lesions [2]. 2. Pathogenic mechanisms in immunoglobulin G4 related disease Autoimmunity and infectious agents are potential immunologic triggers in IgG4-RD. Interleukins 4, 5, 10, and 13 and Fig. 1 Imaging features (magnetic resonance) of a bladder lesion originally considered to be neoplastic. y These authors contributed equally to this work. * Corresponding author. Pathological Anatomy, Polytechnic University of the Marche Region, School of Medicine, United Hospitals, Via Conca 71, I Torrette, Ancona, Italy. Tel ; Fax: address: r.montironi@univpm.it (R. Montironi) /$ see back matter # 2012 European Association of Urology. Published by Elsevier B.V. All rights reserved.
2 [(Fig._2)TD$IG] 866 EUROPEAN UROLOGY 64 (2013) Fig. 2 Morphologic and immunohistochemical features of immunoglobulin G4 (IgG4) related disease: (A) cellular fibrosis with storiform pattern, (B) obliterative phlebitis, (C) dense lymphoplasmacytic infiltrate, and (D) IgG4+ plasma cells. transforming growth factor b are overexpressed through an immune reaction in which Th2 cells predominate, followed by activation of regulatory T cells. These cytokines contribute to the eosinophilia, elevated serum IgG4 and immunoglobulin E concentrations, and fibrosis that are characteristic of IgG4-RD. tion by inflammatory cells results in The inflammatory-cell infiltrate leads progression of Massive infiltraorgan damage. to tumefactive [(Fig._3)TD$IG] Fig. 3 Idiopathic retroperitoneal fibrosis involving (A) the kidney and (B) tubulointerstitial nephritis with an inflammatory infiltrate, fibrosis, and tubular atrophy.
3 EUROPEAN UROLOGY 64 (2013) Table 1 Body sites affected by immunoglobulin G4 related disease Body site Pancreas Bile duct Gall bladder Liver Salivary glands Lacrimal glands and orbit Retroperitoneum and mesentery Cardiovascular/aorta Mediastinum Kidney and ureter Thyroid Breast Lung Central nervous system Prostate Lymph node Clinicopathologic features Lymphoplasmacytic sclerosing pancreatitis (type 1 AIP) and idiopathic duct centric chronic pancreatitis (type 2 AIP) Sclerosing cholangitis Acalculous sclerosing cholecystitis Sclerosing cholangitis involving intrahepatic ducts, inflammatory pseudotumor, portal inflammation with or without interface hepatitis, portal sclerosis, large bile duct obstruction, lobular hepatitis, canalicular cholestasis Chronic sclerosing sialadenitis (Küttner tumor), Mikulicz disease Chronic sclerosing dacryoadenitis, inflammatory pseudotumor Retroperitoneal fibrosis, sclerosing mesenteritis Inflammatory abdominal aortic aneurysm Sclerosing mediastinitis Tubulointerstitial nephritis, membranous glomerulopathy, inflammatory pseudotumor Hypothyroidism, Riedel thyroiditis Sclerosing mastitis Inflammatory pseudotumor, interstitial pneumonia Hypophysitis, sclerosing pachymeningitis Prostatitis Lymphadenopathy with Castleman disease-like features, follicular hyperplasia, interfollicular expansion by plasma cells and immunoblasts AIP = autoimmune pancreatitis. [(Fig._4)TD$FIG] Fig. 4 (A) Radical nephrectomy specimen with hydronephrosis and proximal part of the ureter embedded in a mass originally considered to be cancer of the ureter. (B) Histologically, the mass is composed of cellular fibrosis and (C) dense lymphoplasmacytic infiltrate.
