Background Among patients with end-stage renal disease who aretreated with hemodialysis, solute clearance during dialysisand nutritional adequacy are determinants of mortality. We determinedthe effects of reductions in blood urea nitrogen concentrationsduring dialysis and changes in serum albumin concentrations,as an indicator of nutritional status, on mortality in a largegroup of patients treated with hemodialysis.
Methods We analyzed retrospectively the demographic characteristics,mortality rate, duration of hemodialysis, serum albumin concentration,and urea reduction ratio (defined as the percent reduction inblood urea nitrogen concentration during a single dialysis treatment)in 13,473 patients treated from October 1, 1990, through March31, 1991. The risk of death was determined as a function ofthe urea reduction ratio and serum albumin concentration.
Results As compared with patients with urea reduction ratiosof 65 to 69 percent, patients with values below 60 percent hada higher risk of death during follow-up (odds ratio, 1.28 forurea reduction ratios of 55 to 59 percent and 1.39 for ratiosbelow 55 percent). Fifty-five percent of the patients had ureareduction ratios below 60 percent. The duration of dialysiswas not predictive of mortality. The serum albumin concentrationwas a more powerful (21 times greater) predictor of death thanthe urea reduction ratio, and 60 percent of the patients hadserum albumin concentrations predictive of an increased riskof death (values below 4.0 g per deciliter). The odds ratiofor death was 1.48 for serum albumin concentrations of 3.5 to3.9 g per deciliter and 3.13 for concentrations of 3.0 to 3.4g per deciliter. Diabetic patients had lower serum albumin concentrationsand urea reduction ratios than nondiabetic patients.
Conclusions Low urea reduction ratios during dialysis are associatedwith increased odds ratios for death. These risks are worsenedby inadequate nutrition.
At present, more than 150,000 Americans with end-stage renaldisease benefit from dialysis treatment under Medicare's disease-targetedentitlement program1. Without the widespread availability ofdialysis and kidney transplantation, many lives would have endedprematurely. Despite these achievements, the annual mortalityrate among patients with end-stage renal disease in the UnitedStates increased from 21.0 percent in 1981 to 24.3 percent in19882,3. In contrast, the annual mortality rates among patientswith end-stage renal disease in other industrialized nationshave remained stable and lower than those in the United States3.
The average blood urea nitrogen concentrations before and aftera hemodialysis treatment and between hemodialysis treatments,the duration of individual treatments, and the adequacy of nutritionas assessed by simple laboratory variables may be critical determinantsof the morbidity and mortality of patients treated with hemodialysis4,5,6,7,8.Pursuant to these observations, we undertook a retrospectiveanalysis to define the risk of death as a function of both soluteclearance by hemodialysis and serum albumin concentrations,as a measure of nutritional status, in a large group of patientstreated with hemodialysis. We also evaluated the extent to whichsolute clearance may affect over time the relation between changesin solute clearance and changes (if any) in the patients' nutritionalstatus.
Methods
Patients
National Medical Care, a large provider of hemodialysis services,maintains a patient statistical profile system7,8 that includesselected patient data such as birth date, sex, cause of end-stagerenal disease, time and frequency of dialysis treatments, frequencyand duration of hospitalization, renal-transplantation status,vital status, and the results of common clinical laboratorytests, such as serum electrolyte, creatinine, albumin, and cholesterolconcentrations and blood urea nitrogen concentrations. All thebiochemical analyses were performed by a single clinical laboratory(LifeChem, Northvale, N.J.). This data base includes a measureof the percent reduction in the blood urea nitrogen concentrationduring a single dialysis treatment -- the urea reduction ratio-- as a measure of the adequacy of dialysis. The urea reductionratio is calculated with the formula 100 x (1 - [Ct/Co]), inwhich Ct is the blood urea nitrogen measured five minutes afterthe end of dialysis and Co is the predialysis blood urea nitrogen9.The urea reduction ratio is a function of the clearance of ureafrom the blood by the dialyzer, the length of the individualdialysis treatment, and the volume of distribution of urea ina particular patient. Therefore, the urea reduction ratio isa quantitative measurement of an individual patient's urea clearanceduring a single hemodialysis treatment and can be used as aproxy for the adequacy of solute clearance during a treatment10,11,12.
The 13,473 study subjects were selected from among adult patientswith end-stage renal disease who were receiving hemodialysisthree times per week in the 358 National Medical Care facilitieson October 1, 1990, and who were still receiving dialysis therapysix months later (March 31, 1991) or who had died. Patientswho underwent kidney transplantation, transferred to other dialysisfacilities or to other forms of long-term dialysis, or werelost to follow-up during that interval were excluded. A subgroupof 12,170 patients were treated from October through December1990 (early period) and January through March 1992 (late period).
