Changing patterns in the histopathology of idiopathic nephrotic syndrome in children 1
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1 Kidney International, Vol. 55 (1999), pp Changing patterns in the histopathology of idiopathic nephrotic syndrome in children 1 MELVIN BONILLA-FELIX, CESAR PARRA, TALA DAJANI, MARIA FERRIS, RITA D. SWINFORD, RONALD J. PORTMAN, and REGINA VERANI Department of Pediatrics and Pathology, University of Texas-Houston Health Science Center, Houston, Texas, USA Changing patterns in the histopathology of idiopathic nephrotic The International Study of Kidney Disease in Children syndrome in children. (ISKDC) reported in the 1970s that minimal change ne- Background. It is widely accepted that minimal change nephrotic syndrome (MCNS) was the most common histophrotic syndrome (MCNS) is the most common cause of nelogical lesion in renal biopsies from children with idiophrosis in children. Recent studies have demonstrated an inpathic nephrotic syndrome [1, 2]. This observation was creasing incidence of focal segmental glomerulosclerosis (FSGS) in adults. confirmed by single centers that reported MCNS in al- Methods. To determine possible changes in the etiology of most 90% of cases [3]. The same studies showed that childhood nephrosis, the clinical charts of 152 pediatric patients focal segmental glomerulosclerosis (FSGS) was a rare diagnosed with idiopathic nephrotic syndrome between 1978 cause of nephrosis in children, observed in only 5 to 7% and 1997 were reviewed. Histopathological diagnosis was availof the biopsies [1 3]. More recent studies in adults have able in 105 patients. Results. MCNS was present in 35% of all biopsies, whereas reported an increasing incidence of FSGS during the last FSGS was observed in 31%. Even if we assume that all patients 20 years, accompanied by a significant decline in the without a histological diagnosis had MCNS (presumptive incidence of MCNS [4]. D Agati has suggested that FSGS MCNS), the total incidence of MCNS (biopsy proven preconstitutes the most common glomerulopathy observed sumptive) in our population was only 55%. We observed a dramatic increase in the incidence of FSGS during recent years. among biopsies performed in adult native kidneys [5]. Before 1990, FSGS was diagnosed in 23% of all renal biopsies Unfortunately, in the pediatric population, the only studbut increased to 47% afterward (P 0.02). This pattern was ies performed during the last 20 years have focused on observed in all ethnic groups. In African Americans, there was selected patient populations that were either steroid dea trend for an increase in the incidence of FSGS from 38% pendent or frequent relapsers. In 1981, Siegel et al rebefore 1990 to 69% after A similar trend was observed ported that FSGS was present in 29% of renal biopsies in Caucasians (from 20 to 45%) and Hispanics (from 8 to 33%). Hispanics had the highest incidence of MCNS (biopsy proven performed in children with steroid-dependent nephrotic presumptive: 73%), followed by Caucasians (53%) and African syndrome [6]. Trachtman and colleagues later observed Americans (37%). The mean age for presentation of nephrotic that MCNS was present in 25% of the biopsies persyndrome in African Americans ( years) was higher formed in pediatric patients with frequently relapsing, than in Caucasians ( ) and Hispanics ( ). steroid-sensitive nephrotic syndrome [7]. Conclusions. Our study showed that the incidence of FSGS It has been our impression that the incidence of FSGS in children with idiopathic nephrotic syndrome has increased recently. Furthermore, in African American children, FSGS is has increased in our practice during recent years. In the most common cause of nephrotic syndrome. These findings addition, in agreement with observations from other cen- may have significant implications in the management of child- ters, we have observed a marked predominance of FSGS hood nephrotic syndrome. among African American patients [8 10]. Recently, in a primarily Black population of adolescents with nephrotic syndrome, Baqi et al demonstrated that FSGS was the 1 See Editorial, p most common histological finding with an incidence of Key words: minimal change nephrotic syndrome, focal segmental glomerulonephritis, renal biopsy, childhood nephrosis. pediatric population in United Kingdom, Webb et al 55.2% [11]. Conversely, in a primarily White and Asian noted that MCNS was the most common histological Received for publication May 13, 1998 and in revised form November 20, 1998 diagnosis (80.4%), with only 13.7% of biopsies demon- Accepted for publication November 20, 1998 strating FSGS [12]. Because ethnicity seems to play a 1999 by the International Society of Nephrology key role in the epidemiology of nephrotic syndrome, the 1885
