Follow-up of patients with epidemic poststreptococcal glomerulonephritis

Follow-Up of Patients With Epidemic Poststreptococcal Glomerulonephritis Sergio Wyton L. Pinto, MD, Ricardo Sesso, MSc, Edson Vasconcelos, MD, Yoshimi J. Watanabe, MD, and Agreine M. Pansute, MD ● In 1998 there was a large outbreak of acute glomerulonephritis (GN) in Nova Serrana, Brazil, caused by group C Streptococcus zooepidemicus and linked to the consumption of contaminated cheese produced with unpasteurized milk. This study describes the follow-up of these patients after a mean of 2 years following the acute episode. Of 134 patients identified in 1998, 69 patients were reexamined and underwent measurements of blood pressure, 24-hour creatinine clearance, microalbuminuria (radioimmunoassay), and urine sediment analysis. Of the original group of 134 patients, 3 patients died in the acute phase and 5 patients (3.7%) required chronic dialysis. Of 69 patients reevaluated, 65 patients (94%) were adults (mean age, 39 ⴞ 2 [SE] years) and 47 patients (68%) were women. At the follow-up examination, we found arterial hypertension in 42% of subjects (27 of 64 subjects), serum creatinine levels greater than 1.2 mg/dL in 12% (10 of 68 subjects), reduced creatinine clearance (<80 mL/min/1.73 m2) in 30% (20 of 67 subjects, 2 of them on chronic dialysis therapy), and increased microalbuminuria (>20 ␮g/min) in 34% (22 of 65 subjects). Increased microalbuminuria and/or reduced creatinine clearance were detected in 48% of the subjects (31 of 65 subjects). Patients with microalbuminuria had greater diastolic blood pressure than those without microalbuminuria (mean, 98 ⴞ 4 versus 88 ⴞ 2 mm Hg; P ⴝ 0.02). In conclusion, after a mean of 2 years, patients with epidemic poststreptococcal GN caused by S zooepidemicus present a high rate of hypertension and frequent abnormalities of renal function, with some having reached end-stage renal disease. Longer follow-up will be important to define the prognosis of these patients. © 2001 by the National Kidney Foundation, Inc. INDEX WORDS: Poststreptococcal glomerulonephritis (PSGN); epidemic nephritis; acute nephritis; Streptococcus zooepidemicus; follow-up.

W

E RECENTLY described a large outbreak of acute glomerulonephritis (GN) that occurred from December 1997 to July 1998 in Nova Serrana, Brazil.1 Throat cultures indicated the nephritis was associated with Lancefield group C Streptococcus zooepidemicus, a cause of bovine mastitis. Epidemiological investigation showed that patients had consumed a locally produced cheese prepared with unpasteurized milk. Two hundred fifty-three cases of GN (⬎90% adults) were reported in the region. In the 1950s and 1960s, large outbreaks of poststreptococcal GN (PSGN) that predominantly affected children were reported in association with certain strains of group A Streptococcus species.2-5 In Romania in 1968, 28 cases of GN linked to S zooepidemicus infection were reported.6 Outbreaks of PSGN have been rare since the 1970s. This report describes the follow-up of patients with epidemic nephritis caused by S zooepidemicus reevaluated after a mean of 2 years after the acute episode. METHODS From December 1997 to July 1998, 253 cases of GN were reported in the center-west region of the state of Minas Gerais, Brazil. Most patients resided in Nova Serrana (population, 27,500), regional health district of Divino´polis. The

