Nephrol Dial Transplant (1999) 14: 1889-1897
© 1999 European Renal Association-European Dialysis and Transplant Association
The epidemiology and prognosis of glomerulonephritis in Denmark 1985–1997
1 Departments of Nephrology and 2 Pathology, Herlev Hospital, University of Copenhagen, Denmark
Correspondence and offprint requests to: James Heaf, Graevlingestien 9, 2880 Bagsvaerd, Denmark.
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Abstract |
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Background. The existence of a national renal biopsy register and a national terminal uraemia status register in Denmark provides an opportunity to study the prognosis of glomerulonephritis (GN), and factors influencing prognosis.
Methods. Multivariate analysis of 2380 renal biopsies with GN performed between 1985 and 1997 was done to determine the influence of clinical and histological factors on prognosis.
Results. The incidence of GN (39/mio/year) and individual diagnoses did not change during the period. After 10 years, 32% were dead, 13% terminally uraemic, 5% uraemic and 50% well. Older age increased mortality, but not the incidence of renal failure after the first year. Male sex increased both mortality and incidence of renal failure (34 vs 24% at 10 years, P<0.001). The diagnoses could be divided into three prognostic groups compared with the general population: a good prognostic group (minimal change GN and membranous GN), with a relative mortality of three and a combined renal and patient mortality of four; a poor prognostic group [crescentic GN, HUS/TTP, chronic GN] with relative mortalities of 8–19 and 13–33, respectively; and the remainder with mortalities of 4–7 and 6–12. The presence of multiple glomerular pathology, chronic GN, nephrosclerosis and chronic interstitial nephropathy worsened the prognosis, while the presence of immune deposits only worsened the prognosis of focal segmental glomerulopathy. Mortality was related to uraemia and co-morbidity at biopsy, and to the incidence of renal failure. Renal failure was correlated to uraemia and hypertension at biopsy but not to nephrotic syndrome or atherosclerosis. All vascular complications were increased and were positively related to hypertension and negatively correlated to the incidence of uraemia. Crescentric glomerulonephritis combined with anti-GBM disease had a worse prognosis than Wegener's granulomatosis, with microscopic polyangiitis and pauci-immune disease occupying an intermediate position. The prognosis of mesangioproliferative GN was unaffected by the presence of IgA nephropathy and systemic lupus erythematosus.
Keywords: glomerulonephritis; immunofluorescence; uraemia; dialysis; lupus nephritis; Wegener's granulomatosis
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Introduction |
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Glomerulonephritis (GN) is a rare disease, with a large number of sub-classifications, and most nephrology centres will only meet a small number of patients per year with each type. Reliable prognostic information therefore requires excessively long follow-up periods or multicentre investigations. The existence of a national renal biopsy register (DANYBIR) in Denmark provides an opportunity to study the prognosis of GN and to determine the existence of prognostic factors. A recent questionnaire (personal communication) of 11 of the 15 referral centres, weighted for biopsy activity, showed that the first line treatment of the following glomerular diseases is uniform in Denmark: endocapillary GN is treated symptomatically; minimal change GN (MCGN) with steroids; crescentic GN (Cresc) with steroids, cyclophosphamide and often plasmapheresis (37%); haemolytic uraemic syndrome and thrombotic thrombocytopenic purpura (HUS/TTP) with plasmapheresis; lupus nephritis (WHO 3 and 4) with steroids and pulse cyclophosphamide; and chronic GN symptomatically. The treatment of other forms for GN is heterogenous; only a minority [membranous GN (Mem) 20%, membranoproliferative GN (Mes-P) 36%, mesangioproliferative GN (Mem-P) 36%, focal segmental glomerulopathy (FSGN) 43%)] treated primarily with immunosuppressive therapy (most commonly steroids and cyclophosphamide or azathioprine), the remainder reserving a trial for occasional patients with severe nephrosis or progressive renal failure.