2 1886 Bonilla-Felix et al: Nephrotic syndrome in children results of these two studies could be limited by the racial increase in mesangial matrix and/or segmental cell prolifcomposition of their populations. eration was observed. FSGS was characterized by the This study reports our experience with pediatric idio- presence of at least one glomerulus showing a segmental pathic nephrotic syndrome during the last 20 years in a area of sclerosis with or without accompanying tubular racially mixed population of a major urban city in the atrophy and interstitial fibrosis. Thirty-two out of 33 United States. The demographic data and histopatholog- patients diagnosed with FSGS had three or more glomerical findings were reviewed. uli with segmental sclerotic lesions. Mesangial proliferative glomerulonephritis was defined by the presence of METHODS increased mesangial matrix and moderate to prominent mesangial cell proliferation (more than 4 cells per mesan- Patients gial area), in the absence of segmentally sclerosed glo- Between 1978 and 1997, 152 children with idiopathic meruli. Because of the controversies regarding the signephrotic syndrome were evaluated at University of nificance of IgM deposits in the mesangium, IgM Texas-Houston Health Science Center. Except for two nephropathy was not considered as a separate entity patients who had received therapy with prednisone for [14 16]. Therefore, patients with or without IgM deposits a week, the remaining patients were referred for nephro- by immunofluorescence microscopy were grouped tologic evaluation of edema or new diagnosis of nephrotic gether in this category. Patients who had mesangial syndrome, prior to commencing therapy. None of the changes accompanied by IgA deposits were included in patients had been biopsied before evaluation by the nea separate group (IgA nephropathy). Because it is our phrology service. Patients with systemic illnesses such as practice to treat most patients with corticosteroids prior systemic lupus erythematosus, Henoch-Schönlein purto kidney biopsy, a group of patients who readily repura, sickle cell anemia, malignancies, metabolic disorsponded to prednisone and had no or only occasional ders, or hepatitis or those who were receiving drugs assorelapses (31% of our population) was never biopsied. ciated with the onset of nephrotic syndrome were We defined this group of patients as presumptive MCNS, excluded. Indications for biopsy included steroid resisalthough we recognize that it might represent a more tance or dependence, frequent relapses, an age older heterogenous group of diseases. In patients who had had than eight years, or significant elevation in serum creatimore than one biopsy, the histopathological diagnosis nine at presentation. All patients were treated initially was assigned according to the results of the most recent with corticosteroids (prednisone) at a dose of 2 mg/kg/ day (maximum of 80 mg/day) for four to eight weeks. biopsy. None of the patients were treated with cytotoxics or Statistical analysis cyclosporine prior to kidney biopsy. Data from groups of patients are reported as mean Definitions se or as percentages (frequency of observation in a par- Nephrotic syndrome was defined as the association of ticular group). The statistical analysis was performed by heavy proteinuria with hypoalbuminemia and hyperchobetween chi-square test or analysis of variance for comparisons lesterolemia. The response to therapy was classified acfined multiple groups. Statistical significance was de- cording to the definitions from ISKDC: (a) steroid sensitive complete as a P resolution of proteinuria within eight weeks of prednisone therapy; (b) steroid resistance RESULTS failure to respond to eight consecutive weeks of treatment with prednisone at 2 mg/kg/day; (c) steroid depengroups: Caucasians (N 74, 49%), African Americans Our population was represented by three major ethnic dence recurrence of nephrosis when the dose of corticosteroids is reduced or within two months after the (N 30, 20%), and Hispanics (N 37, 24%). This was discontinuation of therapy; (d) frequent relapses two similar to the general composition of Houston s popula- or more episodes of nephrosis within six months of the tion: Caucasians, 40.6%; African Americans, 27.5%; and initial response or four or more within any 12-month Hispanics, 27.6% [17]. The mean age of our population period (not related to changes in prednisone dose) [13]. was (range of 1 to 20 years old), with a slight male predominance (57%). Hypertension, defined as Pathology blood pressure higher than the 95th percentile for age Renal tissue was examined by light, immunofluores- according to data from the Task Force Report on High cence, and electron microscopy and was interpreted by Blood Pressure in Children and Adolescents, was ob- our renal pathologists. Minimal change disease was charmore served in 21% [18]. Microscopic hematuria, defined as acterized by the absence of any conspicuous abnormality than five red blood cells per high-power field in on light microscopy. In some specimens, a very slight the initial urinalysis, was observed in 32% of the patients.