outbreak was previously described in detail.1 The clinical syndrome began with fever, headache, and myalgia, followed by cervical adenopathy. After 7 to 10 days, patients developed GN with oliguria, hematuria, generalized edema, and hypertension. In July 1998, for the purpose of epidemiological investigation, case registration, and monitoring, the authors reviewed inpatient charts for patients at the Hospital Sa˜o Jose´ in Nova Serrana with discharge codes for nephritis from January to July 1998 and inpatient and outpatient charts for the same period for patients examined by nephrologists at Hospital Sa˜o Joa˜o de Deus in Divino´polis. These were the two health services patients were referred to. An outbreak-related case of nephritis was defined as the presence of at least two of the following symptoms: systolic blood pressure greater than 140 mm Hg or diastolic blood pressure greater than 90 mm Hg for adults and blood pressure greater than the 95th From the Division of Nephrology, Hospital Sa˜o Joa˜o de Deus, Divino´polis; and the Division of Nephrology, Escola Paulista de Medicina, Universidade Federal de Sa˜o Paulo, Sa˜o Paulo, Brazil. Received November 20, 2000; accepted in revised form March 9, 2001. Supported in part by a research grant from the Brazilian Research Council (R.S.). Address reprint requests to Ricardo Sesso, MD, Division of Nephrology, Escola Paulista de Medicina, Unifesp, Rua Botucatu 740, Sa˜o Paulo, SP, Brazil, 04023-900. E-mail: [email protected] © 2001 by the National Kidney Foundation, Inc. 0272-6386/01/3802-0003$35.00/0 doi:10.1053/ajkd.2001.26083

American Journal of Kidney Diseases, Vol 38, No 2 (August), 2001: pp 249-255

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percentile of the age-specific normal limit for children, edema, and at least trace hematuria or proteinuria with 30 mg/dL of protein. Of 152 possible cases of outbreak-related illness indicated by the diagnostic coding of the local physicians, 18 cases did not meet the strict case definition. Of 134 confirmed cases, 120 patients (90%) were adults, 97 patients (72%) were hospitalized, 124 of 126 patients (98%) had edema, all patients had hematuria, 57 of 98 patients (58%) had serum creatinine levels greater than 1.2 mg/dL, and 10 of 12 patients (83%) were found to have low concentrations of serum C3 complement None had nephrotic syndrome. Renal biopsy specimens obtained from 9 patients showed diffuse proliferative glomerular disease consistent with PSGN. In a case-control study, cultures of throat specimens collected from patients and cheese-makers yielded group C S zooepidemicus.1 This agent was not isolated in any culture from control households. During 2 weeks in May 2000, we attempted to contact all patients registered in our files (n ⫽ 134) seen during the epidemic. Patients were visited in their homes by two of the coauthors and members of the regional health district of Divino´polis. During the visit, a recently voided urine sample was collected for sediment examination and a protein dipstick test (Combur10-Test M; Roche, Mannheim, Germany) was performed, a blood sample was drawn (usually after fasting), an interim history was obtained, and a physical examination (including patients’ height and weight) was performed. Blood pressure was measured with a mercury sphygmomanometer in the sitting position after 5 minutes of rest. The average of three measurements taken at 1-minute intervals was used in the analysis. Hypertension was defined as systolic blood pressure greater than 140 mm Hg or diastolic blood pressure greater than 90 mm Hg for adults and blood pressure greater than the 95th percentile of the age-specific normal limit for children. The patient was then carefully instructed in how to collect 24-hour urine for analysis. A container was left with the patient for urine collection, and study personnel returned the next day (after 24 hours) to pick up the container and check the duration of collection. All patients were revisited after an interval of 2 weeks for a second 24-hour urine collection. Blood and urine samples were appropriately stored at 4°C and brought to the reference study laboratory in Divino´polis. When examined within 1 day, urine samples were kept at 4°C; otherwise, they were frozen at –20°C. Urine samples from 24-hour collections were tested for microalbuminuria and creatinine. Blood samples were examined for serum creatinine (alkaline picrate method) and serum urea (urease method) using a spectrophotometer (E-225D, 1995; Companhia de Equipamentos de Laboratorios Modernos, Sa˜o Paulo, Brazil). For analysis of creatinine clearance (corrected for 1.73 m2 of body surface area) and microalbuminuria, the average of two measurements obtained after a 2-week interval was used. Microalbuminuria was assessed by radioimmunoassay using gamma counter equipment (Gamma C12, 1997; Diagnostic Products Corporation, Los Angeles, CA), and values greater than 20 ␮g/min were considered abnormal. Glomerular filtration rate (GFR) was considered reduced when creatinine clearance was less than 80 mL/min/ 1.73 m2. Urine and blood analyses were performed at the reference study laboratory in Divino´polis, and microalbumin-

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uria was tested at the reference laboratory in the city of Belo Horizonte. The patients on this study had no clinical evidence or history indicating previous renal disease.