Laboratory-data files were examined to identify patients whohad one or more determinations of the serum albumin concentrationand the urea reduction ratio between June and September 1990,the four months before the start of the study. The results ofall determinations during this interval were averaged for eachpatient. During this time, the serum albumin concentration wasmeasured a mean (±SD) of 2.3 ±1.0 times per patientand the urea reduction ratio was determined 2.3 ±1.1times per patient. Our retrospective analyses used these resultsfor the patients who met the specified follow-up criteria.
Statistical Analysis
The initial data analysis used a forward stepwise logistic-regressionprocess13,14,15 to evaluate the odds ratios of death in termsof selected demographic characteristics, such as age, sex, race,presence of diabetes mellitus, and primary renal diagnosis.For each renal diagnosis, a separate binary variable was constructed.Demographic characteristics found to be associated with theodds ratios were then fixed in the regression model. The ureareduction ratio and the serum albumin concentration were thenadded to the model. In addition, the patients were grouped accordingto both the urea reduction ratio and serum albumin concentrationas dichotomous variables, and patient profiles were constructedby treating the groups as binary variables in the model.
Finally, we compared the urea reduction ratios and serum albuminconcentrations in 4758 patients with diabetes mellitus withthose in 8715 nondiabetic patients. Group values were adjustedfor age, sex, and race, and the statistical differences betweenthem were evaluated by analysis of covariance.
Results
Patients
A total of 13,473 patients were undergoing hemodialysis on October1, 1990, and fulfilled the entry criteria. Their mean age (±SD)was 59 ±15 years; 48 percent were women, 48 percent werenonwhite, and 35 percent had diabetes. The median duration ofhemodialysis was 30 months. A total of 1556 of the patients(11.5 percent) died during the six-month follow-up period.
Demographic Characteristics, Urea Reduction Ratio, Serum Albumin Concentration, and Risk of Death
The effect of the patients' characteristics on the odds ratiofor death is shown in Table 1. After a mean age of 59 years,each year of advancing age was associated with an approximately3 percent increase in the odds ratio. The odds ratios were higheramong whites and diabetic patients. A similar analysis was performedthat included the serum albumin concentration and the urea reductionratio in the model. Both the serum albumin concentration andthe urea reduction ratio were significant predictors of death,but there was no statistical interaction between these two factors.The duration of each dialysis treatment was also evaluated inthis model. Given the range of times during which hemodialysiswas performed (lower-quartile group, three hours; upper-quartilegroup, four hours), the length of treatment was not associatedwith a risk of death.
Table 1. Relation of the Patients' Characteristics to the Odds Ratio for Death.
As compared with a reference urea reduction ratio of 65 to 69percent, values less than 60 percent were associated with ahigher odds ratio for death (Table 2). The serum albumin concentrationwas an even more powerful predictor of risk. As compared withpatients who had serum albumin concentrations ranging from 4.0to 4.4 g per deciliter, patients with serum albumin concentrationsbelow 4.0 g per deciliter had increased odds ratios for death(Table 2).
Table 2. Adjusted Risk of Death According to the Urea Reduction Ratio or Serum Albumin Concentration in Patients with End-Stage Renal Disease.
The patients were also grouped according to their combined valuesfor urea reduction ratio and serum albumin concentration (Figure 1).Considering patients with a urea reduction ratio of 65percent and a serum albumin concentration of 4.0 g per deciliteras the reference group, lower serum albumin concentrations wereassociated with significant increases in the risk of death forall the urea-reduction-ratio groups. The odds ratios increasedat lower urea reduction ratios for the patients who had serumalbumin concentrations of 3.5 to 3.9 g per deciliter or 3.0to 3.4 g per deciliter, but not for the patients whose serumalbumin concentrations were 4.0 or <3.0 g per deciliter.Thus, both the urea reduction ratio and serum albumin concentrationwere important determinants of the odds of death, but factorsassociated with the serum albumin concentration had a greatereffect.
Figure 1. Odds Ratios for Death for a Range of Urea Reduction Ratios and Serum Albumin Concentrations in 13,473 Patients with End-Stage Renal Disease Treated with Hemodialysis.
A value of 1.0 was assigned to the odds ratio for the reference group (Ref), with a urea reduction ratio of 65 percent and a serum albumin concentration of 4.0 g per deciliter. On the bar graphs, the top symbol indicates the statistical significance of this comparison, the symbol on the right the P value for the comparison with a serum albumin concentration of 4.0 g per deciliter, and the symbol on the left the P value for the comparison with a urea reduction ratio of 65 percent. NS denotes not significant (P>0.05), solid squares a P value of 0.05 to >0.01, and asterisks a P value of 0.01.