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Patients
Data from the following four patient databases were linked to describe the epidemiology and prognosis of GN. (i) The Danish Renal Biopsy Register (DANYBIR). This register contains details of all renal biopsies examined by renal pathologists affiliated to Danish nephrology departments and, therefore, contains virtually all renal biopsy data in Denmark from 1985 to 1997, a period of 11.7 years. For each biopsy, the register contains patient age, sex, date of biopsy, up to four histological diagnoses using the WHO classification [1] and the presence of immune deposits. The following supplementary information is voluntary: presence of clinical systemic disease [e.g. systemic lupus erythematosus (SLE), diabetes]; clinical nephrological data (e.g. proteinuria, nephrotic syndrome, hypertension); and renal function (normal, azotaemia or uraemia). The register has been validated [2] and shown to have a high degree of internal consistency. (ii) The Danish Society of Nephrology Terminal Uraemia Status Register (TUS) contains data concerning every patient in Denmark receiving active treatment for terminal uraemia, and forms the basis of the Danish EDTA register. The register contains the renal diagnosis using standard EDTA terminology and the date of start of active treatment (dialysis or transplantation). Conservative treatment of terminal uraemia is related to patient age, being very rare below 70 years and common above 80 years. Active treatment of patients aged 70–80 years increased dramatically during the period of observation [3] and the register therefore contains details of the large majority of patients experiencing terminal uraemia. (iii) The Danish Population Register contains the date of death or emigration for all Danish inhabitants. The background population at ~5.2 million and the life expectancy remained virtually unchanged during the period of observation [4]. (iv) The Patient Admission Register (LPR) contains hospital admission data since 1977 together with date of admission, date of discharge and WHO ICD discharge diagnoses.
Patients were included in the investigation if they were in the DANYBI register and had one of the following diagnoses: normal (assumed to be MCGN), FSGN, Mes-P, Mem, Mem-P, focal GN, Cresc, HUS/TTP or chronic GN. For the analysis of systemic diseases, a group of patients with systemic disease and non-glomerular diseases was included.
Methods
The following data was registered: patient age, sex, biopsy date, death date, terminal uraemia date and primary glomerular diagnosis. The presence of other histological features was noted as secondary diagnoses: multiple glomerular disease, chronic GN (which could thus be either a primary or secondary diagnosis), nephrosclerosis, malignant nephrosclerosis, atherosclerosis, polyarteritis nodosa/microvascular polyangiitis (PAN) and chronic interstitial nephropathy (CIN). Thirty four patients with diabetic nephropathy as secondary diagnosis were registered as chronic GN. Biopsies were included twice if they contained two different GN diagnoses (excluding Cresc, which was assumed to be the primary diagnosis). Patients were included more than once if repeat biopsies revealed de novo GN. The presence of immune deposits in the basement membrane, the mesangium, tubuli, capillaries or arterioles was noted. Patients registered as terminally uraemic prior to biopsy (usually during the same admission) were registered as terminally uraemic immediately post-biopsy. The presence of the following systemic diseases in either DANYBIR or LPR was noted: SLE, anti-glomerular basement membrane (GBM) disease, Wegener's granulomatosis, PAN, HUS/TTP, Henoch–Schönlein purpura and IgA nephropathy. The occurrence of the following clinical data (available in DANYBIR but not LPR) was registered: normal renal function, azotaemia, haematuria and proteinuria. The first occurrence of the following diagnoses in either DANYBIR or LPR was registered: uraemia (WHO8 792,99 or WHO10 N18,0-19,9), nephrotic syndrome (WHO8 581 or WHO10 N4), cancer (excluding myelomatosis) (WHO8 140–202, 204–209, WHO10 C0–89, 91–98), hypertension (WHO8 400–404, WHO10 I10–15); coronary heart disease (CHD) (WHO8 402, 404, 412–414, 427–429, WHO10 I11, 13, 20–25, 50–52); acute myocardial infarction (AMI) (WHO8 410, WHO10 I21); cerebral haemorrhage (WHO8 430–431, WHO10 I60–62); cerebral thrombosis (WHO8 432–438, WHO10 I63–69); peripheral vascular disease (WHO8 440–445, WHO10 I70–77); diabetes (WHO8 249–250, WHO10 E10–11); lung embolus (WHO8 450, WHO10 I26); thrombophlebitis (WHO8 451–453, WHO10 I80–82). Atherosclerosis incidence was defined as the first occurrence of either CHD, cerebrovascular disease or peripheral vascular disease. Diagnoses were censored for the occurrence of terminal uraemia. Diagnoses were defined as risk factors if their first occurrence was prior to biopsy, and complications if they first appeared later.
