Pulmonary Vascular Disease in Systemic Lupus Erythematosus

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1 Pulmonary Vascular Disease in Systemic Lupus Erythematosus A. OLUSEGUN FAYEMI, M.D.* Department of Pathology, The Mount Sinai School of Medicine of the City University of New York, New York, New York 129 ABSTRACT Fayemi, A. Olusegun: Pulmonary vascular disease in systemic lupus erythematosus. Am J Clin Pathol 65: 28-29,1976. The pulmonary vascular changes in systemic lupus erythematosus (SLE) have been investigated from 2 autopsies performed at the Mount Sinai Hospital from 196 to Acute lesions included fibrinoid necrosis and vasculitis. Chronic lesions consisted of intimal fibrosis, medial hypertrophy, alteration of elastic laminae, periadventitial fibrosis, and, in one case, aneurysmal dilatation. These changes were found variously in arterioles, arteries and veins. The fibrotic and occlusive vascular lesions may account for the syndrome of "unexplained breathlessness" that occurs in SLE. These lesions may progress in certain individuals to overt pulmonary hypertension; the concept of coexisting primary pulmonary hypertension and SLE should be re-examined. (Key words: Systemic lupus erythematosus; Pulmonary vascular disease.) PULMONARY INVOLVEMENT in systemic lupus erythematosus (SLE) is well known, and a variety of pathologic lesions have been described. Although these lesions are nonspecific they may be frequently seen in patients with SLE. Pleurisy, interstitial pneumonitis, atelectasis, and recurrent bronchopneumonia have been well described. 6-13,16 The deposidon of hematoxylin bodies within the pulmonary parenchyma is specific. 12 Insufficient emphasis has been placed on the pulmonary vascular changes in this disease. In a study of the pulmonary blood vessels in 2 autopsied cases of SLE we have found a variety of pulmonary vascular lesions, some previously undescribed, and we have attempted to correlate these Received October 2, 197; received revised manuscript September 29, 1975; accepted for publication September 29, * Present address: Holyname Hospital, Department of Pathology, Teaneck, New Jersey (Send reprint requests to Dr. Fayemi at this address.) morphologic alterations with certain clinical manifestations. Materials and Methods Twenty patients with unequivocal SLE were autopsied at the Mount Sinai Hospital in the ten-year period from 196 to The diagnosis had been confirmed by the typical clinical and laboratory findings. The LE phenomenon, and/or antinuclear antibodies, had been documented in all cases. Characteristic skin lesions had been observed in 19 cases. The clinical records were reviewed and certain features were critically evaluated: mode of presentation of disease, time of onset and symptoms of respiratory involvement, duration of disease, and cause of death. Histologic material, generally including at least one section from each pulmonary lobe, was studied after staining with hema- 28 Downloaded from on 21 February 218

