An epidemic of chronic kidney disease: fact or fiction?

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1 Nephrol Dial Transplant (2008) 23: doi: /ndt/gfn086 Debate on the epidemic of chronic kidney disease The Challenge An epidemic of chronic kidney disease: fact or fiction? Richard J. Glassock 1 and Christopher Winearls 2 1 The David Geffen School of Medicine at UCLA, Los Angeles, CA, USA and 2 Oxford Kidney Unit, Oxford Radcliffe Hospital, Oxford, UK Keywords: chronic kidney disease; estimated glomerular filtration rate; KDOQI; KDIGO 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. Introduction 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 longneglected 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 m 2 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 m 2 reporting of specific values of egfr was recommended only when calculated values of <60 ml/min/1.73 m 2 were obtained [5]. Despite Correspondence and offprint requests to: Richard J. Glassock, 8 Bethany, Laguna Niguel, CA 92677, USA. glassock@cox.net The epidemic of chronic kidney disease 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 populationbased approach to estimation of overall CKD burden C The Author [2008]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please journals.permissions@oxfordjournals.org

2 1118 R. J. Glassock and C. Winearls 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 2000 a Stage b Description Prevalence c (%) Ratio / egfr d 90 + albuminuria EGFR albuminuria EGFR EGFR Total stages ESRD e Prevalence Incidence a Data derived from Reference [12]. b Stages of CKD according to K DOQI (2002) classification. c Prevalence in non-institutionalized adults (age > 20 years) NHANES of (two surveys) and (one survey). d egfr = MDRD abbreviated equation, calibrated, in ml/min/1.73 m 2. e Prevalence and incidence of ESRD population treated with RRT per million population-midpoint (1991 and 2000) USRDS data (Reference [17], s67 s84). 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 2004 a Stage b Description Prevalence c (%) Ratio / egfr d 90 + albuminuria egfr albuminuria egfr egfr Total stages ESRD e Prevalence Incidence a Data derived from Reference [14]. b Stages of CKD according to KDOQI (2002). c Prevalence in non-institutionalized adults (age 20 years) NHANES of (two surveys) and (three surveys). d egfr = MDRD abbreviated equation, calibrated, ml/min/1.73 m 2. e Prevalence and incidence of ESRD population treated with RRT per million population-midpoint (1991 and 2002) USRDS data (Reference [17], s67 s84). [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 to 13% in (Table 1B) [7,13,14]. The corresponding figures for stage 3 CKD are % 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 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 and , consistent with the ageing of the general population [14]. Over 37% of those individuals classified as having stage 3 CKD in 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 stage3and4ckd(egfr= <60 ml/min/1.73 m 2 )were not different over the two time periods (odds ratio = 1.13, CI , 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. 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

3 An epidemic of chronic kidney disease: fact or fiction? 1119 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 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 m 2 (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 crosssectional 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 m 2, respectively [24]. The 5th percentile for similarly aged men and women was 50 and 47 ml/min/1.73 m 2 [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 m 2 ) 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 all comorbid 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 m 2. Several studies have shown no or only a slight increase in risk for elderly individuals with a persistent egfr of ml/min/1.73 m 2 compared to those with an egfr of >60 ml/min/1.73 m 2 [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 ml/min/1.73 m 2 (uncalibrated MDRD equation) had no additional risk of mortality compared to similarly aged patients with an egfr >60 ml/min/1.73 m 2 after adjustment for age, race, gender and comorbidities [32]. Indeed only an egfr of <40 ml/min/1.73 m 2 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 ml/min/1.73 m 2 compared to those with an egfr of >60 ml/min/1.73 m 2 [33]. Thus, it may be surmised that the use of a cut-off of egfr of <60 ml/min/1.73 m 2 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,