Statistical Analysis Chi-square or Fisher’s exact test was used for the comparison of categorical variables. Student’s t-test or MannWhitney test (when appropriate) was used for the comparison of continuous variables. Tests were two-sided, and statistical significance was set at P less than 0.05.

RESULTS

During our attempt to contact patients for the follow-up study in May 2000, of the 134 patients with confirmed PSGN seen in 1998, 3 patients had died in the acute phase of illness, 46 patients could not be located, 10 patients did not agree to undergo medical reevaluation, 3 patients were on chronic dialysis therapy in another city, and 3 patients died (after resolution of the acute illness) of an underlying cause not related to renal disease. Sixty-nine subjects were reevaluated in the present study after a mean of 24 months (range, 20 to 27 months; Fig 1). These patients did not differ from those not reexamined regarding several characteristics at presentation, such as mean age, sex, hospitalization rate, presence of edema, mean systolic and diastolic blood pressures, serum urea and creatinine levels, and need for dialysis. Of the 134 patients, 10 patients required dialysis during the acute phase of illness. Three of these patients died within 1 month of disease. Three patients recovered renal function and discontinued dialysis therapy between 2 and 10 weeks. Four of these patients remained on chronic dialysis therapy. One additional patient started dialysis for chronic renal failure 8 months after the onset of disease. In July 2000, after checking with the dialysis centers of the region, we confirmed that no other subject of the original sample (n ⫽ 134) started chronic dialysis treatment within this period. Furthermore, it is very likely that if any of our patients had started dialysis therapy elsewhere, we would have been informed. Table 1 lists initial characteristics during the acute episode for the 69 patients who were reexamined. Mean age was 39 ⫾ 2 (SE) years (range, 8 to 81 years); 94% were aged older than 15 years. The majority were women and required

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251

Fig 1. Flow chart of study patients.

hospitalization. Systolic and diastolic hypertension occurred in 70% and 64% of the patients, respectively. Ten patients (14.5%) were taking antihypertensive drugs on admission for the treatment of previously diagnosed hypertension. Increased serum creatinine (⬎1.2 mg/dL) and seTable 1.

Baseline Characteristics of Patients

Characteristic

Age (y) ⬍15 ⬎60 Sex Female Male Hospitalization Edema Dialysis Peak systolic blood pressure (mm Hg) ⬎140 Peak diastolic blood pressure (mm Hg) ⬎90 Serum creatinine (mg/dL) ⬎1.2 Serum urea (mg/dL) ⬎45

No. Available*

39 ⫾ 2 4 (6) 7 (10)

69

69 47 (68) 22 (32) 52 (75) 67 (100) 5 (7)

69 67 69

161 ⫾ 3 47 (70)

67

102 ⫾ 2 43 (64) 1.6 (0.6-20.0) 34 (62) 63 (14-182) 32 (63)

67 55 51

NOTE. Values expressed as mean ⫾ SE, number (percent), or median (range). *Patients for whom finding was reported in the medical chart.

rum urea (⬎45 mg/dL) levels were detected in 62% and 63% of the subjects, respectively. Five patients required dialysis. Hematuria (⬎10 red blood cells/field of original magnification ⫻400) was present in all subjects. Blood pressure measurements and laboratory parameters at follow-up are listed in Table 2. Two patients remained on chronic dialysis therapy. High systolic or diastolic blood pressure was detected in 27 of 64 individuals (42%). Overall, 20 subjects (29.0%) were administered antihypertensive drugs. Serum creatinine levels were greater than 1.2 mg/dL in 10 of 68 patients (12%), and creatinine clearances were less than 80 mL/min/1.73 m2 in 20 of 67 patients (30%). Excluding the 2 patients on dialysis therapy, the minimum creatinine clearance value was 48 mL/ min/1.73 m2. Hematuria was present in 10% of the patients. Three of 63 patients (5%) had proteinuria (trace or ⫹) by dipstick; none had nephrotic syndrome. Increased microalbuminuria was detected in 22 of 65 patients (34%; 2 subjects on dialysis therapy were not tested for microalbuminuria). Of the 65 patients in whom microalbuminuria and creatinine clearance were tested, 9 patients (14%) had both test results concomitantly altered, 13 patients (20%) had isolated microalbuminuria, and 9 patients (14%) had only reduced creatinine clearances. Thirty-one of the 65 sub-

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PINTO ET AL Table 2.