3 Bonilla-Felix et al: Nephrotic syndrome in children 1887 Table 1. Distribution of histopathological lesions Table 3. Distribution of histopathology by ethnicity All patients N (%) Biopsy specimens N (%) Caucasian African American Hispanic Histological lesion (N 152) (N 105) Histological lesion N (%) MCNS-Bx 37 (24%) 37 (35%) MCNS-Pres 47 (31%) MCNS-Bx 16 (22%) 7 (23%) 11 (30%) FSGS 33 (22%) 33 (31%) MCNS-Pres 23 (31%) 4 (13%) 16 (43%) Mesangial 26 (17%) 26 (25%) FSGS 13 (18%) 14 (47%) 4 (11%) MPGN 5 (3%) 5 (5%) Mesangial 16 (22%) 4 (13%) 4 (11%) IGA 2 (1%) 2 (2%) MPGN 4 (5%) 0 (0%) 1 (3%) Others 2 (1%) 2 (2%) IGA 1 (1%) 1 (3%) 0 (0%) Others 1 (1%) 0 (0%) 1 (3%) Abbreviations are: MCNS-Bx, biopsy-proven minimal change nephrotic syndrome; MCNS-Pres, presumptive minimal change nephrotic syndrome; Mesandrome; MCNS-Pres, presumptive minimal change nephrotic syndrome; mesan- Abbreviations are: MCNS-Bx, biopsy-proven minimal change nephrotic syngial, mesangial proliferative glomerulonephritis; MPGN, membranoproliferative glomerulonephritis; IGA, IgA nephropathy. gial, mesangial proliferative glomerulonephritis; MPGN, membranoproliferative glomerulonephritis; IGA, IgA nephropathy. Table 2. Changes in histopathology after 1990 it did not reach statistical significance Table 3). If the Histological Incidence Odds Confidence group of patients who were not biopsied (presumptive lesion Year N (%) ratio interval P value MCNS) were included in the analysis, the incidence of FSGS After (47%) , MCNS (presumptive biopsy proven) after 1990 (57%) Before (23%) did not differ from prior to 1990 (54%). MCNS-Bx After (25%) , Before (41%) Table 3 demonstrates the distribution of diagnosis Mesangial After (19%) , among the three major ethnic groups. FSGS was the Before (28%) most common diagnosis in African American children Abbreviations are: MCNS-Bx, biopsy-proven minimal change nephrotic syn- with nephrotic syndrome (47%). This was significantly drome; Mesangial, mesangial proliferative glomerulonephritis. higher than in Caucasian (18%, odds ratio 4.11, P 0.003) and Hispanic children (11%, odds ratio 7.22, P 0.003). When we limit the analysis to biopsy specimens (excluding patients with presumptive MCNS), the Table 1 shows the distribution of causes of nephrotic overall incidence of FSGS in African Americans (54%) syndrome in our population. Minimal change was pres- is still significantly higher than in Caucasians (25%, odds ent in only 35% of all biopsies performed. Even if we ratio 3.41, P 0.03) and Hispanics (19%, odds ratio assume that all children that were not biopsied had 4.96, P 0.03). Conversely, the highest incidence of MCNS (presumptive MCNS), the total incidence of MCNS (presumptive biopsy proven) was observed MCNS (presumptive biopsy proven) was 55%, which among Hispanic children (73%), followed by Caucasian differs from numbers previously reported by the Interna- children (53%), with the lowest being in African Ameritional Study of Kidney Disease in Children (ISKDC) cans children (36%), but these differences were not statistically [2]. By contrast, FSGS was observed in 31% of the biopsies significant. and accounted for 22% of all cases of nephrotic To determine if the increasing incidence of FSGS was syndrome. This is higher than predicted for a pediatric the result of changes in the racial composition of our group. Mesangial proliferative glomerulonephritis was population, we analyzed the ethnical distribution of our the third most common diagnosis, and was present in patients before and after The number of Caucasian 25% of the biopsies. patients evaluated for nephrotic syndrome in our center To determine whether the high incidence of FSGS declined from 58% prior to 1990 and 35% after Concurrently, the African American population increased was the result of an increasing trend during recent years, from 17 to 24%, and the number of Hispanic children we subdivided our group into patients who developed increased from 17 to 35%. Although not statistically signephrotic syndrome before 1990 and patients who prenificant, there was a trend for a higher incidence of FSGS sented on or after FSGS was the most common in all ethnic groups after 1990 (African Americans, 38 to histological lesion observed among the biopsies per- 