CLINICAL FEATURES OF SYSTEMIC LUPUS ERYTHEMATOSUS
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1 55 CLINICAL FEATURES OF SYSTEMIC LUPUS ERYTHEMATOSUS Differences Related to Race and Age of Onset STANLEY P. BALLOU, MUHAMMAD A. KHAN, and IRVING KUSHNER ' We compared the frequency of clinical features of systemic lupus erythematosus (SLE) and determined survival in 113 patients with younger-onset lupus (age <55 at clinical diagnosis) and 25 patients with olderonset disease (age 155 at diagnosis). The most striking difference was in the racial distribution; 59% of the younger patients were black, compared with only 20% of the oldeponset patients (I' < 0.001). Major manifestations of lupus (including clinically evident renal disease, central nervous system involvement, cutaneous involvement, and hemocytopenia) occurred with similar frequency in both age groups. Antibodies to DNA were detectable equally often in both groups, but hypocomplementemia was more common in the younger patients. Five-year survival in the younger-onset group (79%) was similar to that of the older-onset group (72%); there was a tendency toward relatively improved survival in patients in the latter group when compared with the expected survival of appropriately matched control populations. Major significant differences in racial distribution included 1) a higher incidence of serositis in older whites and in blacks regardless of age, and 2) more frequent hypocomplementemia in younger patients within both racial groups. From the Department of Medicine, Case Western Reserve University at Cleveland Metropolitan General Hospital. Supported by grants from the Ohio Lupus Foundation and the Irma H. Bender Arthritis Research Fund. Stanley P. Ballou, MD: Assistant Professor of Medicine; Muhammad A. Khan, MD: Associate Professor of Medicine; Irving Kushner, MD: Professor of Medicine. Address reprint requests to Stanley P. Ballou, Cuyahoga County Hospital, Cleveland Metropolitan General Hospital, 3395 Scranton Road, Cleveland, Ohio Submitted for publication September 8, 1980; accepted in revised form July 2, Systemic lupus erythematosus (SLE) most frequently has its onset in the second through fourth decades of life. When it begins at a later age, the disease seems to be less severe; recent communications have indicated a relatively mild course of disease in patients who develop SLE after the fifth decade of life (1,2). In an attempt to confirm these observations, we compared clinical features of disease in patients in whom lupus began relatively late in life and patients in whom SLE was diagnosed at a younger age, and we compared survival rates in these 2 groups of patients with expected survivq] rates for matched control populations. The finding of a striking difference in racial distribution between younger- and older-onset patients led us to compare clinical features between the younger and older patients in each racial group and between whites and blacks in both age groups. PATIENTS AND METHODS We studied 138 patients with SLE who have been seen at Cleveland Metropolitan General Hospital as either inpatients or outpatients between 1940 and All but 2 met the preliminary American Rheumatism Association criteria for SLE (3). SLE was diagnosed in 25 patients at or after the age of 55 (older-onset group) and in 113 patients before the age of 55 (younger-onset group). Salient clinical features in these patients were ascertained by retrospective review and included: 1) age at diagnosis, 2) evidence of clinical renal involvement (abnormal urine sediment, proteinuria greater than 500 mg/day, or otherwise unexplained elevation of serum creatinine > 1.4 mg/dl), 3) occurrence of chronic renal failure, 4) central nervous system (CNS) involvement, 5) cutaneous involvement, 6) serositis (including pleuritis, pericarditis, or both), and 7) Raynaud's phenomenon. Recorded laboratory findings included: 1) occurrence of thrombocytopenia or hemolytic anemia and 2) presence, at any time during the course of disease, of Arthritis and Rheumatism, Vol. 25, No. 1 (January 1982)
2 56 BALLOU ET AL Table 1. Clinical features in 138 patients with younger- and olderonset lupus Younger Older onset onset (n = 113) (n = 25) Significance* Mean age at diagnosis Sex:fernale/rnale 100/ NS Race: blac Wwhite 66/45 t s/20 P < Clinical renal involvement 60 (53%) 10 (40%) NS Chronic renal failure I2 ( I I%) 2 ( 8%) NS CNSS involvement 45 (40%) 7 ( NS Serositisl 52 (46%) 16 (64%) NS Cutaneous involvement 78 (69%) 16 (64%) NS Raynaud's phenomenon 17 (15%) I ( 4%) NS * NS = not significant. t n = 1 11; I hispanic and I oriental patient not included. S CNS = central nervous system. 