Patient Characteristics and Laboratory Parameters at Follow-Up No. Available*

Characteristic

Mean duration of follow-up (mon) Dialysis Systolic blood pressure (mm Hg) ⬎140 Diastolic blood pressure (mm Hg) ⬎90 Median serum urea (mg/dL) ⬎45 Median serum creatinine (mg/dL) ⬎1.2 Median creatinine clearance (mL/min/1.73 m2) ⬍80 Hematuria ⱖ 10 cells/field ⫻ 400 Leukocyturia ⱖ 10 cells/field ⫻ 400 Median microalbuminuria (␮g/min of albumin) ⬎20 Microalbuminuria with albumin ⬎ 20 ␮g/min or creatinine clearance ⬍ 80 mL/min/1.73 m2

24.6 (20.3-27.0) 2 (3) 145 ⫾ 4 25 (39) 91 ⫾ 2 21 (33) 31 (16-190) 8 (12) 1.0 (0.4-14.1)† 10 (12) 90 (0-133)† 20 (30) 6 (10) 6 (10) 11.4 (1.7-461.0) 22 (34) 31 (48)

69 69 64 64 65 68 67 63 63 65 65

NOTE. Values expressed as mean ⫾ SE, mean or median (range), and number (percent). *Number of patients with available information. †Excluding two patients on dialysis therapy, the maximum value for serum creatinine was 1.6 mg/dl and the minimum value for creatinine clearance was 48 mL/min/1.73 m2.

jects (48%) had at least one of these test results altered. Forty-five of 67 patients (67%) presented with at least one of the following abnormalities: increased microalbuminuria, reduced creatinine clearance, or arterial hypertension. Subjects with microalbuminuria (n ⫽ 22) had greater mean systolic (152 ⫾ 7 versus 141 ⫾ 5 mm Hg; P ⫽ not significant) and diastolic blood pressures (98 ⫾ 4 versus 88 ⫾ 2 mm Hg, respectively; P ⫽ 0.02) at follow-up than those without microalbuminuria (n ⫽ 43). The groups with and without microalbuminuria did not differ significantly regarding other variables tested (age, sex, hospitalization, presence of edema, baseline blood pressure, serum creatinine level at presentation, and creatinine clearance at follow-up). Patients with reduced creatinine clearance (n ⫽ 20) were older (age, 45 ⫾ 3 versus 36 ⫾ 2 years; P ⫽ 0.05), had more frequently undergone dialysis (n ⫽ 4 [20%] versus n ⫽ 1 [2%]; P ⫽ 0.03), presented with greater mean systolic blood pressures in the acute phase of illness (174 ⫾ 7 versus 155 ⫾ 3 mm Hg; P ⫽ 0.03), and had greater median microalbuminuria levels at follow-up (19 versus 10 ␮g/min; P ⫽ 0.06) than the group with normal creatinine clearance values.

Other variables tested did not differ significantly between the groups. DISCUSSION

S equi subspecies zooepidemicus is rare in humans, but is a well-known cause of disease in cows and horses.7 In humans, S zooepidemicus can cause PSGN8 and other syndromes.9-12 Four previous outbreaks attributed to S zooepidemicus have been reported, with illness presenting as PSGN in two outbreaks6,8 and as sepsis or meningitis in the other two outbreaks.13,14 Consumption of unpasteurized milk or milk products was implicated as the source of infection in all four outbreaks. We described a large outbreak of PSGN that occurred in 1998 in Nova Serrana caused by S zooepidemicus and linked to the consumption of cheese produced with unpasteurized milk.1 S zooepidemicus was isolated from throat cultures of case-patients, farm workers, and cheesemakers. In addition, to confirm that outbreakstrain proteins were expressed during infection, we amplified and sequenced the outbreak strain S zooepidemicus M-like protein gene (szp1) and