69%; Caucasians, 20 to 45%; Hispanics, 8 to 33%). formed in patients presenting after 1990 (47%; Table Finally, the potential differences in diagnoses with age 2). This was significantly higher than in biopsies from of the patients were examined. We observed that the mean patients who presented prior to 1990 (23%, P 0.02). age of our population did not change between the two There was a tendency for a lower incidence of biopsy- time periods studied (before 1990, ; after 1990, proven MCNS and mesangial proliferative glomerulone years old, P 0.34). Furthermore, the median phritis (with and without IgM deposits) after 1990, but age for both time periods was the same (four years old),
4 1888 Bonilla-Felix et al: Nephrotic syndrome in children Table 4. Distribution of histopathology by age a higher incidence of FSGS is expected [6, 7]. Studies in Histological Age Incidence Odds Confidence adults have reported that the incidence of FSGS has lesion years N (%) ratio interval P value increased during recent years [4, 5]. MCNS 8 13 (35%) , Our results demonstrate a high incidence of FSGS in (Bx Pres) 8 75 (65%) our pediatric population with nephrotic syndrome. FSGS FSGS 8 18 (49%) , (13%) was identified as the cause of nephrotic syndrome in 22% Mesangial 8 2 (5%) of all pediatric patients evaluated in our center after (21%) This represents 31% of the biopsy specimens. This is the Abbreviations are: Bx Pres, biopsy-proven plus presumptive minimal highest incidence of FSGS ever reported in a pediatric change nephrotic syndrome; Mesangial, mesangial proliferative glomerulonepopulation. The odds of a diagnosis of FSGS in a biopsy phritis. specimen of a child with nephrotic syndrome in the current decade is almost three times higher than prior to This agrees with the pattern described in adult suggesting that the increased incidence in FSGS was not series [4, 5]. We believe that our observations represent result of an age increase in our population. The distribu- a true increase in the incidence of FSGS. Although our tion of diagnoses was subdivided into two age groups (less practice is established in a university-affiliated tertiary than eight years vs. more than eight years old). This age care center, it does not seem that our results were biased was chosen because it has been our limit to treat patients by selection of patients with more severe disease. None empirically with corticosteroids without histological diag- of our patients was referred to us for evaluation of stenosis. The causes of nephrotic syndrome in these groups roid-resistant or steroid-dependent nephrotic syndrome. were significantly different. As shown in Table 4, MCNS Furthermore, except for two patients who had been (presumptive biopsy proven) was more common in the treated with prednisone for a week, the rest of our payounger age group (less than eight years, 65%; more than tients were referred for evaluation of edema or new eight years, 35%, odds ratio 3.5, P 0.002). Similarly, onset nephrotic syndrome before treatment had been the incidence of mesangial proliferative glomerulonephri- commenced. Our findings are in accordance with prelimitis in children younger than eight years (21%) was signifi- nary data from Sorof et al, who reported FSGS as the cantly higher than in the older group (5%, odds ratio cause of proteinuria in 28% of pediatric patients in Hous- 4.62, P 0.05). By contrast, FSGS was significantly more ton (abstract; Sorof et al, J Am Soc Nephrol 8:98A, 1997). common in the older patients (49 vs. 13%, odds ratio Ethnicity seems to play a critical role in the epidemiol- 6.3, P ). Moreover, although the incidence of ogy of nephrotic syndrome. As previously reported by FSGS in patients older than eight years almost doubled others [8 11], we also observed a strong predominance after 1990 (63 vs. 33%, before 1990), it did not change in of FSGS among African Americans (Table 4). FSGS was the younger patients (14% before 1990 vs. 11% after the most common histological lesion observed in this 1990). In addition, a significant difference in the ages at ethnic group. African American children with nephrotic presentation was observed between the different ethnic syndrome have a seven times greater risk of having been groups. The mean age for presentation of