The Acute Vasculitis of Wegener's Granulomatosis in Renal Biopsies

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1 The Acute Vasculitis of Wegener's Granulomatosis in Renal Biopsies RICHARD. NOVAK, M.D., RICHARD G. CHRISTIANSEN, M.D., AND EWALD T. SORENSEN, M.D. The kidney biopsy specimens fromfivepatients with Wegener's Granulomatosis were reviewed in an attempt to characterize the early histological lesion when vasculitis was present. The vascular lesions were found mainly in interlobularsized arteries. The acute vascular lesions were sparse and focal, mainly localized to the intimal area, and with fibrinoid material and platelets constituting the early infiltrate. The electron microscopy and scanning electron microscopy of the involved areas further emphasized the presence of platelets in the early lesion, and accentuated endothelial alterations occurring along with the intimal infiltrate. Morphologic evidence of immune complex presence was not found. (Key words: Vasculitis; Renal biopsy; Wegener's granulomatosis; Scanning electron microscopy) Am J Clin Pathol 1982; 78: THE DIAGNOSIS O WEGENER'S GRANULO MATOSIS (WG), a difficult clinical diagnosis, is frequently made after its systemic involvement has resulted in renal abnormalities. In order to fulfill the usual criteria of WG 5,6 the patients in this study were selected because of the findings of acute vasculitis and/or focal necrotizing glomerulonephritis in renal biopsy specimens, in association with marked upper respiratory symptoms (rhinorrhea, sinusitis, or otitis media) and pulmonary findings on chest xray (Table 1). We report the early histologic changes of acute vasculitis in the kidney biopsy specimens from four of these five patients; one case only showed focal necrotizing glomerulonephritis, which is the other nonspecific finding in kidneys examined in patients with WG. The glomerular lesions have been previously studied. 9 None of these cases showed a granulomatous reaction within the kidney. The emphasis of the report is placed on the sites of localization and initial morphological changes leading to the fibrinoid necrosis seen on light microscopy, the corresponding electron microscopy, and, in one patient who died and was autopsied, the scanning electron microscopy of an artery showing an area of acute vasculitis. amiliarity with the histology of this acute vasculitis of WG in kidney biopsy specimens enables the pathologist to complete the last part of the diagnostic Received October 28, 1982; received revised manuscript and accepted for publication ebruary 19, Address reprint requests to Dr. Novak: Department of Pathology, Rockford School of Medicine, 1601 Parkview Avenue, Rockford, Illinois Departments of Pathology and Medicine, Rockford School of Medicine of the University of Illinois, Rockford, Illinois triad for the clinician, and, thus, enables the clinician to begin treatment with cyclophosphamides. Materials and Methods The kidney biopsy tissues were sectioned, and portions were immediately fixed for light microscopy in 10% buffered formalin; for immunofluorescent studies they were quick frozen in O.C.T. compound; and for electron microscopy, tissues were fixed in 2.5% gluteraldehyde and 0.1 M phosphate buffer. Direct immunofluorescent studies with antisera directed against IgG, IgA, IgM, complement (C3 component), fibrinogen, and albumin were performed. Tissues for scanning electron microscopy were postfixed in 1% phosphate buffered osmium tetroxide with the metal impregnation enhanced by thiocarbohydrazide per the OTOTO technic (osmium tetroxidethiocarbohydrazideosmium tetroxidethiocarbohydrazideosmium tetroxide). 10 Tissue contrast was further increased by uranyl acetate staining. The tissue was embedded in carbowax and ultraplaned with a glass knife. The carbowax was then dissolved in ethanol, and the tissue criticalpoint dried, mounted, and viewed. Results Table 1 contains a summary of the clinical and histologic findings in the five patients studied. In addition to the clinical findings listed, fatigue, malaise, anorexia, weight loss, and fever were common to all the patients at some time prior to the diagnosis. The average time between the onset of symptoms and diagnosis was 4.8 months, emphasizing the difficulty of diagnosis. The glomerular involvement was either focal segmental necrosis, and/or crescent formation. The immunofluorescent studies showed no characteristic pattern other than the fibrin found in the areas of segmental necrosis or within the areas of crescent formation. All five patients were treated with cyclophosphamides. Some were also treated with steroids. The focal areas of acute vasculitis involved mainly /82/0900/0367 $01.05 American Society of Clinical Pathologists 367 Downloaded from

