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View of Uremic Toxins Article Prognosis of CKD Patients Receiving Outpatient Nephrology Care in Italy Luca De Nicola,* Paolo Chiodini,† Carmine Zoccali,‡ Silvio Borrelli,* Bruno Cianciaruso,§ Biagio Di Iorio, Domenico Santoro,¶ Vincenzo Giancaspro,** Cataldo Abaterusso,†† Ciro Gallo,† Giuseppe Conte,* and Roberto Minutolo,* for the SIN-TABLE CKD Study Group‡‡ Summary *Nephrology Division Background and objectives Prognosis in nondialysis chronic kidney disease (CKD) patients under regular and †Unit of Medical nephrology care is rarely investigated. Statistics at the Second University of Naples, Naples, Italy; Design, setting, participants, & measurements We prospectively followed from 2003 to death or June 2010 a ‡ Ն Nephrology Division, cohort of 1248 patients with CKD stages 3 to 5 and previous nephrology care 1 year in 25 Italian outpa- Center of National tient nephrology clinics. Cumulative incidence of ESRD or death before ESRD were estimated using the Research-Institute of competing-risk approach. Biomedicine and Molecular Immunology Hospital, Reggio Results Estimated rates (per 100 patient-years) of ESRD and death 8.3 (95% confidence interval [CI], 7.4 to Calabria, Italy; 9.2) and 5.9 (95% CI 5.2 to 6.6), respectively. Risk of ESRD and death increased progressively from stages 3 §Nephrology Division, to 5. ESRD was more frequent than death in stage 4 and 5 CKD, whereas the opposite was true in stage 3 University Federico II, Naples, Italy; CKD. Younger age, lower body mass index, proteinuria, and high phosphate predicted ESRD, whereas ʈ Nephrology Division, older age, diabetes, previous cardiovascular disease, ESRD, proteinuria, high uric acid, and anemia pre- County Hospital, dicted death (P Ͻ 0.05 for all). Among modifiable risk factors, proteinuria accounted for the greatest contri- Solofra, Italy; bution to the model fit for either outcome. ¶Nephrology Division, University of Messina, Messina, Italy; Conclusions In patients receiving continuity of care in Italian nephrology clinics, ESRD was a more frequent **Nephrology Division, outcome than death in stage 4 and 5 CKD, but the opposite was true in stage 3. Outcomes were predicted Di Venere Hospital, by modifiable risk factors specific to CKD. Proteinuria used in conjunction with estimated GFR refined risk Bari, Italy; ††Division of stratification. These findings provide information, specific to CKD patients under regular outpatient ne- Nephrology, University of Verona, Italy; and phrology care, for risk stratification that complement recent observations in the general population. the ‡‡Italian Society of Clin J Am Soc Nephrol 6: 2421–2428, 2011. doi: 10.2215/CJN.01180211 Nephrology Study Group, “Target BP LEvels in CKD” (see Appendix for the Introduction age and comorbidities modifying the predictive role complete list of The knowledge on the competing risk of the two main of main factors, BP in primis (10–13). Third, intensity Investigators) outcomes of chronic kidney disease (CKD), that is, of nephrology care modifies survival (14). ESRD and death, and on the risk factors underlying Previous studies in referred patients have shown Correspondence: Dr. these outcomes is of paramount importance to put in ESRD rates similar or higher than mortality (10,11,15– Luca De Nicola, Cattedra di Nefrologia - place effective prevention strategies. Community 20); however, the definition of risk factors for these Dip. Gerontologia, studies and analyses made on large health insurance outcomes still remains uncertain. Indeed, in most Geriatria, Mal. databases reported mortality rates remarkably larger studies, information was retrospectively collected, Metabolismo, Seconda than ESRD rates (1–5). However, information on co- and the duration of nephrology care and of CKD Universita`di Napoli, Piazza Miraglia, 80131 horts referred to renal clinics, and particularly in pa- diagnosis, which are main modifiers of the competing Napoli, Italia. Phone/ tients under continuous nephrology care, is scarce. risk of ERSD versus death (14,21), was fairly short or Fax: 39-081-2549409; Specific information on the prognosis and risk fac- unspecified. E-mail: luca.denicola@ unina2.it tors responsible for CKD progression and death in In 2003, we designed the TArget BP LEvels (TABLE) CKD patients followed in the setting of tertiary ne- multicenter cohort study, aimed at identifying risk phrology care is of major relevance for three reasons. factors for ESRD, death, and CV complications in First, these patients represent a selected population adult stage 3 to 5 CKD patients, attending Italian renal with peculiar clinical characteristics with respect to clinics for at least 1 year before the study. The cross- unreferred patients, including younger age, more ad- sectional evaluation revealed a high