"PSEUDORHEUMATOID" SUBCUTANEOUS NODULES
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1 THE AMERICAN JOURNAL O CLINICAL PATHOLOGY Copyright I960 by The Williams & Wilkins Co. Vol. 45, No. 6 Printed in U.S.A. "PSEUDORHEUMATOID" SUBCUTANEOUS NODULES BRUCE W. MESARA, M.D., GERALD L. BRODY, M.D., AND HAROLD A. OBERMAN, M.D. Department of Pathology, The University of Michigan, Ann Arbor, Michigan Subcutaneous nodules characterized by necrotic collagen and occurring in patients without associated disease, such as rheumatoid arthritis, granuloma annulare, or rheumatic fever, have been recognized with increasing frequency in recent years. ' ' 6 ' 14 In adults, nodules may antedate the clinical appearance of rheumatoid arthritis; however, in children, nodules may be unassociated with future systemic disease. In the present study, 10 children and young adults with rheumatoid-like nodules who have been followed for relatively long intervals are presented. The histologic features of these isolated nodules are compared and contrasted with those occurring in patients with rheumatoid arthritis, rheumatic fever, and granuloma annulare. The results of the study permit assessment of the natural history and clinical course of these unusual lesions. REVIEW OP THE LITERATURE Ziegler 16 was the first to report isolated nodules in a 7-year-old girl, in 1941, but attention was not focused on this lesion until 18 years later, when Beatty reported 9 cases in the American literature. Ziegler's patient had nodules over the elbows and left knee. Beatty's patients ranged in age from 11 days to 9 years, 7 of the 9 patients being less than 5 years of age. All of the nodules reported by him were subcutaneous or attached to fascia, tendon, or periosteum, and none of the patients had clinical rheumatic or rheumatoid disease. A history of local trauma was obtained in only of the patients; nevertheless, the author postulated that these nodules represented a peculiar tissue response to trauma. Two of the patients had multiple lesions and others developed new nodules within several months after the time of the Received, November 4, 19G5. This paper was presented at the Annual Meeting of the American Society of Clinical Pathologists, Chicago, Illinois, October 17 to, initial biopsy. No long-term follow-up data were given for these patients. In 1959, Draheim and associates 6 presented 54 cases of "rheumatoid-like" nodules in children who lacked clinical manifestations of rheumatoid disease. The age of peak incidence in these patients was between and 6 years, and they had been followed for 1 to 14 years. One patient developed rheumatic fever, although the nodules had resolved long before onset of the systemic disease. None developed rheumatoid arthritis. Approximately }/i of these patients manifested skin lesions suggestive of granuloma annulare. The authors concluded that a diagnosis of rheumatoid arthritis was not warranted on the basis of the nodule alone, and they postulated that the nodules might have occurred on an allergic basis. Regrettably, this large series has not been fully documented. A 6-year-old girl with subcutaneous nodules in the scalp and lower portion of the skin of the back was reported by Taranta 14 in 196. Two courses of corticosteroid therapy were followed by disappearance of the nodules, and during a period of S years, new nodules did not develop and no systemic disease occurred. Altaian and Caffrey 1 reported children with similar digital nodules. Both children lacked systemic disease and were well during the brief periods of followup reported. There are also scattered reports 5, s ' " 16 of isolated subcutaneous nodules that have been believed to be manifestations of granuloma annulare in patients lacking cutaneous involvement. In retrospect, these lesions may be similar to those described by Beatty and Taranta. Lowney and Simons 9 discussed the occurrence of isolated, subcutaneous, necrotic nodules in adults and children. They concluded that in adults these lesions may be the first sign of rheumatoid arthritis, preceding the onset of joint involvement by as much as 10 years; however, basing their conclusions on a review of cases in the literature,
2 June 1966 PSEUDORHEUMATOID NODULES 685 TABLE 1 CLINICAL INDINGS IN 1 PATIENTS WITH "PSEUDOKHEUMATOID" NODULES Case No. Age at Onset Sex Presenting Lesion(s) (Location) Recurrent* Lesion(s) (Location) ollowup* Present Status yr. 1 4 Right tibia and ilium, buttock Left knee Occiput Left tibia Right tibia, 4 mo. Left knee, mo., yr.; Right tibia, 7 yr. Occiput, mo.; knee, G mo. Left tibia, 4 yr No nodules since age G Nodule on left knee Nodule on knee No nodules since age M Right 5th metatarsal Occiput, arm Right 5th metatarsal, 1 and yr. Occiput, hands, feet, 1 10 G No nodules since age G No new nodules G 8 8 M M M Right tibia Knees Left ulna Right ankle Right wrist Right wrist yr. None Occiput, right metatarsal, 4 mo. Left ulna, mo. None None Left knee, left ankle, 11 yr.; right elbow, left hand, left foot, 14 yr No recurrence Persistent nodules Persistent nodules No recurrence No recurrence Multiple