Nephrology Dialysis Transplantation

Nephrology Dialysis Transplantation 2008 23(4):1117-1121; doi:10.1093/ndt/gfn086

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An epidemic of chronic kidney disease: fact or fiction?

Richard J. Glassock¹ and Christopher Winearls²

¹ The David Geffen School of Medicine at UCLA, Los Angeles, CA, USA ² Oxford Kidney Unit, Oxford Radcliffe Hospital, Oxford, UK

Richard J. Glassock, 8 Bethany, Laguna Niguel, CA 92677, USA. Email: glassock{at}cox.net

Keywords: chronic kidney disease; estimated glomerular filtration rate; KDOQI; KDIGO

	Introduction

Top Introduction The 'epidemic' of chronic... Need for new 'cut-off'... Overestimation of chronic kidney... References

 
The publication of the Kidney Disease Outcomes and Quality Initiative (KDOQI) clinical practice guidelines for the evaluation, classification and stratification of chronic kidney disease (CKD) in February of 2002 was a landmark event [1]. This effort has profoundly impacted clinical practice, helped bring some order to a chaotic system of nomenclature and stimulated a resurgence of interest in this long-neglected domain of clinical nephrology [2]. The nephrology community is now using a definition of the five stages of CKD, based on the presence of ‘kidney damage’ and/or reduced estimated glomerular filtration rate (eGFR) for 3 months or more [1,3]. However, it is noteworthy that three of the five stages of CKD (stages 3, 4 and 5) were arbitrarily defined and based solely on the absolute threshold of eGFR (standardized to 1.73 m² body surface area) without any requirement for concomitant evidence of ‘kidney damage’, such as proteinuria or adjustment for age and gender [2]. These levels of eGFR, combined with the similarly arbitrary selection of a time dimension (3 months) for their persistence to establish ‘chronicity’, became the ‘gold-standard’ for definition of a ‘disease’. The abbreviated modification of diet in renal disease (MDRD) equation for deriving an estimate of true glomerular filtration rate (GFR) from values of serum creatinine (calibrated to the standard used to derive the formula) quickly became the most widely used method for determination of eGFR, despite its lack of validation in subjects without CKD or across a wide spectrum of ages, body habitus, diet, ethnicity and geographic location [4]. Because of inaccuracies, relative to true GFR, when eGFR is >60 ml/min/1.73 m² reporting of specific values of eGFR was recommended only when calculated values of <60 ml/min/1.73 m² were obtained [5]. Despite these limitations epidemiologists have used eGFR to estimate the overall prevalence rates of CKD, in its various stages, in representative samples of the general population.

	The ‘epidemic’ of chronic kidney disease

Top Introduction The 'epidemic' of chronic... Need for new 'cut-off'... Overestimation of chronic kidney... References

 
Many lay and professional publications have frequently and consistently referred to the ‘epidemic’ of CKD (stages 1–4), inferring that the prevalence rate of CKD in the community at large is high and rising rapidly. The conventional definition of an ‘epidemic’ is ‘the occurrence in a community or region of a group of illnesses of similar nature clearly in excess of normal expectancy’ [6]. The phrases ‘epidemic’ and ‘chronic kidney disease’ have been linked in a way that enhances a perception that an ever-increasing burden of stage 1–4 CKD has made and is making an important contribution to the rapid rise in the incidence and the prevalence of treated stage 5 CKD (the so-called epidemic of end-stage renal disease, ESRD) throughout the world.