nephrotic synthat diagnosed with FSGS than Hispanics. Indeed, we found drome in African American children ( years old) Hispanics had the lowest risk for FSGS and the was significantly higher than in Caucasians ( , P highest incidence of MCNS among the three racial 0.01) and Hispanics ( , P 0.001). groups analyzed. This finding differs from observations by Ingulli and Tejani, who reported that the incidence DISCUSSION of FSGS in Hispanic children with nephrotic syndrome in New York was higher than in Caucasians and not It has been widely accepted that MCNS is by far the different from Blacks [8]. Unfortunately, in this study, most common cause of nephrotic syndrome in children. the data of Hispanic children were not separated from The ISKDC reported almost 30 years ago that MCNS the African American group. This fact did not allow us was present in 77% of all renal biopsies performed in to compare the differences between these two Hispanic children with idiopathic nephrotic syndrome [1, 2]. Oth- populations. Nonetheless, it should be noted that our ers reported MCNS in up to 90% [3]. For years, these results agree with preliminary observations from our colobservations have guided the management of pediatric leagues in Houston, who reported no difference in the patients with nephrotic syndrome. More recent studies incidence of FSGS between Hispanic and Caucasian chilfrom Siegel et al and Trachtman et al have shown a dren with proteinuria (abstract; Sorof et al, JAmSoc higher incidence of FSGS in pediatric patients with ste- Nephrol 8:98A, 1997). The contrasting differences beroid-sensitive nephrotic syndrome. However, both of tween Ingulli s report and ours could be related to gethese studies focused on high-risk populations that were netic factors. The Hispanic population in New York was either steroid dependent or frequent relapsers, in which largely formed by Puerto Ricans and other Caribbean
5 Bonilla-Felix et al: Nephrotic syndrome in children 1889 immigrants, whereas in Houston, Mexicans and other nosis [20]. Although initially considered a resistant lesion, immigrants from Central America comprised the major- recent data suggest that more aggressive therapies can ity of the Hispanic group. induce a response in more than 50% of patients [21 24]. A potential explanation for this recent surge in FSGS Furthermore, patients who achieve remission have a sigcould be a change in the ethnic composition of our popu- nificantly improved clinical course [22]. We propose that lation. However, although there was a decline in the a biopsy, either at the onset of nephrotic syndrome in Caucasian population and a slight increase in the number patients at risk (older than eight years, African Ameriof African American children in our group during the cans) or early during the clinical course if problems with study period, the major demographic change observed response to therapy are identified, will be beneficial in was an almost doubling in the number of Hispanic pa- the management of these patients. tients after This correlates with the demographic changes occurring in Houston. Figures from the U.S. ACKNOWLEDGMENTS census for the city of Houston show that the Caucasian The authors thank Dr. Barbara R. Cole for critically reviewing this population in Harris County has decreased from 52.3% manuscript and our nurse, Ms. Patricia Brannan, for assistance in the in 1980 to 40.6% by Conversely, the Hispanic popuabstract form at the 30th Annual Meeting of the American Society of clinical management of these patients. This work was presented in lation increased from 17.6 to 27.6%. The African Ameri- Nephrology. can population has been stable at approximately 27% [17]. Because we have shown that the incidence of FSGS Reprint requests to Melvin Bonilla-Felix, M.D., Pediatric Nephrolis the lowest in the Hispanic group, it is unlikely that ogy, University of Texas, Houston Health Science Center, 6431 Fannin Street, Houston, Texas 77030, USA. changes in the racial composition of our population could mbonilla@ped1.med.uth.tmc.edu completely account for our findings. Another consideration for the rise in the incidence of REFERENCES FSGS is a potential increase in the age of patients re- 1. 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