prevalence of vanced disease, higher burden of cardiovascular (CV) patients not achieving main therapeutic goals (22). In comorbidities, and higher BP (6–9). Second, ESRD this study, we report the prospective follow-up re- and death are predicted by different risk factors, with sults to estimate the competing risks of ESRD and www.cjasn.org Vol 6 October, 2011 Copyright © 2011 by the American Society of Nephrology 2421 2422 Clinical Journal of the American Society of Nephrology death and to assess the main determinants of these out- ing to their distribution, as assessed by the Shapiro–Wilk comes. The results can be helpful in refining the global risk test. Categorical variables were reported as percentages. profile in CKD patients receiving continuity of care in a Differences in characteristics of patients among the three nephrology clinic. CKD stages were tested by means of one-way ANOVA or Kruskal–Wallis (according to their distribution) and Pear- Study Population and Methods son chi-squared test for continuous and categorical vari- This is a prospective observational study performed in ables, respectively. Cochran–Armitage trend test was used 25 Italian outpatient nephrology clinics exclusively dedi- to compare prevalence of modifiable risk factors across cated to the conservative care of CKD and with predefined stages. Possible heterogeneity of target prevalence among clinical and laboratory protocols. centers was investigated by means of intracluster correla- tion coefficient (31). Median follow-up was estimated by the inverse Kaplan–Meier approach (32). Patients Eligible subjects were all of the consecutive patients To assess prognosis of CKD patients according to stage 3 attending the centers during a 9-month period of 2003 with to 5, we used ESRD and death before ESRD as outcomes. A diagnosis of CKD (low estimated GFR [eGFR] and/or pro- further composite end point included ESRD and death, teinuria persisting for Ն3 months), eGFR Ͻ60 ml/min per whichever occurred first. Because ESRD and death before 1.73 m2 (no substitutive treatment), and a first visit at the ESRD are mutually exclusive events (i.e., the occurrence of nephrology clinic dating back at least 1 year before the either one prevents the occurrence of the other), Kaplan– study visit. Patients with acute kidney injury during the 6 Meier estimates of time to ESRD or death before ESRD are months preceding the study visit were excluded. All of the biased; we therefore calculated the cumulative incidence of patients gave informed consent to the protocol, which was ESRD or death before ESRD using the competing-risk ap- approved by the local ethical committee. proach (33), and stages were compared with the Gray test (34). Incidence of the composite outcome was estimated by standard Kaplan–Meier approach. Data Collection and Definitions To assess the predictive role of the uncontrolled modi- The study visit in 2003 was the starting date of the fiable risk factors, we used ESRD and overall (before and follow-up study. The data were collected by participating after ESRD) death as outcomes. Multivariable Cox propor- nephrologists in anonymous case report forms, filled in at tional-hazards models, stratified for CKD stage and center, each center, and then sent back to the coordinating center were used to estimate event-specific hazard ratios (HRs) for quality checks and analyses. At the study visit, infor- and 95% confidence intervals (CIs). When evaluating over- mation was collected on demographic, clinical, and labo- all survival, ESRD was included as time-dependent cova- ratory data and medical history, including any previous riate; when evaluating time to ESRD, dead subjects were CV event, defined as any event among coronary artery censored at the date of death. For each modifiable risk disease, congestive heart failure, and cerebrovascular and factor, the heterogeneity of predictive role among CKD peripheral vascular disease. Twenty-four–hour urine col- stages was assessed by likelihood ratio test of two CKD lection was repeated if the value of the measured creati- stage-stratified models: one with CKD stage-specific esti- nine excretion rate was outside the 60% to 140% range of mates and one with overall risk factor estimate. Under the the value calculated according to Dwyer and Kenler (23). null hypothesis of no heterogeneity, this statistic follows GFR was estimated by the four-variable Modification of approximately a chi-squared distribution on J-1 (i.e., 3to1) Diet in Renal Disease (MDRD) study equation. degrees of freedom (35). The contribution of each covariate At the study visit, we also collected information on main to the model fit was estimated as percentage reduction of modifiable risk factors that were defined as uncontrolled R2 value of the model
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