2 368 NOVAK ET AL. Table 1. Summary of Clinical and Histologic indings A.J.C.P. September 1982 Patient l Clinical findings age sex onset to diagnosis rhinorrhea sinusitis otitis media hearing loss lung lesions (xray) arthralgia Histologic findings per cent glomeruli involved focal & segmental necrosis crescent formation renal vasculitis vessel involved present status 64 M 4 mo 33% arcuate 2yr 47 7 mo 80% 60% 40% 67 6 mo 50% interlobular 4 yr 4 yr 30 2 mo interlobular dead 3.5 wk 28 5 mo 90% 20% 80% interlobular dead 2 mo interlobular arteries. One case showed involvement of an arcuate artery branch. In these biopsy specimens, the areas of acute vasculitis were not common; and many sections had to be carefully reviewed to find a lesion. igure 1 shows a typical area of acute vasculitis located at the bifurcation of an interlobular artery. The lumen of the larger branch is almost completely obliterated due to the extensive deposition of fibrinoid material in the intimal area of the artery. This deposition of fibrinoid material in the intima was characteristic of the acute vasculitis, with only minimal extension of the fibrinoid material into the media of the artery wall. As also seen in igure 1, there is little evidence of an acute inflammatory cell infiltrate into the area of fibrinoid deposition. Enlarged endothelial cell nuclei could always be seen over the area of fibrinoid deposition, and definite breaks in the endothelial cell surface could not be seen in the light microscopy lesions. The corresponding transmission electron microscopy (ig. 2) of a typical lesion showed marked alteration of the endothelial cells, with loss of cytoplasmic organelles and areas of disruption of the endothelial surface, and/or wide interendothelial cell junctions. These findings were not apparent on light microscopy. Immediately below the endothelial surface there was a mixture of fibrin or fibrinlike strands and platelets that were either partially or completely degranulated. Smooth muscle cells adjacent to the intimal area showed nuclei with irregular outlines or membranes, and within the cytoplasm, dilated prominent endoplasmic reticulum similar to the changes Heath described. 8 The prominence of platelets intermixed with the fibrin was a very consistent finding on electron microscopy, and is a finding not appreciated in light microscopy sections of acute vasculitis with fibrinoid change. igures 3 and 4 demonstrate an area of acute vasculitis seen on scanning electron microscopy and comparable with those described above on light and transmission electron microscopy. The endothelial cells at the site of the lesion appear to be enlarged or swollen, and have become widely separated from the media of the artery. In the prominent intimal space present between the endothelial cells and the media, numerous platelets were very apparent. This further emphasized their very active participation at the site of fibrinoid necrosis, but was not apparent in the light microscopy sections. The remainder of the circumference of the artery was not involved, and the endothelium was closely approximated to the media of the vessel, as noted on the left in igure 3. IG. 1 (upper). Bifurcation of an artery. The vessel lumen (L), endothelium and wall on left are uninvolved, the intimal (i) area on the right is filled with amorphous clumps of fibrinoid and other material. Hematoxylin and eosin (X200). IG. 2 (lower, left). Electron micrograph. The lumen (L) shows an interrupted endothelial surface, and platelets (p) and fibrin (f) are now in the intimal area (X2,000). IG. 3 (lower, right). Scanning electron microscopy. Lumen (L). The endothelial surface (e) is widely separated from the media (m). A leukocyte (w) is noted on the endothelial surface, and platelets (p) are noted beneath the endothelium (XI,125). Downloaded from