Statistical analysis
Variables were compared using Student's t-test. Categorical analysis was performed using MANOVA and 
2. Pearson product–moment multiple regression analysis was used to identify independent factors affecting disease incidence. Kaplan–Meier survival analysis was used to compare patient survival, incidence of terminal uraemia and other complications. Multiple groups were compared using Gehan's generalized Wilcoxon test. In order to delineate the independent effects of risk factors, Cox's proportional hazards model was used. The confidence interval was calculated as twice the standard error of the mean.
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Results |
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The epidemiology of glomerulonephritis
A total of 2249 patients and 2325 biopsies were registered. Forty seven (2.0%) biopsies and 76 (3.4%) patients were included twice, making 2380 cases in all. A further 152 patients had systemic disease and non-glomerular disease, primarily CIN. There was no significant change in the incidence of any GN diagnosis during the period of observation, the overall incidence of biopsy-proven GN being 39.2/mio/year. The DANYBIR was compared with patients entering the TUS register from 1994 onwards with the diagnosis GN or systemic disease (EDTA codes 73, 74, 79, 84–89). A total of 164/290 (56%) patients with terminal uraemia and GN were registered in DANYBIR. A further 78 patients (27%) not in DANYBIR were registered in TUS as biopsied, presumably prior to 1985. Nine/13 (69%) patients with SLE were registered, but only 32/79 (41%) with other systemic disease. Assuming that both registers describe the same population, the overall incidence of GN (including non-biopsied) was 73/mio/year.
The number of patients in each category, age and sex distribution are shown in Table 1
. The age of the patients was 42.6±20.2 years, and 41% (confidence interval, CI 39–43) were female. The age distribution is shown in Figure 1.
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The prognosis of glomerulonephritis
A total of 65% of patients had a follow-up of 5 years or more, and 39% of 10 or more. The overall prognosis was poor. After 10 years, 32% were dead, 13% were on dialysis or transplanted, 5% were uraemic and 50% were well. The corresponding figures for 1 year were 10, 8, 6 and 76, and for 5 years 22, 13, 5 and 60. The patient survival related to diagnosis is shown in Table 2
, the renal survival (censored for patient death) in Table 3, and the combined renal and patient survival in Table 4 and Figure 2. A total of 575 patients (26%) were followed until death. The life expectancy of terminal uraemia of this selected subpopulation, with a higher age at biopsy (60.3±14.1 vs 37.3±18.6 years), is shown in Table 3. The figure for renal survival for Cresc may be an underestimate, in that many patients died in the acute phase before registration in TUS. The uraemia prevalence at biopsy and thereafter, and the combined prevalence of uraemia and death, is shown in Table 5. For all diagnoses, there was a highly significant (P<0.001) increase in mortality relative to the general population. Mortality and renal failure followed a log-linear course, except in the case of Cresc and HUS/TTP where an initial 30 and 27% 1-year mortality fell subsequently to 8%/year, and an initial renal failure rate of 29 and 51% fell to 6 and 0%, respectively. Mortality increased with increasing age, and was increased in all age groups, such that patients over 70 years had a median life expectancy of only 1.9 years. In contrast, apart from an initial increase during the first year, related to the higher incidence of Cresc and uraemia at diagnosis in older patients, there was no relationship between age and incidence of renal failure for any diagnosis. Female patients had a lower mortality and also a lower renal failure rate (10-year renal survival 76 vs 66%, P<0.001). This difference was significant for all major diagnostic groups except FSGN. It was more marked for elderly patients (<50 years at diagnosis, 77 vs 69% NS; >50 years, 75 vs 63%; P<0.001). The diagnoses could be divided into three prognostic groups: a good prognostic group (MCGN and Mem GN) with a relative mortality of three and combined renal and patient mortality of four; a poor prognostic group (Cresc, HUS/TTP and chronic GN) with a mortality of 8–19 and a combined mortality of 13–33; and the remainder with figures of 4–7 and 6–12 (Figure 2). The 5-year renal failure and patient mortality (including secondary diagnosis subgroups) were closely correlated (r=0.84, P<0.001). The prevalence of uraemia at biopsy showed a similar pattern to the 5-year patient mortality. Odds ratios for uraemia incidence are not shown, as the incidence of uraemia was closely related to the incidence of terminal uraemia.