2 March 1976 PULMONARY VASCULAR DISEASE IN SLE 285 Table 1. Frequencies of Pulmonary Vascular Lesions in 2 Cases of Systemic Lupus Erythematosus Arterioles Muscular Arteries Elastic Arteries Veins Fibrinoid necrosis Vasculitis Perivascular mucinous edema Periadventitial fibrosis Intimal thickening Medial hypertrophy Alteration of elastic laminae Thrombosis toxylin and eosin, elastica-van Gieson, and, in many instances, Masson's trichrome. Results Clinical Studies The patients, all women, ranged in age from 16 to 67 years, with an average of 37 years. The duration of survival from diagnosis to death was one month to 2 years, with an average of 6'/ years. Most patients manifested polyarthritis, fever, and typical butterfly rash when first seen. The laboratory findings invariably included positive LE cell preparations and positive antinuclear antibodies. Most patients received adrenocortical steroids, for various periods. In a few cases azathioprine and cyclophosphamide had been given. Renal failure and congestive heart failure, when they occurred, were treated in the standard ways. Death was due to a variety of reasons: eight patients developed terminal renal failure; in six, hypertension was a clinical problem. Three patients died of septicemia. Other causes of death included arteriosclerotic cardiovascular disease with or widiout myocardial infarction, and acute myocardial infarction due to coronary arteritis. In one case an aneurysmal intrahepatic artery ruptured, with intrahepatic bleeding. Diffuse small-vessel thrombosis and pulmonary infarction caused the deaths of two patients. Metabolic derangements were the causes of death in two other patients. Respiratory signs and symptoms, prominent in six patients, were related to pleurisy and pleural effusion, bronchopneumonia, atelectasis, and pulmonary infarction. In one case moderate to severe dyspnea had been a clinical problem for many years prior to death without evidence for cardiac, respiratory or renal disease. Autopsy in that case disclosed pulmonary vasculitis, fibrocellular intimal thickening of elastic arteries, muscular arteries with thickened walls and narrow lumina, and chronic interstitial inflammation and fibrosis, with organized pulmonary emboli and foci of pulmonary infarction. Pathology The pulmonary vasculature was involved by both acute and chronic lesions of varying severity in 8 of the 2 cases studied. Thus, in 12 padents no significant vascular change was demonstrable, although other pulmonary parenchymal lesions were present. Table 1 summarizes these vascular alterations. Arterioles. Arteriolar fibrinoid necrosis with severe intimal thickening (Fig. 1) was seen in three cases. In a few cases, arterialization of arterioles was prominent. Muscular Arteries. Muscular arteries were most often and most severely affected. Fibrinoid necrosis (Fig. 2) and vasculitis were common. The fibrinoid necrosis Downloaded from on 21 February 218

3 286 FAYEMI Downloaded from on 21 February 218 AJ.C.P. Vol. 65

4 March 1976 PULMONARY VASCULAR DISEASE IN SLE 287 FIG. 1 (upper, left). Pulmonary arteriole, showing cellular proliferation, thickened wall, and luminal narrowing. Hematoxylin and eosin. x8. FIG. 2 (upper, right). Focal fibrinoid necrosis in the wall of a muscular artery. The lumen is narrowed. Hematoxylin and eosin. x8. FIG. 3 (lower, left). Photomicrograph of muscular artery, showing luminal occlusion by fibrocollagenous intimal thickening. A small recanalized lumen is present. Elastica-van Gieson. x8. FIG. (lower, right). Muscular artery, showing intimal thickening, composed predominantly of elastic tissue. The media is mildly hypertrophic. Elastica-van Gieson. X8. < involved focal areas of the entire wall with fragmentation of the cellular elements and replacement by bright eosinophilic material. Eight cases showed severe fibrocollagenous intimal thickening with luminal narrowing (Fig. 3). Occasionally the intimal thickening was composed predominantly of elastic tissue (Fig. ). Seven cases had thickening and reduplication, with fragmentation and destruction of the elastic laminae. Moderate adventitial fibrosis was a feature of four cases, and perivascular edema was seen in one. One case, with severe pulmonary arterial hypertensive changes, had a "dilatation lesion" consisting of a parent artery with intimal thickening and medial hypertrophy and an area of aneurysmal dilatation. The thin wall of the aneurysmal segment had a single elastic lamina and the lumen was filled by an organized thrombus (Fig. 5). Medial hypertrophy was seen in many arteries. Elastic Arteries. Degeneration with thickening of the intima of the elastic arteries was demonstrable in six cases. The intimal thickening was generally cellular, with focal infiltration by lymphocytes (Fig. 6). A number of elastic arteries had fibrocollagenous intimal hyperplasia (Fig. 7). Pulmonary Veins. The most obvious change of the pulmonary veins was fibrocollagenous intimal thickening, often compromising the lumen, present in five autopsies. Alterations of elastic laminae, though less conspicuous, were more common, and were seen as thickening and fragmentation (Fig. 8). Neither reduplication of elastic laminae nor arterialization of veins could be demonstrated. Discussion Pulmonary vascular involvement in SLE has been reported less frequently than pulmonary parenchymal changes. Baehr and associates 3 found pathologic changes of the pulmonary vessels, particularly fibrinoid necrosis, in 23 autopsied cases of SLE. In four of these, the right heart was enlarged. Fibrinoid necrosis of pulmonary arterioles was also described by Klemperer. 9 Wagenvoort and colleagues 15 reported a case of SLE with widespread necrotizing arteritis of pulmonary arteries and arterioles that had resulted in ischemic necrosis of large areas of the lung. Necrotizing pulmonary arteritis with subsequent fibrous occlusion of arterial lumen was found by Aitchison and Williams. 1 The frequent demonstration of acute changes of fibrinoid necrosis and vasculitis in lungs of patients with SLE may have contributed to the misconception that intimal fibrosis is uncommon. A variety of chronic or healed lesions was present in the lungs of those patients with SLE that we have studied. Muscular arteries are most severely affected. Although acute and chronic changes were found in arterioles, muscular and elastic arteries, the pulmonary veins had intimal fibrosis only. These lesions, typically seen in pulmonary hypertension, Downloaded from on 21 February 218