4 1120 R. J. Glassock and C. Winearls 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 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. Acknowledgements. 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: ) References 1. National Kidney Foundation. Kidney Disease Outcomes Quality Initiative. Clinical Practice Guidelines for Chronic Kidney Disease: evaluation, classification, and stratification. Am J Kidney Dis. 2002; 39(Suppl 1): s1 s Hsu CY, Chertow GM. Chronic renal confusion: insufficiency, failure, dysfunction, or disease. Am J Kidney Dis 2000; 36: Levey AS, Eckardt KU, Tsukamoto Y et al. Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int 2005;67: Stevens LAS, Coresh J, Greene T et al. Assessing kidney functionmeasured and estimated glomerular filtration rate. NEnglJMed2006; 354: Levey AS, Coresh J, Greene T et al. Chronic kidney disease epidemiology collaboration. Ann Intern Med 2006; 145: Gordis L. Epidemiology, 3rd edn. Philadelphia: Elsevier Saunders, 2004, Coresh J, Stevens LA, Levey AS. Chronic kidney disease is common: what do we do next? Nephrol Dial Transplant 2007; 23: Kiberd B. The chronic kidney disease epidemic: stepping back and looking forward. J Am Soc Nephrol 2006; 17: Hsu CY, Vittinghoff E, Lin F et al. The incidence of end-stage renal disease is increasing faster than the prevalence of chronic renal insufficiency. Ann Intern Med 2004; 141: Clase CM, Garg AX, Kiberd BA. Prevalence of low glomerular filtration rate in nondiabetic Americans: Third National Health and Nutrition Examination Survey (NHANES III). J Am Soc Nephrol 2002; 13: Coresh J, Astor BC, Greene T et al. Prevalence of chronic kidney disease and decreased renal function in the adult US population: Third National Health and Nutrition Examination Survey. AmJKidneyDis. 2003; 41: Coresh J, Byrd-Holt D, Astor BC et al. Chronic kidney disease awareness, prevalence and trends among US adults, 1999 to J Am Soc Nephrol 2005; 16: Centers of Disease Control (CDC). Prevalence of chronic kidney disease and associated risk factors United States, MMWR Morb Mortal Wkly Rep 2007; 56: Coresh J, Selvin E, Stevens LA et al. Prevalence of chronic kidney disease in the United States. JAMA 2007; 298: Eriksen BO, Ingebretsen OC. In chronic kidney disease staging the use of the chronicity criterion affects prognosis and the rate of progression. Kidney Int 2007; 72: Eriksen BO, Ingebretsen OC. The progression of chronic kidney disease: a 10-year population-based study of the effects of gender and age. Kidney Int 2006: United States Renal Data System Annual Data Report. Am J Kidney Dis 2007; 49(Suppl 1): s Stengel B, Couchoud C. Chronic kidney disease prevalence and treated end-stage renal disease incidence: a complex relationship. JAmSoc Nephrol 2006; 17:

5 An epidemic of chronic kidney disease: fact or fiction? Hallan ST, Coresh J, Astor BC et al. International comparison of the relationship of chronic kidney disease prevalence and ESRD risk. J Am Soc Nephrol 2006; 17: Levey AS, Andreoli SP, DuBose T et al. Chronic kidney disease: common, harmful and treatable World Kidney Day J Am Soc Nephrol 2007; 18: Ansell D, Feest TG, Tomson C et al. UK Renal Registry Report 2006 UK Renal Registry, Bristol, UK, 29 ( 22. Davies DF, Shock NW. Age changes in glomerular filtration rate, effective plasma flow and tubular excretory capacity in adult males. J Clin Invest. 1950; 29: Wesson LG. Physiology of the Human Kidney. New York: Grune and Stattton, Wetzels JFM, Kiemeney LALM, Swinkels DW et al. Age-and gender-specific reference values of estimated GFR in Caucasians: the Nijmegen Biomedical Study. Kidney Int 2007; 72: George CRP. Disease explicated and disease defined. Ph.D. Thesis. University of Sydney, Majunath G, Tighiouart H, Coresh J et al. Level of kidney function as a risk factor for cardiovascular outcomes in the elderly. Kidney Int 2003; 63: Go AS, Chertow GM, Fan D et al. Chronic kidney disease and the risks of death, cardiovascular events and hospitalization. N Engl J Med 2004; 351: Muntner P, He J, Astor BC et al. Traditional and non-traditional risk factors predict coronary heart disease in chronic kidney disease: results from the atherosclerosis risk in communities study. J Am Soc Nephrol 2004; 16: Foley RN, Wang C, Collins AJ. Cardiovascular risk factor profiles and kidney function stage in the US general population: the NHANES III study. Mayo Clin Proc 2005; 80: Clase CM, Kiberd BA, Garg AX. Relationships between glomerular filtration rate and the prevalence of metabolic abnormalities: results from the Third National Health and Nutrition Survey Examination Survey (NHANES III). Nephron Clin Pract 2007; 105: c178 c Tonelli M, Pfeffer MA. Kidney disease and cardiovascular risk. Ann Rev Med 2007; 58: Steinman MA, Borzecki A, Walter LC. Mortality risk stratification in chronic kidney disease: one size for all ages? J Am Soc Nephrol 2006; 17: Stengel B, Loury P, Froissart M et al. Long-term outcome in the elderly with chronic kidney disease (CKD) in the general population (Abstract). Nephrol Dial Transplant 2007; 22(Suppl 6): vi Ma YC, Zuo L, Chen JH et al. Modified glomerular filtration rate estimating equations for Chinese patients with chronic kidney disease. J Am Soc Nephrol 2006; 17: Vassalotti JA, Stevens LA and Levey AS. Special announcement: Testing for Chronic Kidney Disease: a position statement from the National Kidney Foundation. Am J Kidney Dis 2007; 50: Received for publication: Accepted in revised form:

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