3 Vol. 78 No. 3 BRIE SCIENTIIC REPORTS 369 w X Downloaded from

4 NOVAK ET AL. 370 A.J.C.P. September 1982 IG. 4. Higher power scanning electron microscopy. The separation of the endothelium (e) and media (m) further accentuated with platelets (p) very apparent (X3,750). Discussion Over the years, investigations into the morphology of acute vasculitis have tended to stress the origin and terminology for the eosinophilic or fibrinoid infiltrate in the affected vessel walls.7 It seems clear that the fibrinoid material is fibrin in various states of polymerization, and now the role of the other components of the infiltrate are receiving more attention. 3,8 In this review of WG involvement of the kidney, vessels with acute lesions were mainly of the interlobular size, one of arcuate artery size. The sparsity and focal nature of the early vascular lesions is important to remember, and as many sections as possible must be reviewed to rule out the presence of vasculitis, if the glomerular changes (focal segmental necrotizing glomerulonephritis) and clinical findings are consistent with WG. Appel and associates made the same observation, and even suggested open biopsy, if WG is a serious diagnostic possibility.1 They also pointed out that there may be renal involvement without any clinical or laboratory findings of renal disease. WG is considered by most pathologists to be an im Downloaded from mune disorder, possibly a hypersensitivity reaction.4,5 Immune complexes, however, are rarely demonstrated at the areas of damage, either glomerular or vascular, and have not been demonstrated in this review.4 Experimentally, however, immune complexes can produce vasculitis, but are cleared rapidly from the areas of involvement.2 Whatever the agent, the early focal involvement of endothelium is dramatic. Whether the etiologic agent acts directly or via an intermediary mechanism is not apparent from the morphologic changes. What is apparent is the effect on the permeability of the endothelial surface and the resultant accumulation of plasma, fibrin, and platelets in the intimal area. Platelets are very actively involved early in this process, and vasoactive amines released from the platelets probably contribute considerably to this increased endothelial permeability. auci 5 proposes a mechanism whereby circulating immune complexes, via an IgEmediated reaction, activate both basophils and platelets and result in a release of their vasoactive amines. This, in turn, results in the early findings of vasculitis. As stated above, no immune complexes were demonstrated in this study, and the same IgE mediated reaction at

5 vol. 78.No. 3 BRIE SCIENTIIC REPORTS 37 J the site of endothelial damage and fibrinoid necrosis in the vessel wall could be initiated by some other etiologic agent, or specifically sensitized basophils and/or platelets. The accompanying passage of plasma and subsequent formation of fibrin or fibrinoid give the typical appearance of the light microscopy lesion. The electron and scanning microscopy in this review accentuate the extensive participation of platelets in this early lesion. The pathologist must be alert to the fact that these lesions can involve only a portion of the circumference of an arterial wall, are often found at a bifurcation of a vessel, and will be very sparse in a tissue sample. In addition, the fibrinoid necrosis may be limited mainly to the intimal area of the vessel, and, in the acute renal lesion, very little polymorphonuclear reaction within the wall will be noticed. inding the lesion in a renal biopsy specimen is of considerable help to the clinician, and will enable him to proceed more confidently with proper treatment. Acknowledgment. The author thanks Theodore S. Ingrassia III for his technical assistance in performing the scanning electron microscopy. References 1. Apel GB, Gee B, Kashgarian M, Hayslett JP: Wegener's granulomatosis clinicalpathologic correlations and longterm course. Am J Kidney Dis 1981; 1: Cochrane CG: Studies on the localization of circulating antigenantibody complexes and other macromolecules in vessels. J Exp Med 1963; 118: Donald KJ, Edwards RL, McEvoy JDS: An ultrastructural study of the pathogenesis of tissue injury in limited Wegener's Granulomatosis. Pathology 1976; 8: auci AS, Haynes B, Katz P: The spectrum of vasculitis. Ann Intern Med 1978; 89: auci AS, Wolff SM: Wegener's granulomatosis and related diseases. DM 1977; 23: auci AS, Wolff SM: Wegener's granulomatosis: studies in eighteen patients and a review of the literature. Medicine 1973; 52: Gitlan D, Craig JM, Janeway CA: Studies on the nature of fibrinoid in the collagen diseases. Am J Pathol 1957; 33: Heath D, Smith P: The electron microscopy of fibrinoid necrosis in pulmonary arteries. Thorax 1978; 33: Horn RG, auci AS, Rosenthal AS, Wolff SM: Renal biopsy in Wegener's granulomatosis. Am J Pathol 1974; 74: Malick LE, Wilson RB: Evaluation of a modified technique for SEM examination of vertebrate specimens without evaporated metal layers. Proceedings of the Scanning Electron Microscope Symposium 1975; Part 1: Downloaded from

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