5 288 ^If^ FAYEMI? *I Downloaded from on 21 February 218 AJ.C.P. Vol.65

6 March 1976 PULMONARY VASCULAR DISEASE IN SLE 289 Fie. 5 (upper, left). Muscular artery, showing medial hypertrophy, intimal thickening, and a "dilatation lesion" with a thin wall and a single elastic lamina. Elastica-van Gieson. X8. FIG. 6 (upper, right). Elastic artery, showing cellular intimal proliferation with focal lymphocytic infiltrate. Hematoxylin and eosin. x8. FIG. 7 (lower, left). Elastic artery, showing fibrocollagenous intimal thickening. Elastica-van Gieson. x8. FIG. 8 (lower, right). Pulmonary vein, showing fibrous intimal thickening and fragmentation of elastic lamina. Elastica-van Gieson. X8. include intimal and medial changes and aneurysmal dilatation. It is interesting that although some of the patients developed dyspnea during the course of their illness, it was generally ascribed to the accompanying pulmonary infections. In many cases the associated renal disease was severe enough to mask the pulmonary symptoms. Of interest also was the absence of cor pulmonale or right ventricular hypertrophy despite the extensive pulmonary vascular changes. This indicates either a rapid evolution of these vascular lesions or a lack of correlation between pulmonary vascular morphology and its effect on the right heart in SLE. The most frequently occurring alteration of arterioles, arteries and veins was intimal thickening, sufficient to cause considerable luminal narrowing. These lesions were unrelated to the age of the patient or to therapy by corticosteroids, cyclophosphamide, or azathioprine. The pathogenesis of intimal thickening is unclear, and Wagenvoort and associates 15 have suggested four pathogenetic pathways: (1) a nonspecific response; (2) organization of thrombi; (3) response to increased pulmonary blood flow or increased pulmonary blood pressure; () hypoxia. We believe that patients with SLE may sustain damage to the vascular endothelium from vasculitis or thrombosis, or both, and that intimal proliferation and thickening of the pulmonary vasculation follow these acute phenomena. The morphogenesis of the pulmonary vascular lesions in SLE is not known. Johnson and Richardson 8 have described necrosis, vasculitis, thrombi, and proliferative changes occurring in small blood vessels of the central nervous system in patients with SLE. The deposition of immune complexes has been incriminated as being a major factor in the evolution of the vascular necrosis in the kidney 1 and brain. 2-8 To our knowledge, the presence of immune complexes in the lung in SLE has not been documented, and the role of these factors in the pathogenesis of pulmonary vascular lesions can only be speculated upon at the present time. Three clinical patterns of pulmonary involvement in SLE have been described. 7 Bilateral pleurisy may be associated with fever and toxemia. Recurrent febrile attacks of cough, pleurisy, and dyspnea may occur. Less commonly, there may be unexplained breathlessness. The first two patterns are probably related to pleurisy and recurrent bronchopneumonia, which are common in SLE. Breathlessness has not been well explained. The severe degenerative vascular changes may lead to recurrent pulmonary infarction and thus may be the basis of the unexplained breathlessness. Pulmonary hypertension has been recognized in patients with SLE.,5- ' Thus, at a clinicopathologic conference, a 21 -yearold woman with multiple arthralgias, Raynaud's phenomenon complicated by the development of ulceration of finger tips, and posidve LE cell preparation, was discussed. The muscular arteries showed intimal thickening, healed pulmonary Downloaded from on 21 February 218