Frequency Distribution and Temporal Trends for Urea Reduction Ratio Values and Serum Albumin Concentrations
The frequency distribution of the mean urea reduction ratiofor each patient from June through September 1990 is shown inFigure 2. The mean urea reduction ratio was 58 ±10 percent.Ten percent of the values were 70 percent; 24 percent were 65 percent, and 45 percent were 60 percent. In contrast, 33percent of the patients had urea reduction ratios that werebelow 55 percent, and 16 percent had values below 50 percent.For individual patients, the average urea reduction ratios fromJune through September 1990 were not significantly differentfrom the values obtained from October 1990 through March 1991(58 ±10 percent vs. 59 ±9 percent, P>0.05).
Figure 2. Frequency Distribution of the Average Urea Reduction Ratios and Serum Albumin Concentrations in Patients with End-Stage Renal Disease Treated with Hemodialysis from June through September 1990.
The distribution of values for the serum albumin concentrationsfor each patient from June through September 1990 is shown inFigure 2. The mean serum albumin concentration was 3.8 ±0.4g per deciliter. Sixty percent of the serum albumin concentrationswere below 4.0 g per deciliter, 13 percent were below 3.5 gper deciliter, 2 percent were below 3.0 g per deciliter, andless than 1 percent were below 2.5 g per deciliter. There wasno correlation between the serum albumin concentration and theurea reduction ratio.
For 12,170 patients treated from October through December 1990(early period) and January through March 1992 (late period),we averaged both the urea reduction ratio and the serum albuminconcentration. During the early period, preliminary data concerningthe influence of the urea reduction ratio and the serum albuminconcentration on the risk of death among patients treated withhemodialysis were disseminated to facility medical directors,and they were urged to respond to these data in their individualfacilities. The mean urea reduction ratio increased from 58±9 percent during the early period to 62 ±8 percentduring the late period (P<0.001). The lower-quartile groupof urea reduction ratios increased from 53 to 56 percent (Figure 3).The mean serum albumin concentration during this intervaldecreased from 3.9 ±0.3 to 3.7 ±0.3 g per deciliter(P<0.001). Each patient's early-period urea reduction ratioand serum albumin concentration were subtracted from the correspondinglate-period values. Although the correlation of the change inserum albumin with the change in the urea reduction ratio wasdirect and statistically significant (r = 0.044, P<0.001),the r2 statistic (0.002) indicated a weak association.
Figure 3. Trends in Median Urea Reduction Ratios in Patients with End-Stage Renal Disease Treated with Hemodialysis from October 1990 through March 1992.
We identified a subgroup of 178 patients in whom the urea reductionratio was 50 percent during the early period and increasedto 60 percent in the late period. The mean urea reduction ratioin this group increased from 43 ±3 percent in the earlyperiod to 67 ±8 percent in the late period, and the meanserum albumin concentration fell from 3.8 ±0.5 to 3.7±0.4 g per deciliter (P = 0.01). In contrast, we identified37 patients with urea reduction ratios of 65 percent in theearly period that fell to 55 percent during the late period.The mean urea reduction ratios during the early and late periodsin this group were 71 ±14 percent and 50 ±7 percent,respectively. The mean serum albumin concentrations in thesepatients were 3.7 ±0.5 and 3.6 ±0.5 g per deciliter,respectively (P not significant). There was no correlation inthe magnitude of the change in serum albumin concentration betweenthe patients in whom the urea reduction ratio increased andthe patients in whom it decreased.
Urea Reduction Ratio and Serum Albumin Concentrations in Diabetic and Nondiabetic Patients
An adjustment for the serum albumin concentration and urea reductionratio in the statistical model was associated with a reductionin the odds ratio for death in the diabetic patients. Hence,we evaluated potential differences in the distributions of theserum albumin concentration and urea reduction ratio in patientswith and those without diabetes. Women had higher urea reductionratios than men during treatment (61 ±9 vs. 56 ±9percent, P<0.001), and nondiabetic patients had higher valuesthan diabetic patients during treatment (59 ±10 vs. 57±10 percent, P<0.001). The nondiabetic patients hadhigher serum albumin concentrations than the diabetic patients(3.9 ±0.4 vs. 3.8 ±0.3 g per deciliter, P<0.001).
Discussion
Our results support the conclusions of previous studies thatinadequate dialysis and poor nutrition are major factors contributingto the excessive mortality of patients treated with hemodialysisin the United States. We used the urea reduction ratio as ameasure of the adequacy of dialysis8,9,10,11,12,16. When theurea reduction ratio was included in the statistical model,the odds of death were not associated with the duration of dialysistreatments (range, three to four hours) commonly used in thesepatients. This finding seems to contradict previous studiessuggesting that treatment time itself is a critical determinantof survival for patients undergoing hemodialysis6,7. In theseearlier studies, however, no direct measure of solute clearancewas reported. The National Cooperative Dialysis Study4,5,17also found that the length of dialysis had a significant effecton patient survival,5,18 whereas we did not. Our results suggestthat the intensity of treatment should be sufficient to resultin a urea reduction ratio of 60 percent, whereas a urea reductionratio of >50 percent was implied to be adequate by the NationalCooperative Dialysis Study4,5,9,17. The majority of patientscurrently treated with hemodialysis would not have been eligibleto participate in the cooperative study because of age and coexistingconditions such as diabetes mellitus19,20. Our data suggestthat this patient population may require more intensive dialysisto achieve greater clearance.