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documented positive case-patient serological response to the outbreak-specific M-like protein.15 Unlike the more common PSGN attributed to group A streptococcus, which affects children, this and other outbreaks of GN caused by S zooepidemicus predominantly affected adults.6,8 There is no explanation for the unusual age distribution seen in GN caused by this microorganism. In the original study, we surveyed 50 adults and 50 children about their consumption of queijo fresco. Different patterns of cheese consumption did not seem to account for the greater attack rates among adults (unpublished data). Such host factors as age-related immunologic susceptibility may have contributed to the onset of PSGN in Nova Serrana. The largest previous outbreak associated with S zooepidemicus occurred in Romania in 1968.6 Of 85 patients (87% adults) with sore throat and lymphadenitis, one third developed GN. Two patients showed nephrotic edema 7 months after the acute phase of illness. In another report, three cases of nephritis after mild upper-respiratory tract infection occurred in members of a family in North Yorkshire, UK.8 No further details about the follow-up of these patients were given. Previous reports of acute PSGN were basically associated with group A streptococcus.2,3,5,16 Of these, three large epidemic episodes have been well described. In 1953, in Red Lake, Minnesota, 63 cases of PSGN, 96% in children, were reported.2,17 After a 10-year follow-up, none developed end-stage renal disease (ESRD) and 18% had urinary abnormalities. In Trinidad from 1964 to 1966, there were 760 cases of PSGN (510 epidemic, 250 endemic), mainly in children.3,18 Complete recovery occurred in more than 95% of patients and none had ESRD after 12 to 17 years. In Maracaibo, Venezuela, in 1968, of 384 detected cases (85% children), persistent urinary and renal function abnormalities were seen in 21% after 11 to 12 years.16,19 In the present outbreak of GN, illness was severe at presentation. Of 134 patients initially identified, 3 patients (2.2%) died, 72% had been hospitalized, 10 patients (7.5%) required dialysis, 58% had serum creatinine levels greater than 1.2 mg/dL, and more than 85% had hypertension. Baseline characteristics of the 69 patients

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followed up in this report did not differ from the overall group of 134 individuals. During follow-up, hypertension and urinary abnormalities were more frequently detected in this series than in other outbreaks of PSGN associated with group A streptococcus.16-19 It was remarkable that hypertension was observed in 42% of the patients, a considerably greater proportion than that reported for epidemic PSGN (2%).18 However, at least two other series of sporadic PSGN in adults have reported high rates of hypertension: 29%20 and 42%21 after more than 2 years of follow-up. The prevalence of hypertension during follow-up was clearly greater than would be expected for adults (age, 15 to 50 years) in Brazil (18.1%).22 Moreover, the proportion of patients administered antihypertensive drugs on follow-up was significantly greater than on admission. Although total proteinuria was uncommon and no patient had nephrotic syndrome, microalbuminuria was detected in 34% of the patients. Microalbuminuria correlated with high blood pressure at follow-up. Only one previous report assessed microalbuminuria in patients with PSGN.23 Buzio et al23 detected microalbuminuria in 9 of 26 patients (35%) with sporadic PSGN, with renal biopsy showing diffuse mesangial proliferation after a mean follow-up of 10 years. It was notable that several of our patients had microalbuminuria without a reduced creatinine clearance, indicating that glomerular damage may exist in the absence of reduced GFR and may eventually precede it. Conversely, reduced GFR was also observed in patients without microalbuminuria. This suggests that in some cases, low GFR may not be related to increased glomerular permeability to albumin. Reduced GFR measured by creatinine clearance was detected in 30% of the patients and was associated with older age, need for dialysis, and greater systolic blood pressure at presentation. It is noteworthy that 4 patients required chronic dialysis since the onset of disease and 1 additional patient started dialysis therapy for ESRD 8 months after the acute phase (5 of 134 patients; 3.7%). In the literature, although the short-term prognosis of GN caused by group A streptococci is excellent with an early mortality rate of approximately 0.5%,24 the long-term prognosis has