5 n = 23 patients. B lncludes pleuritis and pericarditis. antibodies to double-stranded DNA as detected by the Crithidiu fuciliae immunofluorescent pethod (4), or reduced levels of serum C3 (<W mg/dl). Finally, we determined the type and dosage of treatment administered during the course OF disease in 126 of the patients. Regimens recorded weye: high-dose systemic corficosteroids (>30 mg prednisone daily for at least 3 consecutive months, at any period during the course of disease), lowdose corticosteroids (530 mg prednisone daily, or >3Q mg for less than 3 consecutive months), or immunosuppressive agents (employed at any time). Survival rates for the 113 patients with youngeronset lupus and the 25 patients with older-onset lupus were calculated by the life-table method (5) and were compared m + z W a LA a W rn White 5 Black Other 4 J h MF MF I\r I AGE AT DIAGNOSIS, YEARS Figure 1. The distribution of 138 lupus patients by age (at diagnosis), race, and sex. using the logrank test (6). These survival rates were also compared with the expected survival of control populations matched for age, sex, race, and calendar year (7). Disease onset, for purposes of this study, was defined as the age at clinical diagnosis, i.e., that point when multisystem disease was manifest without alternate explanation, so that the diagnosis of SLE could confidently be made. Statistical comparisons between groups were carried out by the chisquare test and Fisher's exact test. RESULTS Cliqical features in the 2 groups of patients are shown in Table 1. Female predominance appeared less marked in the patients with older-onset lupus (3: 1) than in the younger group (8:1), although this difference did not attain statistical significance (0.05 < P < 0.1). There was a significant difference in racial distribution between groups: 59% of the younger-onset patients were blacks, compared with only 20% of the older-onset group (P < 0.001). The distribution of all patients by age, race, and sex is showr) in Figure 1. The frequency of occurrence of other clinical features-including clinically evident renal disease, chronic renal failure, central nervous system manifestations, serositis, cutaneous involvement, and Raynaud's phenomenon-did not differ significantly in the 2 groups. Selected laboratory findings are shown in Table 2. The occurrence of hemocytopenia (thrombocytopenia or hemolytic anemia) and the frequency of detection of antibodies to double-stranded DNA were similar in both groups. Reduced levels of serum complement (C3), however, were detected in a greater proportion of younger patients (P < 0.02). Therapy employed in the 2 groups is shown in Table 3. The younger-onset patients tended to receive high-dose corticosteroids more often; however, the difference did not achieve statistical significance. Survival curves for the I13 younger-onset and 25 older-onset patients are illustrated in Figures 2 and Tqble 2. Laboratory features in 138 patients with younger- and older-onset lupus Younger Older onset onset (n = 113) (n = 25) Significance* Hernocytopeniat 27 (25%)$ 3 ( 12%) NS Elevated levels of antidna 76 (671) 19 (76%) Reduced C3 level 63 (68%)8 8 (40%)7 NS P < 0.02 * NS = not significant. t Hernocytopenia = hemolytic anemia or thrornbocytopenk. S n = 110. I n = 92.!I n = 20.
3 CLINICAL FEATURES OF SLE 57 Table 3. Therapy in patients with younger- and older-onset lupus. ~ Younger - Older onset onset Treatment n = 103 n = 23 Significance* Immunosuppressives 20 (19%) 3 (13%) NS High-dose steroidst 49 (48%) 7 (30%) NS Low-dose steroids$ 42 (41%) 12 (5296) NS * NS = not significant. t >30 mg prednisone daily for at least 3 consecutive months. $ 530 mg prednisone daily or >30 mglday For less than 3 consecutive months. 3 respectively. In each group there was a significant decrease in survival when compared with the expected survival of a control population matched for age, race, sex, and calendar year (P < 0.001). Survival at 5 years was 78.9% in the younger-onset patients and 7 I.9% in those with older-onset disease (P = not significant, by logrank test). The survival of the older-onset patients, however, did not differ as markedly from the expected survival of an age-matched control population as did that of the younger age group. At 7 years, for example, survival in the older group (71.9%) was 83% of expected, and in the younger group (70.9%) was 73% of expected (P = not significant). Because of the possibility that differences in clinical manifestations between younger- and olderonset SLE might reflect differences in the racial makeup of these groups, we compared the frequency of these clinical manifestations between the yobnger and older patients in each racial group and between blacks and whites within the two age groups. The significant -1 I00 90 (Jj 70 YEARS '\ Expected '. \ \ \o Observed I I I FROM DIAGNOSIS Figure 3. Observed and expected survival curves for 25 SLE patients with older-onset disease (mean age of onset, 62). differences we found are shown in Table 4. The comparisons between younger and older black patients and between older white and black patients are not shown because the small number of older black patients precluded meaningful analyses. There was a higher frequtncy of serositis in older whites than in younger whlte patients and in younger blacks than younger whites, while hypocomplementemia was present more often in younger