The increased odds ratio for death with urea reduction ratiosbelow 60 percent and the original frequency distribution ofvalues for the urea reduction ratio suggest that dialysis mortalitymay decrease with more intensive dialysis. Beginning in late1990, National Medical Care provided facilities and medicaldirectors with local and national data about the odds ratiofor death and the distribution of urea reduction ratios. A subsequentupward trend in urea reduction ratios was probably the resultof a revised definition of adequate dialysis -- that is, a targeturea reduction ratio of 60 percent.
Like the authors of previous studies of patients with renaland other diseases,7,8,21,22 we found that the serum albuminconcentration was the most powerful predictor of death. However,the urea reduction ratio and serum albumin concentration wereindependent predictors. For the approximately 60 percent ofpatients at risk because of a low serum albumin concentration(<4.0 g per deciliter), the odds ratios associated with inadequatenutrition (as reflected by low serum albumin concentrations)may be magnified by the presence of suboptimal dialysis. Someinvestigators suggest that augmentation of urea clearance willimprove a patient's nutritional status23,24. We did not findthis to be the case, and the correlation between the adequacyof dialysis and nutritional status (as measured by serum albuminconcentration) was weak. Of course, the persistence of a lowserum albumin concentration despite an increased urea reductionratio could have been due to many factors other than malnutrition,including hepatocellular dysfunction, hypervolemia, and exposureto pyrogenic cytokines.
Our analysis confirms the observation that differences in nutritionand the intensity of dialysis explain part of the excess mortalityamong diabetic patients with end-stage renal disease25. Patientswith diabetes have lower serum albumin concentrations and ureareduction ratios than nondiabetic patients. Possible factorscontributing to the lower urea reduction ratios in these patientsinclude compromised blood flow during a dialysis treatment asa result of hemodynamic instability, poor flow through the vascularaccess for hemodialysis, the provision of less intensive dialysisbecause of inappropriate reliance on low prehemodialysis bloodurea nitrogen or serum creatinine values as measures of theadequacy of dialysis, and the prescription of suboptimal therapybecause of prejudices that excessive morbidity and mortalityare unavoidable in diabetic patients. Women treated with hemodialysishad higher urea reduction ratios and a reduced odds ratio ofdeath. Physicians may have prescribed dialysis treatment independentlyof a patient's body size, resulting in increased urea reductionratios in women, who are generally smaller than men.
Because our study was retrospective, a causal relation betweenthe urea reduction ratio, serum albumin concentration, or bothand the risk of death should be inferred from these data withcaution. However, these results may have practical implicationsfor the care of patients being treated with hemodialysis. Nephrologistsmay have only limited success in improving nutritional statusby augmenting dialysis. Thus, both these components of caremust be monitored and independently corrected when they aresuboptimal -- a urea reduction ratio below 60 percent and aserum albumin concentration of less than 4.0 g per deciliter.Strategies that improve solute clearance during hemodialysisinclude using more efficient dialyzers, increasing the timeof hemodialysis, and optimizing the blood and dialysate flowsduring each dialysis treatment. The nutritional status of patientsundergoing hemodialysis should be monitored routinely, and wheninadequacies are identified, corrective measures must be instituted.These measures include augmenting the patient's caloric intakeby providing hyperalimentation during dialysis treatments, correctingdental deficiencies, improving gastrointestinal abnormalities,and supplementing finances for nutritious foods.
Supported in part by a grant (DK45656-01) from the NationalInstitute of Diabetes and Digestive and Kidney Diseases (toDr. Owen).
Source Information
From Brigham and Women's Hospital and Harvard Medical School, Boston (W.F.O., J.M.L.), and National Medical Care, Inc. (a subsidiary of W.R. Grace & Co.), Waltham, Mass. (N.L.L., Y.L., E.G.L.).
Address reprint requests to Dr. Owen at the Seeley Mudd Bldg., Brigham and Women's Hospital, 250 Longwood Ave., Boston, MA 02115.
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(2007). Protein metabolism in glucocorticoid excess: study in Cushing's syndrome and the effect of treatment. Am. J. Physiol. Endocrinol. Metab.