We question whether stage 1–4 CKD, especially stage 3 CKD, really is as common as is claimed and as highlighted in the accompanying editorial by Coresh, Stevens and Levey [7]. We further have doubts as to whether CKD, especially stage 3, is rising in prevalence in the general population. Published commentaries have pointed out the difficulties in estimating the prevalence of CKD from indirect calculation of eGFR [8]. The best and perhaps the only legitimate evidence concerning the burden of CKD in the general population comes from surveys in which individuals deemed to be representative of the characteristics of the population as a whole are examined for features of CKD, including serum creatinine levels, eGFR and urine albumin excretion. Surveys based on clinical laboratory measurements of serum creatinine obtained from subjects enrolled in health plans or under medical care give incorrectly high CKD prevalence estimates because persons with other evidence of kidney disease or believed to be at higher risk for kidney disease are more likely to undergo testing. The National Health and Nutrition Examination Surveys (NHANES), periodically conducted in the USA (in non-institutionalized adults over the age of 20 years), are good examples of the population-based approach to estimation of overall CKD burden [9–14]. A total of five surveys conducted between 1988 and 2004 have been used to quantify the changing prevalence of CKD over time [14] (Tables 1 and 2). Earlier summaries of surveys conducted between 1988 and 2000 showed relative stability of stage 3 and 4 CKD and only small increases in stage 1 and 2 CKD (Table 1A) [11,12]. More recently published estimates through 2004 have suggested a rise in population prevalence of stage 1–4 CKD revised from 10% in 1988–1994 to 13% in 1999–2004 (Table 1B) [7,13,14]. The corresponding figures for stage 3 CKD are 5.4–7.7% and for stage 4 CKD from 0.21% to 0.35% over the same period of time. Interestingly, 76% of individuals classified as having stage 3 CKD in 1999–2004 had no increase of albumin excretion above normal [14]. A marked increase in the fraction of patients over 70 years of age was also noted between 1988–1994 and 1999–2004, consistent with the ageing of the general population [14]. Over 37% of those individuals classified as having stage 3 CKD in 1999–2004 were over 70 years of age [14]. In the more recently published report a ‘conservative trend analysis’ was conducted in an attempt to equate the serum creatinine concentrations in young, healthy individuals (ages 20–39, free of hypertension or diabetes) between the two groups of surveys. In this analysis, after adjustment for age, the prevalences of stage 3 and 4 CKD (eGFR = <60 ml/min/1.73 m²) were not different over the two time periods (odds ratio = 1.13, CI 0.79–1.30, P = 0.07). This analysis casts some doubt on the conclusion of Coresh, Stevens and Levey [7] that the prevalence of CKD is indeed rising, after accounting for age differences and serum creatinine measurements in the population.

View this table: [in this window] [in a new window]   Table 1 Trends in the United States population prevalence of stage 1–4 chronic kidney disease (CKD) derived from National Health and Nutrition Examination Surveys (NHANES) and the population prevalence and incidence of end-stage renal disease (ESRD, stage 5 CKD; United States Renal Data System, USRDS) treated with renal replacement therapy (RRT) between 1988 and 2000a

 

View this table: [in this window] [in a new window]   Table 2 Trends in the United States population prevalence of stage 1–4 chronic kidney disease (CKD) derived from National Health and Nutrition Examination Surveys and the population prevalence and incident of end-stage renal disease (ESRD, stage 5 CKD; United States Renal Data System, USRDS) treated with renal replacement therapy (RRT) between 1988 and 2004a

 
In addition, all of the surveys conducted by NHANES used only a single serum creatinine measurement, and it is not possible to include a dimension of ‘chronicity’ implicit in the definition of CKD in these analyses. It has been estimated that 25–30% of subjects initially categorized as stage 3 CKD will subsequently no longer fall into this category when repeated measurements are obtained over 3 months or more after the ‘qualifying’ test [15,16]. The ‘chronicity’ of disease is an important and often overlooked aspect of population-based surveys of CKD [15]. We suggested that the use of a single serum creatinine value and lack of estimations of ‘chronicity’ may have led to an overestimation of the prevalence of CKD in these surveys.

It must also be stressed that during the same intervals examined by NHANES the incidence rate of stage 5 CKD (ESRD) receiving renal replacement therapy (RRT) rose nearly six times more rapidly than the prevalence rates of stage 1–4 CKD [17]. Similar observations have been previously reported for the periods between 1978 and 1991 [9]. Thus a posited ‘epidemic’ of CKD did not apparently fuel the ‘epidemic’ of treated ESRD observed during this period of time [8,9]. However, as pointed out in the accompanying editorial by Coresh, Stevens and Levey [7], the prevalence of CKD at any given stage at any one point in time (point prevalence) is determined by the incidence of CKD and also by how rapidly individual patients migrate from one stage to the next as the disease progresses towards ESRD [18]. The phenomenon of a changing pace of progression could be a possible explanation for these observations, as suggested by Hallan et al. [19], but it seems rather unlikely to explain the relative stability of prevalence rates of CKD over a decade when significant therapeutic advances were made in the retardation of progression of renal disease. Based on our interpretation of the available data, we concluded that (1) no ‘epidemic’ of CKD existed, at least in the USA, between 1998 and 2004 and (2) the estimation of the overall prevalence of CKD in the population, especially stage 3 CKD, has been overestimated and is not as ‘common’ as advocated by Coresh, Stevens and Levey [7]. More research is needed to better define the true prevalence of CKD in the community at large.