patients, regardless of race. There was also a slightly increased incidence of hemocytopenia in younger whites as compared with other groups. " YEARS FROM DIAGNOSIS Figure 2. Observed and expected survival curves for 113 SLE patients with onset of disease before age 55 (mean age of onsef, 32). DISCUSSION Within a group of 138 SLE patients, there were 25 patients (18%) in whom SLE was diagnosed at 55 years of age or later. This proportion is slightly higher than that (12%) reported from other centers (1.2). However, we chose to define "onset" as the time of clinical diagnosis of SLE. We did not regard onset as the occurrence of the first manifestation, since this may be a less precisely definable point in time. It is nonetheless possible that some of our older-onset patients may have had symptoms attributable to SLE for some years before the time when a definite diagnosis of lupus could be established. The major differences bet ween these younger-
4 ~~ 58 BALLOU ET AL Table 4. Disease manifestations in subsets of patients with lupus, categorized by race and sex. Younger Older Younger Younger white white white black (n = 45) (n = 20) P (n = 45) (n = 66) P Serositis I1 (25%) 13 (65%) <O.Ol 11 (25%) 39 (59%) <0.001 Hypocbmple- N Sll mentemia (C3) 29 (73%)* 7 (41%)t C (73%)* 33 (65%)$ Hemoc ytopenia 16 (36%) 3 (is%) co.1 16 (36%) 11 (17%)~ <o.o5 *n=40. t n = 17. t n = n = NS = not significant and older-onset patients involved the sex and race distributions. The widely recognized female predominance of SLE was much less apparent in the older patients (about 3:l) than in the younger group (about 8: 1). This observation has been noted in the previous studies of Maddock (8) and Masi and Kaslow (9). The racial distribution in patients with olderonset SLE is even more interesting: only 20% of these patients were black, as compared with 59% of the younger patients, a highly significant difference (P < 0.001). The predisposition of black females for development of SLE was noted by Siegel et al (10,ll) in epidemiologic studies in New York City and Jefferson County, Alabama, and has been recently reemphasized by Fessel (12). It has not been widely appreciated, however, that this predominance is apparently largely restricted to younger patients, even though the data of Siegel et a1 (10) suggested that the propensity for SLE to occur in black females was more apparent in patients aged Among previously reported patients with older-onset SLE, Baker et al (1) and Foad et a1 (13) noted that 2 of 31 and none of 9 patients, respectively, were black; the racial distribution of their younger patients was not reported. No other studies have specifically addressed the racial distribution of older-onset SLE patients. Our study suggests that younger, but not older, black females are particularly predisposed to SLE. This difference may account for the reduced mortality from SLE in older black patients recently reported by Kaslow and Masi (14). The frequency of major clinical manifestations of lupus was similar in the 2 age groups. Several other investigators have studied manifestations of lupus in patients with older-onset disease. Wilson et al (2) noted a decreased incidence of renal involvement with age, while Urowitz et a1 (15) and Baker et al (I) reported that skin involvement was less frequent; the latter group also found a reduced occurrence of central nervous system involvement in older patients. We did not find such differences in our series. The occurrence of hemocytopenia (either thrombocytopenia or hemolytic anemia or both) could be evaluated in 135 of our patients. We found this manifestation to be slightly more common in younger patients, as previously noted by Alger et a1 (16). This increased frequency was apparently confined to younger white patients, in whom hemocytopenia was significantly more common than in younger blacks. The presence of serologic abnormalities in patients with older-onset lupus was studied by Wilson et a1 (1). They found higher levels of total hemolytic complement and less marked serologic abnormalities in older patients. Serum C3 leiels were available in 112 of our patients and were less often depressed in the older age group, regardless of race. However, antibodies to double-stranded DNA were present in elevated titers at some time during the course of disease in a similar proportion of patients in both groups. Assessment of therapy employed during the course of disease revealed no significant differences between the 2 groups. There was a tendency to use high doses of corticosteroids more frequently in younger patients, although this difference did not achieve statistical significance. Both Baker et al (1) and Urowitz et a1 (15) also noted a reduced steroid requirement in patients with older-onset SLE. While strongly persuasive evidence of less severe disease in older-onset patients was not found on evaluation of clinical manifestations, survival curves did suggest relatively improved prognosis for life of the older patients compared with the younger patients.