292: E1426-E1432
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Kshirsagar, A. V., Craig, R. G., Beck, J. D., Moss, K., Offenbacher, S., Kotanko, P., Yoshino, M., Levin, N. W., Yip, J. K., Almas, K., Lupovici, E., Falk, R. J.
(2007). Severe Periodontitis Is Associated with Low Serum Albumin among Patients on Maintenance Hemodialysis Therapy. CJASN
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Kilpatrick, R. D., McAllister, C. J., Kovesdy, C. P., Derose, S. F., Kopple, J. D., Kalantar-Zadeh, K.
(2007). Association between Serum Lipids and Survival in Hemodialysis Patients and Impact of Race. J. Am. Soc. Nephrol.
18: 293-303
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Rocco, M. V., Frankenfield, D. L., Hopson, S. D., McClellan, W. M.
(2006). Relationship between clinical performance measures and outcomes among patients receiving long-term hemodialysis.. ANN INTERN MED
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Amaral, S., Hwang, W., Fivush, B., Neu, A., Frankenfield, D., Furth, S.
(2006). Association of Mortality and Hospitalization with Achievement of Adult Hemoglobin Targets in Adolescents Maintained on Hemodialysis. J. Am. Soc. Nephrol.
17: 2878-2885
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Joki, N., Hase, H., Tanaka, Y., Takahashi, Y., Saijyo, T., Ishikawa, H., Inishi, Y., Imamura, Y., Hara, H., Tsunoda, T., Nakamura, M.
(2006). Relationship between serum albumin level before initiating haemodialysis and angiographic severity of coronary atherosclerosis in end-stage renal disease patients. Nephrol Dial Transplant
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Ricci, Z., Bellomo, R., Ronco, C.
(2006). Dose of Dialysis in Acute Renal Failure. CJASN
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Bellizzi, V., Scalfi, L., Terracciano, V., De Nicola, L., Minutolo, R., Marra, M., Guida, B., Cianciaruso, B., Conte, G., Di Iorio, B. R.
(2006). Early Changes in Bioelectrical Estimates of Body Composition in Chronic Kidney Disease. J. Am. Soc. Nephrol.
17: 1481-1487
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Jindal, K., Chan, C. T., Deziel, C., Hirsch, D., Soroka, S. D., Tonelli, M., Culleton, B. F.
(2006). CHAPTER 1: Hemodialysis Adequacy in Adults. J. Am. Soc. Nephrol.
17: S4-S7
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Jindal, K., Chan, C. T., Deziel, C., Hirsch, D., Soroka, S. D., Tonelli, M., Culleton, B. F.
(2006). CHAPTER 5: Frequent and Sustained Hemodialysis. J. Am. Soc. Nephrol.
17: S24-S27
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Wu, D. Y., Shinaberger, C. S., Regidor, D. L., McAllister, C. J., Kopple, J. D., Kalantar-Zadeh, K.
(2006). Association between Serum Bicarbonate and Death in Hemodialysis Patients: Is It Better to Be Acidotic or Alkalotic?. CJASN
1: 70-78
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Traynor, J. P., Oun, H. A., McKenzie, P., Shilliday, I. R., McKay, I. G., Dunlop, A., Geddes, C. C., Mactier, R. A.
(2005). Assessing the utility of the stop dialysate flow method in patients receiving haemodiafiltration. Nephrol Dial Transplant
20: 2479-2484
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Greene, T., Daugirdas, J., Depner, T., Allon, M., Beck, G., Chumlea, C., Delmez, J., Gotch, F., Kusek, J. W., Levin, N., Owen, W., Schulman, G., Star, R., Toto, R., Eknoyan, G., for the Hemodialysis Study Group,
(2005). Association of Achieved Dialysis Dose with Mortality in the Hemodialysis Study: An Example of "Dose-Targeting Bias". J. Am. Soc. Nephrol.
16: 3371-3380
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Kalantar-Zadeh, K., Regidor, D. L., McAllister, C. J., Michael, B., Warnock, D. G.
(2005). Time-Dependent Associations between Iron and Mortality in Hemodialysis Patients. J. Am. Soc. Nephrol.
16: 3070-3080
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Chan, C. T., Li, S. H., Verma, S.
(2005). Nocturnal hemodialysis is associated with restoration of impaired endothelial progenitor cell biology in end-stage renal disease. Am. J. Physiol. Renal Physiol.
289: F679-F684
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Ward, R. A.
(2005). Protein-Leaking Membranes for Hemodialysis: A New Class of Membranes in Search of an Application?. J. Am. Soc. Nephrol.
16: 2421-2430
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Andreoli, S. P., Brewer, E. D., Watkins, S., Fivush, B., Powe, N., Shevchek, J., Foreman, J.
(2005). American Society of Pediatric Nephrology Position Paper on Linking Reimbursement to Quality of Care. J. Am. Soc. Nephrol.