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The influence of secondary diagnoses and immune deposits
The prognosis was affected by the presence of additional histological diagnoses. Age- and sex-adjusted risk ratios, excluding the primary diagnoses MCGN (which by definition cannot have secondary diagnoses), Cresc, chronic GN and HUS/TTP, are shown in Table 6
. The presence of multiple GN, chronic GN, nephrosclerosis and CIN all increased the risk of renal failure, but only chronic GN, malignant nephrosclerosis and CIN significantly affected mortality.
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Immunofluorescence was performed on 1790 (78%) biopsies. Basement membrane deposition was found in 46%, mesangial 33%, tubular 13%, capillary 21% and arteriolar 10%. With the obvious exception of Cresc GN, only mesangial deposition had a significant overall effect on age- and sex-adjusted prognosis, increasing the risk of renal failure by 66% (CI 26–119%, P<0.01). Further perusal showed that this adverse effect was confined mainly to patients with FSGN where the risk of renal failure was increased 109% (16–277%), and where a negative effect of basement membrane deposition was also noted (OR 1.82, CI 1.07–3.12, P<0.02).
The effect of clinical variables on prognosis
There was no difference in prognosis for referral diagnoses nephrotic syndrome, proteinuria or haematuria, while hypertension and uraemia as referral diagnosis had a poorer prognosis. The influence of clinical status at biopsy is shown in Table 6
. The presence of cancer, uraemia, diabetes mellitus and all forms of atherosclerostic disease, but not hypertension, had a significant negative impact on patient survival. Atherosclerotic disease had no influence on progression of renal disease to renal failure, the presence of uraemia and hypertension being significant predictors of renal failure. Renal survival was proportional to renal function at biopsy (5-year survival: normal function 92%, azotaemia 70%, uraemia 59%). The presence of nephrotic syndrome was not a significant independent predictor. Further perusal showed that nephrosis was related to a number of beneficial factors: nephrotic patients were younger (40.0±22.8 vs 43.3±19.4 years, P<0.002), less often hypertensive (14 vs 19%, P<0.02) and less often uraemic (6 vs 15%, P<0.001). Patients with MCGN (32%) and Mem (46%) were more often nephrotic than other diagnoses (13%, P<0.001).
Clinical complications after diagnosis
The first occurrence of each diagnosis after biopsy (censored for renal failure) was registered, patients being censored if the diagnosis occurred prior to biopsy. The annual incidence was compared with that of the general population [5] (Table 7). The incidence of all vascular complications was higher than expected. The figures for expected incidence are an overestimate, since multiple admissions with the same diagnosis are included in the national statistics. Only one GN diagnosis significantly affected the age- and sex-adjusted incidence of complications. MCGN patients had less atherosclerosis (OR 0.46, CI 0.27–0.79), hypertension (0.36, 0.19–0.70), CHD (0.46, 0.25–0.89), AMI (0.33, 0.12–0.93) and cerebral thrombosis (0.35, 0.13–0.95). Patients with Mem-P had more hypertension (2.2, 1.17–4.1). There was no significant overall difference in cancer incidence. However, in a subgroup analysis, patients over 60 years with Mem had an insignificantly increased cumulative cancer incidence after biopsy (13.9 vs 6.0%, P=0.07).