persistent nodules * Interval after excision of presenting lesion. they postulated that in children these nodules, which were usually located over the tibia, olecranon, or skull, represented unusual manifestations of granuloma annulare. The issue has been clouded by other reports 4 1 of dermal nodules in patients with rheumatoid arthritis. This emphasizes the need for a more definitive distinction between the nodules of granuloma annulare and rheumatoid arthritis than the mere location of the lesions. MATERIALS AND METHODS All biopsies of rheumatoid and rheumatic nodules, and of granuloma annulare, seen at The University of Michigan Medical Center between 1944 and 1964 were reviewed. The hospital records of the children or other patients who had these lesions without concurrent rheumatoid arthritis or rheumatic fever were studied in detail. Twelve patients had no evidence of systemic disease when the subcutaneous nodules presented. The nodules examined microscopically had been present clinically for from 5 weeks to S years before excision, 6 having been observed for less than 6 months. Long-term follow-up information on all patients was obtained through correspondence with the patients or with their family physicians. The clinical findings are summarized in Table 1. The original slides were reviewed, paraffin blocks were recut, and the following stains were utilized: hematoxylin and eosin, phosphotungstic acid hematoxylin, periodic acid- Schiff, and acid mucopolysaccharide (method of Rinehart and Abul-Haj). A similar number of nodules from patients with granuloma annulare, rheumatoid arthritis, and rheumatic fever were subjected to the same staining technics for comparison. CLINICAL INDINGS Association with systemic disease or trauma. None of the patients had symptoms of rheumatic fever, rheumatoid arthritis, or other systemic disease. Three years after nodules had been detected, 1 patient (Case ) developed acute glomerulotubular nephritis, from which she recovered. There was no change in
3 686 MESARA ET AL. Vol. 45 DISTRIBUTION BY CASE O Primary nodulei A Recurrent nodutet IG. 1. Location of primary and recurrent "pseudorhcumatoid" nodules in 1 patients. the nodules during the course of the nephritis. Another patient (Case 9) had no history of joint pain or pharyngitis; however, the antistreptolysin 0 titer was 500 Todd units weeks prior to biopsy. The erythrocytic sedimentation rate was normal, as were other laboratory determinations. There was no evidence of carditis or cardiac murmurs. An indefinite history of local trauma, before the appearance of the nodules, was obtained in only cases. Age and sex. Eight of the 1 patients were females. Their ages at onset ranged from to S years; the average age of the patients was 4 years. It should be noted that several of the patients were seen in this hospital for as long as 11 years after the initial occurrence of the nodules. Physical findings. The majority of the nodules presented as firm masses, usually deeply attached to underlying periosteum or fascia. Only of the lesions were painful or tender to palpation. In 4 patients the nodules were described as freely movable in the subcutaneum. Although the lesions were widely distributed over the body (ig. 1), there was a predilection for involvement of the extremities, especially over bony protuberances, and of the occipital region of the skull. Only 1 of the nodules was located at the elbow. The nodules varied in greatest dimension from a few millimeters to cm.; the majority were approximately 1 cm. in diameter. One patient (Case ) presented with a cluster of 4 nodules in the occiput, whereas the remainder of the patients had discrete nodules at separate locations. All of the primary nodules in which depth of involvement was documented (S cases) were located in the subcutaneum. Recurrent nodules in areas of previous excision were fixed to the dermis by scar tissue. Recurrent lesions. Seven patients developed recurrent nodules in areas of previous excision, and 5 developed nodules at new locations after the presenting lesions were excised. our patients developed recurrences within as brief an interval as months from the time of removal of the primary lesion. Two other patients (Cases 4 and 5) had recurrent nodules which spontaneously regressed and disappeared at the operative site. The remainder of the unexcised recurrent nodules decreased only slightly in size during the follow-up intervals. Therapy. The majority of these patients received no treatment, despite the histologic diagnosis of "rheumatoid nodule." One patient (Case S) was administered large doses of aspirin. The nodules persisted, but were said to be smaller. Two other patients (Cases 5 and 9) received prophylactic doses of penicillin for 1 and 10 years, respectively. In Case 9 the therapy was initiated when the antistreptolysin 0 titer was elevated on 1 occasion. None of these patients received corticosteriods. ollow-up. All of the patients have been followed for at least 1 year, and some have been observed for as long as 17 years from the time of detection of the lesions. Although there have been recurrent nodules at the primary site, or new nodules in other areas, none of the patients has developed physical signs or symptoms indicative of systemic disease such as rheumatic fever or rheumatoid arthritis. PATHOLOGIC INDINGS The nodules from patients without clinical manifestations of rheumatoid arthritis