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Wynne, K., Giannitsopoulou, K., Small, C. J., Patterson, M., Frost, G., Ghatei, M. A., Brown, E. A., Bloom, S. R., Choi, P.
(2005). Subcutaneous Ghrelin Enhances Acute Food Intake in Malnourished Patients Who Receive Maintenance Peritoneal Dialysis: A Randomized, Placebo-Controlled Trial. J. Am. Soc. Nephrol.
16: 2111-2118
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Seres, D. S.
(2005). Surrogate Nutrition Markers, Malnutrition, and Adequacy of Nutrition Support. Nutr Clin Pract
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Manhes, G., Heng, A. E., Aublet-Cuvelier, B., Gazuy, N., Deteix, P., Souweine, B.
(2005). Clinical features and outcome of chronic dialysis patients admitted to an intensive care unit. Nephrol Dial Transplant
20: 1127-1133
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Allon, M., Radeva, M., Bailey, J., Beddhu, S., Butterly, D., Coyne, D. W., Depner, T. A., Gassman, J. J., Kaufman, A. M., Kaysen, G. A., Lewis, J. A., Schwab, S. J., for the HEMO Study Group,
(2005). The spectrum of infection-related morbidity in hospitalized haemodialysis patients. Nephrol Dial Transplant
20: 1180-1186
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Agalou, S., Ahmed, N., Babaei-Jadidi, R., Dawnay, A., Thornalley, P. J.
(2005). Profound Mishandling of Protein Glycation Degradation Products in Uremia and Dialysis. J. Am. Soc. Nephrol.
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Kamimura, M. A., Majchrzak, K. M., Cuppari, L., Pupim, L. B.
(2005). Protein and Energy Depletion in Chronic Hemodialysis Patients: Clinical Applicability of Diagnostic Tools. Nutr Clin Pract
20: 162-175
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Plantinga, L. C., Jaar, B. G., Fink, N. E., Sadler, J. H., Levin, N. W., Coresh, J., Klag, M. J., Powe, N. R.
(2005). Frequency of patient-physician contact in chronic kidney disease care and achievement of clinical performance targets. Int J Qual Health Care
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Kalantar-Zadeh, K., Kilpatrick, R. D., McAllister, C. J., Greenland, S., Kopple, J. D.
(2005). Reverse Epidemiology of Hypertension and Cardiovascular Death in the Hemodialysis Population: The 58th Annual Fall Conference and Scientific Sessions. Hypertension
45: 811-817
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Grooteman, M. P. C., Nube, M. J.
(2004). Impact of the type of dialyser on the clinical outcome in chronic haemodialysis patients: does it really matter?. Nephrol Dial Transplant
19: 2965-2970
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Plantinga, L. C., Fink, N. E., Jaar, B. G., Sadler, J. H., Coresh, J., Klag, M. J., Levey, A. S., Powe, N. R.
(2004). Frequency of Sit-Down Patient Care Rounds, Attainment of Clinical Performance Targets, Hospitalization, and Mortality in Hemodialysis Patients. J. Am. Soc. Nephrol.
15: 3144-3153
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Sambrook, P. N., Chen, J. S., March, L. M., Cameron, I. D., Cumming, R. G., Lord, S. R., Schwarz, J., Seibel, M. J.
(2004). Serum Parathyroid Hormone Is Associated with Increased Mortality Independent of 25-Hydroxy Vitamin D Status, Bone Mass, and Renal Function in the Frail and Very Old: A Cohort Study. J. Clin. Endocrinol. Metab.
89: 5477-5481
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Chiang, C.-K., Hsu, S.-P., Pai, M.-F., Peng, Y.-S., Ho, T.-I, Liu, S.-H., Hung, K.-Y., Tsai, T.-J.
(2004). Interleukin-18 is a strong predictor of hospitalization in haemodialysis patients. Nephrol Dial Transplant
19: 2810-2815
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Dara, S. I., Afessa, B., Bajwa, A. A., Albright, R. C.
(2004). Outcome of Patients With End-Stage Renal Disease Admitted to the Intensive Care Unit. Mayo Clin Proc.
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Wiederkehr, M. R., Kalogiros, J., Krapf, R.
(2004). Correction of metabolic acidosis improves thyroid and growth hormone axes in haemodialysis patients. Nephrol Dial Transplant
19: 1190-1197
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Kloppenburg, W. D., Stegeman, C. A., Kremer Hovinga, T. K., Vastenburg, G., Vos, P., de Jong, P. E., Huisman, R. M.
(2004). Effect of prescribing a high protein diet and increasing the dose of dialysis on nutrition in stable chronic haemodialysis patients: a randomized, controlled trial. Nephrol Dial Transplant
19: 1212-1223
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Termorshuizen, F., Dekker, F. W., van Manen, J. G., Korevaar, J. C., Boeschoten, E. W., Krediet, R. T.