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The influence of nephrological status at biopsy is shown in Table 8
. Hypertension was associated with an increased risk of atherosclerosis, CHD, AMI, cerebral haemmorhage, cerebral thrombosis and peripheral atherosclerosis, while uraemia was associated with a lower risk of cerebral thrombosis, CHD, atherosclerosis and thrombophlebitis. The presence of nephrotic syndrome doubled the risk of thrombophlebitis and pulmonary embolus to 3.6 and 2.0%, respectively.
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The influence of systemic disease
Cresc GN was classified as either anti-GBM disease, PAN, Wegener's granulomatosis, or unclassified. Clinical details are shown in Table 9
. Wegener's granulomatosis had a good prognosis, anti-GBM GN a poor prognosis and PAN and unclassified an intermediate prognosis. The overall incidence of biopsied Wegener's granulomatosis was 3.6/mio/year, since 50% had diseases other than Cresc, primarily FSGN (16%) and CIN (18%). These patients had a better survival (5-year combined renal and patient survival 57%, P<0.01).
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The incidence of lupus nephritis was 5.5/mio/year. The age was 31.8±14.0 years and 76% were female. A variety of diagnoses were found: Mes-P 32%, CIN 26%, Mem-P 8%, FSGN 7%, Mem 7%, Cresc 4%, MCGN 3% and other 13%. The Mes-P prognosis was as good as that for other acute GN combined, with a 10-year patient survival of 88% and renal survival of 81%, combined 72%. CIN had a poorer prognosis: 64, 58 and 41%, respectively, P<0.05.
IgA nephropathy (incidence 1.8/mio/year) and Henoch–Schönlein purpura (0.9) were combined. The age was 29.1±14.7 years and 28% were female. The diagnoses were Mes-P 42%, FSGN 30%, CIN 11%, MCGN 9% and other 8%. As with lupus, there was no prognostic difference between FSGN and Mes-P, and the overall prognosis was good, with 10-year survival rates of patient 93%, renal 77% and combined 72%. These relatively good results were, however, related to the patients' young age: the age- and sex-adjusted prognosis for Mes-P was similar regardless of whether the patients had SLE, IgA nephropathy or no systemic disease.
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Discussion |
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Renal biopsy often will not be performed, or will be reserved for particularly aggressive cases, as the likelihood of therapeutic consequences is low in the following situations: steroid-sensitive nephrotic syndrome in children; intermittent haematuria without proteinuria; post-infectious GN; and bilateral small kidneys. For these reasons, the incidence of MCGN, endocapillary GN, chronic GN and IgA nephropathy is probably underrepresented in this series, and the measured prognosis unduly pessimistic. With this caveat, the study presents reliable incidence data for a large and homogenous population. The measured incidence of 39/mio/year compares with 47 [6], 34 [7], 63 [8] and 86 [9] in other European series. Comparing the biopsy register with the EDTA register suggests that the biopsy register contains 56% of all GN patients, making the overall incidence 73/mio/year. It is expected that the register will eventually represent 70–80% of patients. As previously noted, GN incidence is approximately doubled in the elderly [6]. We also noted a peak in the 20–30 years age group. The distribution of renal diagnoses corresponds to other series, with one exception: IgA nephropathy was rare, and represented only a minority of patients with Mes-P. This can be related partly to the biopsy policy mentioned above, and to the fact that immunofluorescence was not performed in 22% of cases, but this can hardly explain the whole difference. The incidence of IgA nephropathy, however, varies from 4 to 44% of different biopsy series [10] and this difference is probably real [11]; the Danish population would appear to be at the low end of this spectrum.