4 June 1966 "PESUDORHEUMATOID" NODULES IG. (upper). "Pseudorheumatoid" nodule manifesting necrosis surrounded by florid proliferation of histiocytes and lymphocytes. This nodule had been present for months. Hematoxylin and eosin. X 0. IG. (lower). Detailed view of margin of area of necrosis and cellular proliferation in igure. Note much greater cellularity than in igure 4. Hematoxylin and eosin. X
5 688 MESARA ET, AL.... < & * :* IG. 4 (upper). Subcutaneous nodule in adult patient with rheumatoid arthritis. The nodule had been present for months. Hematoxylin and eosin. X 116. IG. 5 (lower). Vascular proliferation adjacent to "pseudorheumatoid" nodule. Hematoxylin and eosin. X 60. Vol. 45
6 June 1966 PSEUDORHEUMATOID NODULES 689 '?"',Vsi'/'«'i7 C io. G. Collagenization of periphery and center of "psci.idorheumnt.oid" nodule. The lesion had been present for approximately 1 year. Hematoxylin and eosin. X 8.5. were compared with nodules from patients with rheumatoid arthritis, granuloma annulare, or rheumatic fever. The necrosis in the rheumatoid and "pseudorheumatoid" nodules, as well as in the nodules of rheumatic fever, was located in the subcutaneum, whereas that seen in granuloma annulare was centered in the dermis. In some of the recurrent "pseudorheumatoid" nodules, as well as in the large rheumatoid nodules, necrosis extended into the lower dermis. The extent of necrosis in the "pseudorheumatoid" nodule generally was intermediate between that seen in patients with rheumatoid nodules and that seen in granuloma annulare. The extension of fibrinoid necrosis into the surrounding tissue, fusion of adjacent foci of necrosis, and central karyorrhexis, all features which tend to characterize rheumatoid nodules, were uncommon in the pseudorheumatoid nodules. The "pseudorheumatoid" nodule, especially in the first few months of its development, was characterized by proliferation of histiocytes. In some instances, this process overshadowed areas of necrosis (igs. and ); at equivalent stages of development, it was more extensive than that seen in rheumatoid nodules (ig. 4). Increase in numbers of capillaries and hypertrophy of endothelial cells were components of the "pseudorheumatoid" and rheumatoid nodules, but were not a predominant feature of the nodules in patients with rheumatic fever or granuloma annulare (ig. 5). Lymphocytic and plasmacytic infiltrates usually accompanied the formation of new blood vessels, although such an inflammatory response was less pronounced in the "pseudorheumatoid" nodules. There also appeared to be less peripheral scarring in these lesions than was seen in the rheumatoid nodules, although this was not true of long-standing lesions (ig. 6). Broad zones of acid mucopolysaccharide (AMP)-positive material were present in areas of necrosis, as well as between adjacent collagen in the dermis and around blood vessels in specimens from patients with granuloma annulare. The areas of necrosis in the evolving "pseudorheumatoid" nodule also
7 690 MESARA ET AL. Vol. 45 contained AMP-positive material; however, this was also present in the nodule of rheumatic fever and, to a variable degree, in the early rheumatoid nodule. Even the early rheumatoid and rheumatic nodules contained a considerable amount of phosphotungstic acid-hematoxylin-positive material (fibrin-h'brinoid). In marked contrast, this material was sparse in the areas of necrosis in the "pseudorheumatoid" nodules and in nodules of granuloma annulare. It should be noted that the histologic differences were often more quantitative than qualitative and in several instances were insufficient to differentiate the lesions. DISCUSSION The patients with "pseudorheumatoid" nodules were free from evidence of systemic disease when the nodules were removed and remained so for as long as 17 years. In more than one half of the patients the nodules recurred and persisted. Subcutaneous nodules over bony prominences are, by tradition, the stigmata of systemic disease, especially rheumatic fever or rheumatoid arthritis. ' ' 1 We found no reports of a rheumatic nodule which had preceded clinical onset of rheumatic fever and had persisted until the onset of major manifestations of the disease; however, reports indicated that subutaneous rheumatoid nodules occur in adults to 10 years before onset of symptomatic rheumatoid arthritis. 