(2004). Relative Contribution of Residual Renal Function and Different Measures of Adequacy to Survival in Hemodialysis Patients: An analysis of the Netherlands Cooperative Study on the Adequacy of Dialysis (NECOSAD)-2. J. Am. Soc. Nephrol.
15: 1061-1070
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McClellan, W. M., Hodgin, E., Pastan, S., McAdams, L., Soucie, M.
(2004). A Randomized Evaluation of Two Health Care Quality Improvement Program (HCQIP) Interventions to Improve the Adequacy of Hemodialysis Care of ESRD Patients: Feedback Alone versus Intensive Intervention. J. Am. Soc. Nephrol.
15: 754-760
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Lambie, S. H., Taal, M. W., Fluck, R. J., McIntyre, C. W.
(2004). Analysis of factors associated with variability in haemodialysis adequacy. Nephrol Dial Transplant
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Metcalfe, W., Khan, I.H., Prescott, G.J., Simpson, K., Macleod, A.M.
(2003). Hospitalization in the first year of renal replacement therapy for end-stage renal disease. QJM
96: 899-909
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Cheung, A. K., Levin, N. W., Greene, T., Agodoa, L., Bailey, J., Beck, G., Clark, W., Levey, A. S., Leypoldt, J. K., Ornt, D. B., Rocco, M. V., Schulman, G., Schwab, S., Teehan, B., Eknoyan, G.
(2003). Effects of High-Flux Hemodialysis on Clinical Outcomes: Results of the HEMO Study. J. Am. Soc. Nephrol.
14: 3251-3263
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Brimble, K. S., Treleaven, D. J., Onge, J. S., Carlisle, E. J.
(2003). Risk factors for increased variability in dialysis delivery in haemodialysis patients. Nephrol Dial Transplant
18: 2112-2117
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Szczech, L. A., Reddan, D. N., Klassen, P. S., Coladonato, J., Chua, B., Lowrie, E. G., Lazarus, J. M., Owen, W. F. Jr
(2003). Interactions between dialysis-related volume exposures, nutritional surrogates and mortality among ESRD patients. Nephrol Dial Transplant
18: 1585-1591
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Szczech, L. A., Reddan, D. N., Klassen, P. S., Coladonato, J., Chua, B., Lowrie, E. G., Lazarus, J. M., Owen, W. F. Jr
(2003). Interactions between dialysis-related volume exposures, nutritional surrogates and mortality among ESRD patients. Nephrol Dial Transplant
18: 1585-1591
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Teng, M., Wolf, M., Lowrie, E., Ofsthun, N., Lazarus, J. M., Thadhani, R.
(2003). Survival of Patients Undergoing Hemodialysis with Paricalcitol or Calcitriol Therapy. NEJM
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Wang, A. Y.-M., Woo, J., Lam, C. W.-K., Wang, M., Sea, M. M.-M., Lui, S.-F., Li, P. K.-T., Sanderson, J.
(2003). Is a Single Time Point C-Reactive Protein Predictive of Outcome in Peritoneal Dialysis Patients?. J. Am. Soc. Nephrol.
14: 1871-1879
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Ono, K., Tsuchida, A., Kawai, H., Matsuo, H., Wakamatsu, R., Maezawa, A., Yano, S., Kawada, T., Nojima, Y.
(2003). Ankle-Brachial Blood Pressure Index Predicts All-Cause and Cardiovascular Mortality in Hemodialysis Patients. J. Am. Soc. Nephrol.
14: 1591-1598
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Teehan, G. S., Liangos, O., Jaber, B. L.
(2003). Update on Dialytic Management of Acute Renal Failure. J Intensive Care Med
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Rodriguez, R. A., Mendelson, M., O'Hare, A. M., Hsu, L. C., Schoenfeld, P.
(2003). Determinants of Survival among HIV-Infected Chronic Dialysis Patients. J. Am. Soc. Nephrol.
14: 1307-1313
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McIntyre, C. W., Lambie, S. H., Taal, M. W., Fluck, R. J.
(2003). Assessment of haemodialysis adequacy by ionic dialysance: intra-patient variability of delivered treatment. Nephrol Dial Transplant
18: 559-562
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Sehgal, A. R.
(2003). Impact of Quality Improvement Efforts on Race and Sex Disparities in Hemodialysis. JAMA
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Eknoyan, G., Beck, G. J., Cheung, A. K., Daugirdas, J. T., Greene, T., Kusek, J. W., Allon, M., Bailey, J., Delmez, J. A., Depner, T. A., Dwyer, J. T., Levey, A. S., Levin, N. W., Milford, E., Ornt, D. B., Rocco, M. V., Schulman, G., Schwab, S. J., Teehan, B. P., Toto, R., the Hemodialysis (HEMO) Study Group,
(2002). Effect of Dialysis Dose and Membrane Flux in Maintenance Hemodialysis. NEJM
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Kinchen, K. S., Sadler, J., Fink, N., Brookmeyer, R., Klag, M. J., Levey, A. S., Powe, N. R.