	Need for new ‘cut-off’ values for eGFR to define chronic kidney ‘disease’

Top Introduction The 'epidemic' of chronic... Need for new 'cut-off'... Overestimation of chronic kidney... References

 
While the overall prevalence rate of CKD can be disputed, published estimates of the number of individuals affected with CKD still raise concerns [20]. A purported 13.1% prevalence of stage 1–4 CKD translates into 26.3 million individuals (adults over age 20 years) in the USA, 16.2 million (62%) of whom would have stage 3 or 4 CKD, according to the current eGFR-based definitions of KDOQI and the recent reports from NHANES [7,14]. Furthermore, it has been shown that public awareness of this ‘fact’ is low [12,14,20]. As we have indicated, these estimates may exaggerate the frequency of CKD in the population, particularly in the large group of individuals with stage 3 CKD (56% of the entire estimated CKD population) [14]. It is therefore worth examining the characteristics of the stage 3 CKD population more carefully. Most of the adults (>60%) identified with stage 3 CKD are older (>60 years of age) and females outnumber males about 1.75:1 [10,11,14]. The observed male:female ratio for CKD (0.6:1) is the opposite of that seen in ESRD receiving RRT, which was 1.7:1 in the USA in 2004 and 1.6:1 in the UK in 2005 [11,12,17,21]. These findings raise questions about the appropriateness of an arbitrary ‘cut-off’ value of <60 ml/min/1.73 m² (without any requirement for a concomitant increase in albumin excretion above normal or other evidence of structural renal disease) as a definition for CKD (stages 3 and 4) without some adjustment for the normal gender-specific decline in eGFR with ageing [14,22,23]. In a recent cross-sectional population-based study the median eGFR (calibrated MDRD equation) for apparently ‘healthy’ septuagenarian (70–79 years old) Caucasian males and females was 70 and 63 ml/min/1.73 m², respectively [24]. The 5th percentile for similarly aged men and women was 50 and 47 ml/min/1.73 m² [24]. Thus, a very substantial portion of ‘healthy’ men and even more elderly women will be classified as having stage 3 CKD using the current guidelines even in the absence of other features of kidney disease. A lower ‘cut-off’ for defining CKD in the absence of kidney damage (such as an eGFR of <45 ml/min/1.73 m²) or using a percentile distribution based on age and gender would lead to a marked reduction in the number of those individuals who are currently, and in our view erroneously, categorized as having a ‘disease’.

We recognize that there is a semantic issue of not calling the ‘normal’ decline in eGFR with ageing a ‘disease’. While definitions of ‘disease’ vary, a purely statistical definition is weak and one that incorporates the concept of a ‘disadvantage’ is preferred [25]. The evidence that an eGFR above the 5th percentile adjusted for age and gender specifically and independently confers a ‘special’ risk or unique disadvantage (including eventual progression to treated ESRD and morbidity or mortality related to cardiovascular disease) after adjustment for allcomorbid risk factors (including proteinuria) is not established [26–31]. Many studies have demonstrated a stepwise increase in the risk of cardiovascular events with decrements in eGFR, and concomitant proteinuria would be expected to enhance this risk even further. However, the major increase in risk is seen with an eGFR <45 ml/min/1.73 m². Several studies have shown no or only a slight increase in risk for elderly individuals with a persistent eGFR of 45–59 ml/min/1.73 m² compared to those with an eGFR of >60 ml/min/1.73 m² [26,32,34]. In a study of almost 3 million largely male patients attending veterans administration outpatient clinics O’Hare and co-workers [32] found that patients over age 45 years and an eGFR of 50–59 ml/min/1.73 m² (uncalibrated MDRD equation) had no additional risk of mortality compared to similarly aged patients with an eGFR >60 ml/min/1.73 m² after adjustment for age, race, gender and comorbidities [32]. Indeed only an eGFR of <40 ml/min/1.73 m² was consistently associated with an increased risk of mortality in all age groups. In addition, preliminary results from the ‘Three Cities’ study in France did not show any increased mortality risk for elderly (over 65 years of age) individuals with an eGFR (calibrated MDRD equation) of 45– 59 ml/min/1.73 m² compared to those with an eGFR of >60 ml/min/1.73 m² [33].