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remained controversial. Several research groups reported a very good long-term prognosis, mainly in epidemic cases17,18 and children.25,26 The chance of having ESRD has been less than 1% in 10 years.24 Other factors, such as presentation with nephrotic syndrome20,25,27 and renal histological findings shortly after onset, have also been suggested as predictors of outcome.26-28 In Maracaibo, of 120 patients with epidemic and sporadic PSGN followed up for 5 to 6 years, 8% of the overall group and 26% of the adults (5 of 19 adults) had a reduced creatinine clearance (⬍70 mL/min/1.73 m2).16 Medium- to long-term prognosis in adults with sporadic PSGN seems to be less favorable,16,21,29 with chronic renal disease reaching 50% of the patients in 2 to 15 years of follow-up in the series of Baldwin et al21 (11 of 126 patients had ESRD). However, the worse prognosis in the latter series might reflect bias in patient selection, the diagnosis of PSGN, and criteria used to define progression to chronicity. It has been shown that histological resolution may not occur in some patients for up to 9 years after the attack of PSGN.26,28,29 There are a number of difficulties and possible biases in the comparison of follow-up studies of PSGN and the interpretation of their validity. Studies have included both episodic and epidemic disease, as well as patients with a variety of social, geographic, and ethnic backgrounds and variable rates of hospitalization, degrees of proteinuria, and severity at presentation. Moreover, different criteria may have been used to define PSGN and progression to chronicity. Renal biopsy is usually not performed if patients do not have clinical and/or laboratory abnormalities. Reliable methods of GFR measurement and sensitive indicators of glomerular impairment have not been used. In particular, the possibility of superimposed renal disease before presentation with PSGN is very difficult to exclude. The case ascertainment methods used in the earlier phase of the present outbreak would not have identified most illness that did not result in hospital admission or referral to a nephrologist. Therefore, we may have studied cases with more severe symptoms and presentation. In conclusion, after a mean follow-up of 2 years, patients with epidemic PSGN caused by S zooepidemicus present with frequent abnormali-

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ties of renal function and a high rate of hypertension. Longer follow-up of this cohort will be important for knowledge of the natural history of the disease, rate of progression toward ESRD, and assessment of the long-term prognostic value of microalbuminuria. REFERENCES 1. Balter S, Benin A, Pinto SWL, Teixeira L, Alvim GG, Luna E, Jackson D, LaClaire L, Elliott J, Facklam R, Schuchat A: Epidemic nephritis in Nova Serrana, Brazil. Lancet 355:1776-1780, 2000 2. Kleinman H: Epidemic acute glomerulonephritis at Red Lake. Minnesota Med 37:479-483, 1954 3. Poon-King T, Mohammed I, Cox R, Potter EV, Simon NM, Siegel AC, Earle DP: Recurrent epidemic nephritis in South Trinidad. N Engl J Med 277:728-733, 1967 4. Kodama T, Miyamoto Y, Kotake I, Ochiai S: Epidemic nephritis in Japan. Yokohama Med Bull 9:105-118, 1958 5. Rammelkamp CH, Stetson CA, Krause RM, Perry WD, Kohen RJ: Epidemic nephritis. Trans Assoc Am Phys 17:276-282, 1954 6. Duca E, Teodorovici G, Radu C, Vita A, TalasmanNiculescu P, Bernescu E, Feldi C, Rosca V: A new nephritogenic streptococcus. J Hyg 67:691-698, 1969 7. Woolcock JB: Epidemiology of equine streptococci. Res Vet Sci 18:113-114, 1975 8. Barham M, Thorton TJ, Lange K: Nephritis caused by Streptococcus zooepidemicus (Lancefield group C). Lancet 1:945-948, 1983 9. Barham M, Ljunggren A, McIntyre M: Human infection with Streptococcus zooepidemicus (Lancefield group C): Three case reports. Epidemiol Infect 98:183-190, 1987 10. Ferrandiere M, Cattier B, Dequin PF, Hazouard E, Legras A, Perrotin D: Septicemia and meningitis due to Streptococcus zooepidemicus. Eur J Clin Microbiol Infect Dis 17:290-291, 1998 11. Rose HD, Allen JR, Witte G: Streptococcus zooepidemicus (group C) pneumonia in a human. J Clin Microbiol 11:76-78, 1980 12. Collazos J, Echevarria MJ, Ayarza R, Miguel J: Streptococcus zooepidemicus septic arthritis: Case report and review of group C streptococcal arthritis. Clin Infect Dis 15:744-746, 1992 13. Centers for Disease Control and Prevention: Group C streptococcal infections associated with eating homemade cheese, New Mexico. MMWR Morb Mortal Wkly Rep 32:510-516, 1983 14. Edwards AT, Roulson M, Ironside MJ: A milk-borne outbreak of serious infection due to Streptococcus zooepidemicus (Lancefield group C). Epidemiol Infect 101:43-51, 1988 15. Nicholson ML, Ferdinand LR, Sampson JS, Benin A, Balter S, Pinto SWL, Dowell S, Facklam RR, Carlone GM, Beall B: Analysis of immunoreactivity to a Streptococcus equi subsp. zooepidemicus M-like protein to confirm an outbreak of post-streptococcal glomerulonephritis, and sequences of M-like proteins from isolates obtained from different host species. J Clin Microbiol 38:4126-4130, 2000