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Williams, D. M., Sreedhar, S. S., Mickell, J. J., Chan, J. C. M.
(2002). Acute Kidney Failure: A Pediatric Experience Over 20 Years. Arch Pediatr Adolesc Med
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Fink, J. C., Zhan, M., Blahut, S. A., Soucie, M., McClellan, W. M.
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Winkelmayer, W. C., Glynn, R. J., Mittleman, M. A., Levin, R., Pliskin, J. S., Avorn, J.
(2002). Comparing Mortality of Elderly Patients on Hemodialysis versus Peritoneal Dialysis: A Propensity Score Approach. J. Am. Soc. Nephrol.
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Brimble, K. S., Onge, J. S., Treleaven, D. J., Carlisle, E. J.
(2002). Comparison of volume of blood processed on haemodialysis adequacy measurement sessions vs regular non-adequacy sessions. Nephrol Dial Transplant
17: 1470-1474
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Port, F. K., Ashby, V. B., Dhingra, R. K., Roys, E. C., Wolfe, R. A.
(2002). Dialysis Dose and Body Mass Index Are Strongly Associated with Survival in Hemodialysis Patients. J. Am. Soc. Nephrol.
13: 1061-1066
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Qureshi, A. R., Alvestrand, A., Divino-Filho, J. C., Gutierrez, A., Heimburger, O., Lindholm, B., Bergstrom, J.
(2002). Inflammation, Malnutrition, and Cardiac Disease as Predictors of Mortality in Hemodialysis Patients. J. Am. Soc. Nephrol.
13: S28-36
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Keshaviah, P., Collins, A. J., Ma, J. Z., Churchill, D. N., Thorpe, K. E.
(2002). Survival Comparison between Hemodialysis and Peritoneal Dialysis Based on Matched Doses of Delivered Therapy. J. Am. Soc. Nephrol.
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Copley, J. B.
(2001). Resistance Training Enhances the Value of Protein Restriction in the Treatment of Chronic Kidney Disease. ANN INTERN MED
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Sarnak, M. J., Jaber, B. L.
(2001). Pulmonary Infectious Mortality Among Patients With End-Stage Renal Disease. Chest
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Peri, U. N., Fenves, A. Z., Middleton, J. P.
(2001). Improving survival of octogenarian patients selected for haemodialysis. Nephrol Dial Transplant
16: 2201-2206
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GANESH, S. K., STACK, A. G., LEVIN, N. W., HULBERT-SHEARON, T., PORT, F. K.
(2001). Association of Elevated Serum PO4, Ca PO4 Product, and Parathyroid Hormone with Cardiac Mortality Risk in Chronic Hemodialysis Patients. J. Am. Soc. Nephrol.
12: 2131-2138
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Schiffl, H., Lang, S. M., Stratakis, D., Fischer, R.
(2001). Effects of ultrapure dialysis fluid on nutritional status and inflammatory parameters. Nephrol Dial Transplant
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Clase, C. M., St Pierre, M. W., Churchill, D. N.
(2001). Conversion between bromcresol green- and bromcresol purple-measured albumin in renal disease. Nephrol Dial Transplant
16: 1925-1929
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GIORDANO, M., FEO, P. D., LUCIDI, P., dePASCALE, E., GIORDANO, G., INFANTONE, L., ZOCCOLO, A. M., CASTELLINO, P.
(2001). Increased Albumin and Fibrinogen Synthesis in Hemodialysis Patients with Normal Nutritional Status. J. Am. Soc. Nephrol.
12: 349-354
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Movilli, E., Carlo Cancarini, G., Zani, R., Camerini, C., Sandrini, M., Maiorca, R.
(2001). Adequacy of dialysis reduces the doses of recombinant erythropoietin independently from the use of biocompatible membranes in haemodialysis patients. Nephrol Dial Transplant
16: 111-114
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Carfray, A., Patel, K., Whitaker, P., Garrick, P., Griffiths, G. J., Warwick, G. L.
(2000). Albumin as an outcome measure in haemodialysis in patients: the effect of variation in assay method. Nephrol Dial Transplant
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Zenios, S. A., Fuloria, P. C.
(2000). Managing the Delivery of Dialysis Therapy: A Multiclass Fluid Model Analysis. Management Science
46: 1317-1336
[Abstract]
65 percent and a serum albumin concentration of 
50 percent during the early period and increased to 
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