Thus, it may be surmised that the use of a ‘cut-off’ of eGFR of <60 ml/min/1.73 m² without any correction for age or gender, and without any consideration of concomitant albuminuria, may misclassify as many as 30–50% of elderly subjects as having stage 3 CKD, thus further inflating the CKD prevalence estimates mentioned earlier. Finally, the estimation of CKD prevalence in other populations having characteristics (diet, body habitus, environment, ethnicity) different from those used to generate the MDRD estimating equation and having different gender- and age-dependent changes in eGFR could also materially influence the accuracy of CKD prevalence, as has already been shown for China [34].

	Overestimation of chronic kidney disease burden and suggestions for corrective action

Top Introduction The 'epidemic' of chronic... Need for new 'cut-off'... Overestimation of chronic kidney... References

 
We posit that the prevalence rate of stage 1–4 CKD in the general population, particularly stage 3 CKD, has been significantly overestimated due to the failure of both the KDOQI and KDIGO classifications to take into account age and gender influences on the ‘normal’ distribution of eGFR. Furthermore, sampling errors (a single serum creatinine measurement) have contributed to these overestimations in prospective population-wide surveys. Studies carried out over time in well-defined populations (USA) have not suggested that the prevalence of stage 1–4 CKD is increasing at ‘epidemic’ proportions and also indicate that a rising burden of CKD or its more rapid progression to ESRD does not appear to be a likely explanation for the ‘epidemic’ of treated ESRD. The origins of this latter ‘epidemic’, which many developed nations experienced in the recent past and which now appears to be subsiding, remain uncertain [13]. Enhanced access to ESRD treatment is a plausible, yet unproven, explanation for the rising and now stable numbers of treated ESRD patients in many developed nations. The observed higher level of renal function at the onset of RRT would be consistent with enhanced access being a major driving force behind the previous increase in treated ESRD [13]. If our analysis is correct, a substantial revision of the KDOQI (and KDIGO) guidelines for staging stage 1–4 CKD is overdue, and its replacement needs to take into account the gender-specific ‘normal’ decline in eGFR with ageing, perhaps using percentile rather than absolute eGFR thresholds. Greater emphasis also needs to be placed on the dimension of time to validate the ‘chronicity’ of the process. As we learn more about the natural history of CKD from longitudinal, community-based studies it has become increasingly apparent that the CKD classification system developed in 2002, while representing a conceptual advance, now needs revision. Much additional epidemiologic research is needed to more carefully define the true prevalence of CKD that confers specific disadvantages (e.g. progression to ESRD or increased cardiovascular risk) on the members of well-defined populations. The possible specific ‘disadvantage’ imposed on individuals of varying age and gender within a given population that is related to the eGFR levels alone, independent of other risk factors such as proteinuria, hypertension, diabetes, hyperlipidaemia, cigarette smoking and obesity, needs to be proven in prospective studies. We welcome the recent position statement of the NKF that acknowledges the problems of oversimplifying the definition of CKD and look forward to an improved version [35]. Should a new and improved system of defining and categorizing CKD emerge from debates such as this, we would expect that more realistic estimates of CKD prevalence in the population as a whole would ensue. We would also anticipate that better detection and management strategies, which limit the ‘false’ identification of ‘non-existent’ disease and enhance the accurate diagnosis of ‘true’ disease, would inexorably follow.

	Acknowledgments

 
The senior author (R.J.G.) wishes to thank Alan Hull and Chi-Yuan Hsu for the review of preliminary versions of this editorial and for their helpful suggestions for improvement.

Conflict of interest statement. None declared.

(See related article by Paul E. de Jong et al. Fact or fiction of the epidemic of chronic kidney disease—let us not squabble about estimated GFR only, but also focus on albuminuria. Nephrol Dial Transplant 2008; 23: 1092–1095.)

	References

Top Introduction The 'epidemic' of chronic... Need for new 'cut-off'... Overestimation of chronic kidney... References

 

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Received for publication: 3. 9.07
Accepted in revised form: 29. 1.08

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