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16. Rodriguez-Iturbe B, Garcia R, Rubio L, Cuenca L, Treser G, Lange K: Epidemic glomerulonephritis in Maracaibo. Evidence for progression to chronicity. Clin Nephrol 5:197-206, 1976 17. Perlman LV, Hederman RC, Kleinman H, Vernier RL: Poststreptococcal glomerulonephritis. A 10-year follow-up of an epidemic. JAMA 194:175-182, 1965 18. Potter EV, Lipschultz AS, Abidh S, Poon-King T, Earle AP: Twelve to seventeen-year follow-up of patients with poststreptococcal acute glomerulonephritis in Trinidad. N Engl J Med 307:725-729, 1982 19. Garcia R, Rubio L, Rodriguez-Iturbe B: Long-term prognosis of epidemic poststreptococcal glomerulonephritis in Maracaibo: Follow-up studies 11-12 years after the acute episode. Clin Nephrol 15:291-298, 1981 20. Vogl W, Renke M, Mayer-Eichberger D, Schmitt H, Bohle A: Long-term prognosis for endocapillary glomerulonephritis of poststreptococcal type in children and adults. Nephron 44:58-65, 1986 21. Baldwin DS, Gluck MC, Schacht RG, Gallo G: Long-term course of poststreptococcal glomerulonephritis. Ann Intern Med 80:342-258, 1974 22. Ribeiro MBD, Ribeiro AB, Neto CS, Chaves CC, Kater CE, Iunes M, Saragoc¸a MAS, Zanella MT, Anc¸a˜o MS, Marson O, Kohlmann O, Franco RJS, Nunes SF, Ramos OL:

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Hypertension and economic activities in Sa˜o Paulo, Brazil. Hypertension 3:S233-S237, 1981 (suppl II) 23. Buzio C, Allefri S, Mutti A, Perazzoli F, Bergamaschi E: Significance of albuminuria in the follow-up of acute poststreptococcal glomerulonephritis. Clin Nephrol 41:259264, 1994 24. Rodriguez-Iturbe B: Epidemic poststreptococcal glomerulonephritis. Kidney Int 25:129-136, 1984 25. Dodge WF, Spargo BH, Travis LB, Srivastava RN, Carvajal HF, DeBeukelaer MM, Longley MP, Menchaca JA: Poststreptococcal glomerulonephritis. A prospective study in children. N Engl J Med 286:273-278, 1972 26. Travis LB, Dodge WF, Beathard GA, Spargo BH, Lorentz WB, Carvajal HT, Berger M: Acute glomerulonephritis. A review of the natural history with emphasis on prognosis. Clin Nephrol 1:169-181, 1973 27. Hinglais N, Garcia-Torres R, Kleinknecht D: Longterm prognosis in acute glomerulonephritis. The predictive value of early clinical and pathologic features observed in 65 patients. Am J Med 56:52-60, 1974 28. Lien JWK, Mathew TH, Meadows R: Acute poststreptococcal glomerulonephritis in adults: A long-term study. Q J Med 48:99-111, 1979 29. Schacht RG, Gluck MC, Gallo GR, Baldwin DS: Progression to uremia after remission of acute postreptococcal glomerulonephritis. N Engl J Med 295:977-981, 1976