4 868 [(Fig._5)TD$FIG] EUROPEAN UROLOGY 64 (2013) Fig. 5 (A) Whole-mount section of a bladder specimen involved by immunoglobulin G4 (IgG4) related disease. (B) Cellular fibrosis with a dense lymphoplasmacytic infiltrate involves the mucosa extending to (C) the perivesical tissue, and (D) including IgG4+ plasma cells. enlargement of the affected sites and to organ dysfunction. Epithelial damage may result from tissue inflammation and immune-complex deposition. 3. Imaging features and serologic findings The imaging features are generally nonspecific and do not permit reliable distinctions between IgG4-RD and cancer [3] (Fig. 1). Lymph node enlargement, as evidenced by imaging studies, is often associated with IgG4-RD and may be multifocal, with mediastinal, abdominal, and axillary lymph nodes being involved most commonly [4]. The clinical differential diagnosis in such cases with lymphadenopathy includes lymphoma, multicentric Castleman disease, or metastatic malignant tumor. A raised serum IgG4 level is not mandatory for the diagnosis but may be of valuable assistance. Serum IgG4 titer often correlates with disease activity and the number of involved organs. In addition, high serum levels of polyclonal g-globulins often occur [5]. 4. Treatment When vital organs are involved, aggressive treatment is needed because IgG4-RD can lead to organ dysfunction and failure [3]. Glucocorticoids, typically the first line of therapy, appear to be effective (initially, at least) in the majority of patients with IgG4-RD. Although IgG4 concentrations become lower with glucocorticoid treatment in the great majority of patients in whom they are elevated at baseline, they remain above normal values in most patients. The decision to give steroid therapy, however, requires a precise diagnosis, a major determinant of treatment responsiveness being the degree of fibrosis within the affected organs. The possibility of biopsy-based diagnosis relies on the combination of the three major morphologic features described in the next section of this article. Unfortunately, the presence of all these specific features, especially in small fragments, is seen only in a minority of cases. The presence of abundant IgG4+ plasma cells and a high IgG4/IgG ratio are important for tissue diagnosis [6,7]. For patients with recurrent or refractory disease, B-cell depletion with rituximab appears to be a useful approach [8]. Swift clinical responses have been observed. In patients treated with rituximab, IgG4 serum concentrations decline sharply. This decline is associated with clinical improvement within weeks. In view of the high success rate of corticosteroid therapy in IgG4-RD, it can be anticipated that in the future, the only patients who will be treated surgically will be those who are
5 [(Fig._6)TD$FIG] EUROPEAN UROLOGY 64 (2013) Fig. 6 (A) Enlarged lymph node whose histology is that of type I immunoglobulin G4 (IgG4) related lymphadenopathy, that is, (B,C) Castleman s diseaselike morphology, (D) including IgG4+ plasma cells. refractory to steroids or immunoregulatory drugs and/or in whom carcinoma continues to be suspected. 5. The three major morphologic features Cellular fibrosis with storiform pattern is a special type of fibrosis characterized by fibroblast and myofibroblast proliferation with delicate collagen bands forming short fascicles with a storiform pattern or herringbone pattern (Fig. 2A), intermixed with inflammatory cells [6,7]. Obliterative phlebitis, i.e., the lymphoplasmacytic infiltration that involves veins (phlebitis), usually begins at the periphery of venous walls, spreading through the wall as the inflammation progresses (Fig. 2B). The fully developed lesion, the obliterative phlebitis, is characterized by organized obstruction of veins with wall destruction due to dense lymphoplasmacytic infiltration [6,7]. Dense lymphoplasmacytic infiltrate is characterized by diffuse but sometimes focal infiltration of small lymphocytes and plasma cells (Fig. 2C). Eosinophils are often observed. The most relevant and important feature is the increased number of IgG4+ plasma cells (Fig. 2D). Analysis of IgG4 immunostaining helps to distinguish IgG4-RD from other conditions. A variety of cut-off points, ranging from >10 to >50 IgG4+ plasma cells per high-power field, has been proposed. The ratio of IgG4-bearing plasma cells to IgG-bearing plasma cells further assists in confirming the diagnosis of IgG4-RD: A ratio >50% is very suggestive of the diagnosis. IgG4-RD is more difficult to diagnose in the late phase of organ involvement, when fewer plasma cells are present and fibrosis may predominate in some tissues. The pattern of fibrosis and the ratio of IgG4 to total IgG provide crucial information in this context [6,7]. 6. Organ involvement IgG4-RD has been described in almost every organ system [3]: the pancreatobiliary tract, liver, salivary glands, nasopharynx, bone marrow, lacrimal gland, extraocular muscles and retrobulbar space, lungs, lymph nodes, meninges, aorta and arteries, skin, breast, thyroid gland, and pericardium, as well as in genitourinary organs (Table 1). Many medical conditions that have long been viewed as conditions confined to single organs are part of the spectrum of IgG4-RD. Mikulicz syndrome, Küttner tumor, and Riedel thyroiditis names embedded in the medical literature for more than a century in some cases may now be replaced by designations that describe a key pathologic feature and perhaps provide more insight into the pathophysiology.