The present study contains follow-up data for up to 12 years for a large population with glomerular disease, and permits reliable conclusions to be drawn concerning prognostic factors for death and renal failure. Age was a risk factor for death, but not renal failure, either overall or for any diagnosis. Previous studies have shown a negative effect of age [10,12–16] while others have shown no effect [17–20]. In contrast, we found a highly significant adverse effect of male sex for both death and renal failure, which was significant for Mem, MCGN, Mes-P and Mem-P. While by no means universal [10,13], this difference has been found in at least 20 previous studies [10] including IgA nephropathy [11,21], lupus nephritis [22,23], Mem [20,24–27] and Mem-P [28,29]. Since this finding is so widespread, it is tempting to regard it as a universal feature of renal function in GN. One possible theoretical explanation is haemodynamic damage in hypofunctioning kidneys, which is presumably greater in males due to higher protein intake [30]. Another possibility is increased atherosclerosis, but we found no negative impact of atherosclerosis on renal survival. Hormonal differences do not appear to be the explanation, as the difference was more marked in patients over 50 years of age.
Mortality was increased for all diagnoses and, even for the `benign' diagnoses, MCGN and Mem, was double that of the general population. This is in contrast to previous suggestions that Mem has a normal survival [31,32]. Mortality was closely related to the presence of uraemia at diagnosis, and to progression to renal failure, there being no reason to doubt that this is causative. More surprisingly, no independent adverse effect of nephrotic syndrome on patient and renal survival was seen. Occasional studies have reached a similar conclusion [32], the majority finding nephrosis to be an adverse factor [10,13–16,33–36]. This unexpected finding is partly related to the fact that nephrosis was more common in the more benign diseases. One disadvantage of this study is that proteinuria was not quantified, and that many patients will have gone into spontaneous or induced remission without this being registered, with a consequent improvement in prognosis. Only Cresc and HUS/TTP showed signs of being `curable' diseases, all other diagnoses showing a constantly increased rate of death and renal failure throughout the period of observation.
The diagnoses can be divided into three prognostic groups: a good prognostic group (MCGN and Mem GN) with a relative mortality of three and combined renal and patient mortality of four; a poor prognostic group (Cresc, HUS/TTP and chronic GN) with a relative mortality of 6–10 and combined mortality of 10–20; and the remainder with mortalities of 4–5 and 6–10 (Figure 2). Space does not permit a detailed review of the literature concerning prognosis, but certain features should be noted. Mem GN, which in this series was treated primarily conservatively, had a benign prognosis, with a 10-year renal survival of 87%. Recent series have given similar results, with 10-year renal survival rates varying between 76 and 98% [20,31,32,37–39]. Immunosuppressive treatment of this disease is controversial; the onus of proof rests clearly upon those advocating active treatment. Nor, as others [39,40], did we find a significantly increased incidence of malignancy in this group. This suggests that investigation for occult neoplasm should be reserved for patients with a clinical suspicion. The reputation of Mem-P as the worst form of primary GN is confirmed, in this series having a long-term renal failure rate even higher than Cresc, partly related to a higher pre- and post-biopsy incidence of hypertension. While anti-GBM disease had the same patient survival as Wegener's granulomatosis, renal survival was much lower; while all forms of Wegener's granulomatosis are susceptible to immunosuppressive therapy [41], oliguric patients with anti-GBM disease will rarely respond to therapy [42].
The poor prognosis could be related to an increased incidence of all vascular complications (Table 7). Hypertension, as expected, had an adverse effect on all forms of atherosclerotic complications, emphasizing that pedantic blood pressure control is mandatory in this patient group [43]. Uraemia per se appeared to have a protective effect, possibly secondary to its anticoagulant effects. As expected, nephrosis doubled the risk of pulmonary embolus and deep thrombophlebitis. Hypercholesterolaemia secondary to nephrotic syndrome should theoretically increase the risk of CHD, but the evidence for this is equivocal [44,45]. The incidence of ischaemic heart disease was increased 26% in nephrotic patients, but this was only borderline significant, and was not accompanied by any increase in AMI incidence. Primary diagnoses had no independent effect on complications, other than a beneficial effect of MCGN diagnosis. This is perhaps related to the fact that the primary manifestation of MCGN, nephrosis, is the factor that is most amenable to pharmacological intervention.
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Accepted in revised form: 19. 3.99
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