5 CLINICAL FEATURES OF SLE 59 The "adjusted" survival rates (the proportion of surviving patients as a percentage of the survivors of a matched control population) at 7 years were 83% in the older patients and 73% in the younger patients. This difference, while not statistically significant, is consistent with previous impressions of more favorable prognosis in patients with older-onset disease (17). Baker et a1 (I) also observed a favorable 5-year survival rate in their group of 31 older-onset patients. The overall 5-year survival of all patients in our series, 77.4%, is comparable to that recently reported from the Lupus Survival Study Group (18). The significantly different racial distribution between the two age groups indicates that the frequency of clinical features in these groups might be influenced by racial factors. We therefore compared features among various subsets defined by race and age of onset, i.e., younger whites, younger blacks, older whites, and older blacks. We found that serositis was more frequent in older whites than in younger white patients. An increased incidence of lupus pulmonary involvement in older-onset patients was also found by Baker et a1 (I) and Urowitz et al (15). Our failure to find an age-related difference in this manifestation when patients were not categorized by race is explained by the observation that serositis was also more common in black patients, who were predominantly younger. Other significant differences included an increased incidence of hemocytopenia in younger whites and more frequent hypocomplementemia in younger patients regardless of race. We also compared clinical features among all black and white patients without regard to age of onset. Both chronic renal failure and fatalities occurred significantly more frequently in black than in white patients (P < 0.05); when compared within age groups, however, these differences were not statistically significant. Although some previous reports have noted an increased morbidity and mortality in blacks (14,19). other investigators have not found such a relationship between race and prognosis (20-22). In summary, the most distinctive features that characterized patients with older-onset SLE in this study were the sex and race distributions, which demonstrated a reduced predominance of females and blacks. With the exception of serositis and hypocomplementemia, other major clinical features occurred with similar frequency in younger- and older-onset patients. Life-table analysis showed similar survival rates in both groups; however, there was a tendency toward improved survival in older-onset patients when compared with the expected survival of matched control populations. REFERENCES 1. Baker SB, Rovira JR, Campion EW, Mills JA: Late onset systemic lupus erythematosus. Am J Med 66: , Wilson HA, Winfield JB, Hamilton ME, Spyker DA. Brunner CM, Davis JS: Serologic studies in late onset systemic lupus erythematosus (abstract). Arthritis Rheum 22:674, Cohen AS, Reynolds WE, Franklin EC, Kulka JP, Ropes MW, Shulman LE, Wallace SL: Preliminary criteria for the classification of systemic lupus erythematosus. Bull Rheum Dis 21: , Crowe W, Kushner I: An immunofluorescent method using Crithidia luciliae to detect antibodies to doublestranded DNA. Arthritis Rheum 20: , Merrell M, Shulman LE: Determination of prognosis in chronic disease, illustrated by systemic lupus erythematosus. J Chronic Dis 1:12-32, Pet0 R, Pike MC, Armitage P, Breslow NE, Cox DR. Howard SV, Mantel N, McPherson K, Pet0 J, Smith PG: Design and analysis of randomized clinical trials requiring prolonged observation of each patient. 11. Analysis and examples. Br J Cancer 35: 1-39, Axtell LM: Computing survival rates for chronic disease patients. JAMA 186: , Maddock RK: Incidence of systemic lupus erythematosus by age and sex. JAMA 191: , Masi AT, Kaslow RA: Sex effects in systemic lupus erythematosus: a clue to pathogenesis. Arthritis Rheum 21: , Siegel M, Holley HL, Lee SL: Epidemiologic studies on systemic lupus erythematosus: comparative data for New York City and Jefferson County, Alabama, Arthritis Rheum 13: , Siegel M, Lee SL: The epidemiology of systemic lupus erythematosus. Semin Arthritis Rheum 3: Fessel WJ: Systemic lupus erythematosus in the community. Arch Intern Med 134: , Foad BSI, Sheon RP, Kirsner AB: Systemic lupus erythematosus in the elderly. Arch Intern Med 130: , Kaslow RA, Masi AT: Age, sex, and race effects on mortality from systemic lupus erythematosus in the United States. Arthritis Rheum 21 : , Urowitz MB, Stevens MB, Shulman LE: The influence of age on the clinical pattern of systemic lupus erythematosus (abstract). Arthritis Rheum 10: Alger M, Alarcon-Segovia D, Rivero SJ: Hemolytic
6 BALLOU ET AL anemia and thrombocytopenic purpura: two related subsets of systemic lupus erythematosus. J Rheumatol 4: , McCombs RP, Patterson JF: Factors influencing the course and prognosis of systemic lupus erythematosus. N Engl J Med 260: , Ginzler E, Diamond H: A multicenter study of survival in systemic lupus erythematosus (abstract). Arthritis Rheum 22:613, Siege1 M, Seelenfreund M: Racial and social factors in systemic lupus erythematosus. JAMA 191 :77-80, Dubois EL, Wiezchowiecki M, Cox MB, Weiner JM: Duration and death in systemic lupus erythematosus. JAMA 227: , Fries JF, Holman HR: Systemic Lupus Erythematosus: A Clinical Analysis. Philadelphia, W.B. Saunders Company, 1975, pp Estes D, Christian CL: The natural history of systemic lupus erythematosus by prospective analysis. Medicine 50:85-95, 1971
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