6 870 EUROPEAN UROLOGY 64 (2013) Lymphadenopathy may also develop following an established diagnosis of extranodal IgG4-RD or may be the initial presenting manifestation with subsequent discovery of systemic IgG4-RD. The enlarged lymph nodes may be asymptomatic or may give rise to a mass effect in various body sites. Five histologic patterns of IgG4-related lymphadenopathy have been described [4]. IgG4-RD increases the risk of developing lymphoma. Cases of pulmonary adenocarcinoma, salivary duct carcinoma, urothelial carcinoma in situ, and gastrointestinal clear cell sarcoma in association with IgG4-RD have been reported [6] Immunoglobulin G4 related disease involving genitourinary organs A subset of idiopathic retroperitoneal fibrosis cases could be classified in the IgG4-related sclerosing disease spectrum. Idiopathic retroperitoneal fibrosis may extend to involve the kidney (Fig. 3A) and ureter. IgG4-RD may involve the kidneys, leading to disturbances in renal function [9,10]. Radiologic studies may demonstrate the presence of poorly circumscribed nodular masses in the kidneys, often necessitating the exclusion of malignancy. The commonest findings on biopsy or nephrectomy are tubulointerstitial nephritis with an IgG4+, plasma cell-rich inflammatory infiltrate, fibrosis, and tubular atrophy (Fig. 3B). Using electron microscopy, IgG4 electron-dense deposits have been demonstrated in the peritubular basement membrane. The renal glomeruli are usually uninvolved, but few cases with concurrent membranous nephropathy have been recorded. Tubulointerstitial nephritis is steroid responsive, whereas the response of membranous glomerulonephritis can be variable. Very recently, our group had the chance to examine histologically a radical nephrectomy specimen with an 8-cm segment of ureter. The proximal part of the ureter was embedded in a hard and white mass that measured 5 cm at its widest diameter (Fig. 4A 4C). The clinical diagnosis was cancer involving the ureter with hydronephrosis. The lesion showed the typical histologic and immunohistochemical features of IgG4-RD. The process involved the mucosa, the muscularis propria, and the periureteral tissue. Three cases of IgG4-RD involving the ureter have been reported by Kim et al. [11]. A case report with a literature review of IgG4- related ureteritis misdiagnosed as ureteral cancer preoperatively has been published by Joo et al. [12]. IgG4-related chronic sclerosing pyelitis has also been reported. Concerning the bladder, our group has recently examined a partial cystectomy specimen with a whitish and hard mass measuring 6 cm at its widest diameter. The specimen was from a man with a clinical diagnosis of locally advanced bladder cancer. Histologically, the lesion showed the three major features of IgG4-RD, including a discrete number of eosinophils. The lesion involved the whole thickness of the bladder from the mucosa to the perivesical tissue (Fig. 5A 5D). There was an associated regional lymphadenopathy whose histology was that of IgG4-related lymphadenopathy (Type I, Castleman disease-like morphology) (Fig. 6A 6D). The patient also had high serum levels of polyclonal g-globulins (Fig. 7A). Glucocorticoid treatment induced a dramatic improvement compared with the original clinical presentation, including regression of the residual bladder mass, disappearance of the lymphadenopathy, and normal level of serum g-globulins (Fig. 7B). A similar case was observed by Jae Y. Ro (pers. comm.). IgG4-related prostatitis has recently been reported in patients with and without autoimmune pancreatitis [13]. Patients showed lower urinary tract symptoms, and prostate enlargement was evident on digital rectal examination. The symptoms and radiologic findings improved after steroid therapy. Histologically, the prostate showed dense infiltration of IgG4+ plasma cells and lymphocytes, obliterative phlebitis, and gland atrophy with dense fibrosis. IgG4-RD has also been observed in the seminal vesicles. Urethral caruncle is a benign inflammatory and fibrous polypoid urethral mass of unclear etiology. Using immunohistochemical markers, it appears unrelated to the viral infections that result in tumor formation and other mucosal abnormalities of various body sites. Abnormal expression of anaplastic lymphoma kinase protein, as seen in inflammatory myofibroblastic tumors, is absent. Increased numbers of IgG4+ plasma cells in a subset of lesions raise the possibility that some cases may be related to the autoimmune phenomena of IgG4-RD [14,15]. [(Fig._7)TD$FIG] Fig. 7 (A) High serum levels of polyclonal g-globulins (at arrow). (B) Normal level of serum g-globulins following glucocorticoid treatment (at arrow).