7 29 FAYEMI A J.C.P. Vol. 65 emboli and right ventricular hypertrophy. It was concluded that this was a case of Raynaud's disease associated with pulmonary hypertension caused by the constrictive effect on the vessels of the lung. A similar case was reported by Sergent and Lockshin. 1 Their patient died of progressive pulmonary hypertension. Cummings 5 also reported a case of SLE in a 31-year-old farm worker who also had pulmonary hypertension. However, she was alive and well two years after diagnosis. This combination of lesions has led to the hypothesis that primary pulmonary hypertension may develop as a manifestation of SLE or the two entities may coexist in the same patient. The present study emphasizes the widespread vascular changes that may occur in SLE, even in the absence of Raynaud's phenomenon. Although pulmonary lesions are common in SLE, only a few patients go on to develop clinical manifestations of pulmonary hypertension and right heart failure. 11 We believe that the vascular changes in the lungs are an integral part of SLE, and, therefore, this disease should be included as a cause of secondary pulmonary hypertension. References 1. Aitchison JD, Williams AW: Pulmonary changes in disseminated lupus erythematosus. Ann Rheum Dis 15:26-32, Atkins JK, Quismorio FP, Friou GI: The choroid plexus in systemic lupus erythematosus (SLE): Arthritis Rheum 1:18 (abstr), Baehr G, Klemperer P, Schiffrin A: A diffuse disease of the peripheral circulation (usually associated with lupus erythematosus and endocarditis). Trans Assoc Am Physicians 5: , Case records of the Massachusetts General Hospital, Case N Engl J Med 288: 2-21, Cummings P: Primary pulmonary hypertension and SLE. N Engl J Med 288:178, Foldes J: Acute systemic lupus erythematosus. Am J Clin Pathol 16:16-173, Hoffbrand BI, Beck ER: "Unexplained" dyspnea and shrinking lungs in systemic lupus erythematosus. Br Med J 1: , Johnson RT, Richardson EP: The neurological manifestations of systemic lupus erythematosus. Medicine 7: , Klemperer P, Pollack AD, Baehr G: Pathology of disseminated lupus erythematosus. Arch Pathol 32: , Koffler D: Immunopathogenesis of systemic lupus erythematosus. Annu Rev Med 25:19-16, Olsen EGJ: Pathology of the Heart. Intercontinental Medical Cooperation, New York, New York, Olsen EGJ, Lever JV: Pulmonary changes in systemic lupus erythematosus. Br J Chest Dis 66:71-78, Rakov HL, Taylor JS: Acute disseminated lupus erythematosus without cutaneous manifestations and heretofore undescribed pulmonary lesions. Arch Intern Med 7:88-1, Sergent JS, Lockshin MD: Primary pulmonary hypertension and SLE. N Engl J Med 288: 178, Wagenvoort CA, Heath D, Edwards JE: The Pathology of Pulmonary Vasculature. Springfield, 111. Charles C Thomas, Yamamoto Y: Pathological study of 61 autopsied cases in disseminated lupus erythematosus. Nuguta Med J 77:129-12, 1963 Downloaded from on 21 February 218

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