9 Similar reports have not been recorded for children. Little evidence is available to explain the etiology of these lesions. The location of the nodules in the patients is similar to that reported by other authors. The distribution over bony prominences is analogous to the nodules of rheumatoid arthritis and rheumatic fever. None of these patients had dermal lesions suggestive of granuloma annulare, in contrast to the 5 per cent incidence of granuloma annulare in the series reported by Draheim and associates. Although subcutaneous nodules have been induced in children with rheumatic fever by local daily trauma, 10 only patients in the present report had a history of trauma. It is unlikely that the nodules represent, in part, a reaction to streptococcal infection. Only 1 of the patients manifested an elevated antistreptolysin 0 titer. In the remainder, there was no clinical streptococcal infection. Latex-fixation tests for rheumatoid arthritis were negative in of the patients. These comparatively innocuous lesions cannot be distinguished histologically from rheumatoid nodules with absolute certainty; however, several morphologic features are helpful. The pseudorheumatoid nodule, especially early in its evolution, generally shows more florid proliferation of histiocytes and a lesser degree of peripheral collagenization than does the rheumatoid nodule. urthermore, although proliferation of capillaries and chronic perivasculitis were seen in both, they were more pronounced in the rheumatoid nodule. The "pseudorheumatoid" nodules usually contained more acid mucopolysaccharide and less central karyorrhexis and fibrinoid (phosphotungstic acid-hematoxylinpositive) material than did the rheumatoid nodule at equivalent stages of development. Scant fibrinoid and considerable AMP were present in the lesions of granuloma annulare. Nevertheless, these differences were a matter of degree and difficult to interpret in the individual example. Most important is the recognition of the characteristic distribution and clinical course of the lesions. The subcutaneous necrotic nodules occurred in young children and had most frequently involved the lower extremities and occiput. Only 1 nodule occurred over the olecranon process. The majority of the patients developed recurrent nodules at the site of biopsy or in new areas, and the lesions often persisted for many years. Yet, most important, in no instance were the lesions associated with systemic disease. Therefore, one may conclude that the presence of such nodules in young children, in the absence of other manifestations of systemic disease, i.e., rheumatic fever or rheumatoid arthritis, is not sufficient reason to subject the patients to long-term prophylactic therapy. SUMMARY Twelve patients with subcutaneous nodules and without demonstrable evidence
8 June 1966 "PSEUDOKHEUMATOID" NODULES G91 of rheumatoid arthritis or rheumatic fever are presented. After a follow-up period of 1 to 17 years, none has developed systemic disease, despite the fact that the nodules have recurred or persisted in more than one half of the instances. Although the nodules cannot be distinguished with certainty from those of rheumatoid arthritis or rheumatic fever, they tend to have a more florid proliferation of histiocytes, a lesser degree of peripheral collagenization, and less central fibrinoid necrosis than do the nodules in the other diseases mentioned. REERENCES 1. Altman, R, S., and Caffrey, P. R.: Isolated subcutaneous rheumatic nodules. Pediatrics, 4: , 19(54.. Baldwin, J. S., Kerr, J. M., Kuttner, A. G., and Doyle, E..: Observations on rheumatic nodules over a 0-vear period. J. Pediat., 56: , Beatty, E. C: Rheumatic-like nodules occurring in nonrhcumatic children. A. M. A. Arch. Path., 68: , Bowers, R. E.: Histology of granuloma annulare compared with that of necrobiotic nodules of rheumatoid arthritis. Brit. J. Dcrmat., 61: 47-50, Dannenberg, A. M., Young, 1., and Tuncali, M. T.: Granuloma annulare; report of a case with lesions in the galea aponeurotica of a child. A. M. A. J. Dis. Child., 96: 70-7, Draheim, J. II., Johnson, L. C, and Helwig, E. B.: A clinicopathologic analysis of "rheumatoid" nodules occurring in 54 children. Am. J. Path. 5: 078, Keil, ]!.: The rheumatic subcutaneous nodules and simulating lesions. Medicine. 17: 01-80, Lenahan, G. T.: Case for diagnosis (granuloma annulare). A. M. A. Arch. Dermat. & Syph., 71: , Lowney, E. D., and Simons, II. M.: "Rheumatoid" nodules of skin. Arch. Dermat. & Syph., 88: , Massell, B.., Mote, J. R., and Jones, T. D.: Artificial induction of subcutaneous nodules in patients with rheumatic fever. J. Clin. Invest., 16: 15-18, Miller, H. E.: Subcutaneous granuloma annulare? Arch. Dermat. & Syph., 60: , Rosenberg, E..: Pathology of rheumatoid arthritis, In Hollander, J. L.: Arthritis and Allied Conditions, Ed. 0. Philadelphia: Lea & ebiger, 1900, pp. 1S Shulman, L. E., and Bunim, J. J.: Disorders of the joints, In Harrison, T. R., Adams, R. D., Bennett, I. L., Resnik, W. II., Thorn, G. W., and Wintrobc, M. M.: Principles of Internal Medicine, Ed. 4. New York: McGraw-Hill, 190, pp Taranta, A.: Occurrence of rheumatic-like subcutaneous nodules without evidence of joint or heart, disease. Report of a case. New England J. Med., 66: 1-10, Tizard, J. P. M.: Subcutaneous nodules for diagnosis, granuloma annulare. Proc. Roy. Soc. Med., 41: 01-0, Ziegler, E.: Rheumatismus nodosus als einzige Manifestation der rheumatischen Krankhcit. Arch. Kinderh., 1SS: 1-0, 1941.
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