7 [(Fig._8)TD$FIG] EUROPEAN UROLOGY 64 (2013) Fig. 8 (A) Paratesticular fibrous pseudotumor. (B) Whole-mount section of the paratesticular fibrous pseudotumor showing the uninvolved testis. (C) The paratesticular lesions exhibiting cellular fibrosis. Paratesticular fibrous pseudotumor is a rare, benign condition of unknown etiology characterized by solitary or multiple intrascrotal nodules composed of dense fibrous tissue with a variable, sometimes sparse, inflammatory infiltrate (Fig. 8A 8C). Based on certain similarities to other fibroinflammatory disorders characterized by infiltrates of IgG4-expressing plasma cells, the plasma cell distribution and immunoglobulin isotypes in three cases of paratesticular fibrous and inflammatory pseudotumor were investigated in a recent study. All three cases showed a high number of IgG4+ plasma cells with an IgG4 IgG ratio of 44 48%. This finding indicates that paratesticular fibrous pseudotumor might belong to the growing list of conditions associated with IgG4-RD [16,17]. 7. Conclusions IgG4-RD, a multiorgan system disease that has been recognized in the last 10 yr, is a fibroinflammatory condition with a marked propensity to present as massforming lesions [2,18], characterized by a dense lymphoplasmacytic infiltrate, the presence of abundant IgG4+ plasma cells, frequent elevation of serum IgG4 levels, and a dramatic initial response to glucocorticoid. Correct preoperative identification is crucial to avoid unnecessary major surgical in genitourinary and nongenitourinary organs and initiate corticosteroid therapy. Conflicts of interest: The authors have nothing to disclose.
8 872 EUROPEAN UROLOGY 64 (2013) References [11] Kim SA, Lee SR, Huh J, Shen SS, Ro JY. IgG4-associated inflammatory pseudotumor of ureter: clinicopathologic and immunohistochemi- [1] Tsuboi H, Matsuo N, Iizuka M, et al. Analysis of IgG4 class switchrelated molecules in IgG4-related disease. Arthritis Res Ther 2012;14:R171. [2] Deshpande V, Zen Y, Chan JK, et al. Consensus statement on the cal study of 3 cases. Hum Pathol 2011;42: [12] Joo M, Chang SH, Kim H, Lee KC, Ro JY. Idiopathic segmental ureteritis, misdiagnosed as ureteral cancer preoperatively: a case report with literature review. Pathol Int 2010;60: pathology of IgG4-related disease. Mod Pathol 2012;25: [13] Hart PA, Smyrk TC, Chari ST. IgG4-related prostatitis: a rare cause of [3] Stone JH, Zen Y, Deshpande V. IgG4-related disease. N Engl J Med steroid-responsive obstructive urinary symptoms. Int J Urol 2013; 2012;366: [4] Sato Y, Yoshino T. IgG4-related lymphadenopathy. Int J Rheumatol 2012: [5] Kawa S, Ito T, Watanabe T, et al. The utility of serum IgG4 concentrations as a biomarker. Int J Rheumatol 2012: dx.doi.org/ /2012/ [6] Hirabayashi K, Zamboni G. IgG4-related disease. Pathologica 2012;104: [7] Deshpande V. The pathology of IgG4-related disease: critical issues and challenges. Semin Diagn Pathol 2012;29: : [14] Choi JW, Kim SY, Moon KC, Cho JY, Kim SH. Immunoglobulin g4related sclerosing disease involving the urethra: case report. Korean J Radiol 2012;13: [15] Williamson SR, Scarpelli M, Lopez-Beltran A, Montironi R, Conces MR, Cheng L. Urethral caruncle: a lesion related to IgG4-associated sclerosing disease? J Clin Pathol 2013;66: [16] Bo smu ller H, von Weyhern CH, Adam P, Alibegovic V, Mikuz G, Fend F. Paratesticular fibrous pseudotumor an IgG4-related disorder? Virchows Arch 2011;458: [8] Khosroshahi A, Carruthers MN, Deshpande V, Unizony S, Bloch DB, [17] Hart PA, Moyer AM, Yi ES, Hogan MC, Pearson RK, Chari ST. Stone JH. Rituximab for the treatment of IgG4-related disease: IgG4-related paratesticular pseudotumor in a patient with autoim- lessons from 10 consecutive patients. Medicine (Baltimore) mune pancreatitis and retroperitoneal fibrosis: an extrapancreatic 2012;91: manifestation of IgG4-related disease. Hum Pathol 2012;43: [9] Cornell LD. IgG4-related kidney disease. Semin Diagn Pathol 2012;29: [18] Clevenger JA, Wang M, Maclennan GT, Montironi R, Lopez-Beltran [10] Alkhasawneh AN, Allan RW. IgG4 inflammatory pseudotumor of A, Cheng L. Evidence for clonal fibroblast proliferation and autoim- the kidney. Case Rep Urol 2012: mune process in idiopathic retroperitoneal fibrosis. Hum Pathol 2012/ ;43:
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