Original Article
The Urea Reduction Ratio and Serum Albumin Concentration as Predictors of Mortality in Patients Undergoing Hemodialysis
N Engl J Med 1993; 329:1001-1006September 30, 1993
- Abstract
Background
Among patients with end-stage renal disease who are treated with hemodialysis, solute clearance during dialysis and nutritional adequacy are determinants of mortality. We determined the effects of reductions in blood urea nitrogen concentrations during dialysis and changes in serum albumin concentrations, as an indicator of nutritional status, on mortality in a large group 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 in blood urea nitrogen concentration during a single dialysis treatment) in 13,473 patients treated from October 1, 1990, through March 31, 1991. The risk of death was determined as a function of the urea reduction ratio and serum albumin concentration.
Results
As compared with patients with urea reduction ratios of 65 to 69 percent, patients with values below 60 percent had a higher risk of death during follow-up (odds ratio, 1.28 for urea reduction ratios of 55 to 59 percent and 1.39 for ratios below 55 percent). Fifty-five percent of the patients had urea reduction ratios below 60 percent. The duration of dialysis was not predictive of mortality. The serum albumin concentration was a more powerful (21 times greater) predictor of death than the urea reduction ratio, and 60 percent of the patients had serum albumin concentrations predictive of an increased risk of death (values below 4.0 g per deciliter). The odds ratio for death was 1.48 for serum albumin concentrations of 3.5 to 3.9 g per deciliter and 3.13 for concentrations of 3.0 to 3.4 g per deciliter. Diabetic patients had lower serum albumin concentrations and urea reduction ratios than nondiabetic patients.
Conclusions
Low urea reduction ratios during dialysis are associated with increased odds ratios for death. These risks are worsened by inadequate nutrition.
Media in This Article
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.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.Article Activity
- Article
At present, more than 150,000 Americans with end-stage renal disease benefit from dialysis treatment under Medicare's disease-targeted entitlement program1. Without the widespread availability of dialysis and kidney transplantation, many lives would have ended prematurely. Despite these achievements, the annual mortality rate among patients with end-stage renal disease in the United States increased from 21.0 percent in 1981 to 24.3 percent in 19882,3. In contrast, the annual mortality rates among patients with end-stage renal disease in other industrialized nations have remained stable and lower than those in the United States3.
The average blood urea nitrogen concentrations before and after a hemodialysis treatment and between hemodialysis treatments, the duration of individual treatments, and the adequacy of nutrition as assessed by simple laboratory variables may be critical determinants of the morbidity and mortality of patients treated with hemodialysis4-8. Pursuant to these observations, we undertook a retrospective analysis to define the risk of death as a function of both solute clearance by hemodialysis and serum albumin concentrations, as a measure of nutritional status, in a large group of patients treated with hemodialysis. We also evaluated the extent to which solute clearance may affect over time the relation between changes in solute clearance and changes (if any) in the patients' nutritional status.
Methods
Patients
National Medical Care, a large provider of hemodialysis services, maintains a patient statistical profile system7,8 that includes selected patient data such as birth date, sex, cause of end-stage renal disease, time and frequency of dialysis treatments, frequency and duration of hospitalization, renal-transplantation status, vital status, and the results of common clinical laboratory tests, such as serum electrolyte, creatinine, albumin, and cholesterol concentrations and blood urea nitrogen concentrations. All the biochemical analyses were performed by a single clinical laboratory (LifeChem, Northvale, N.J.). This data base includes a measure of the percent reduction in the blood urea nitrogen concentration during a single dialysis treatment -- the urea reduction ratio -- as a measure of the adequacy of dialysis. The urea reduction ratio is calculated with the formula 100 × (1 - [Ct/Co]), in which Ct is the blood urea nitrogen measured five minutes after the end of dialysis and Co is the predialysis blood urea nitrogen9. The urea reduction ratio is a function of the clearance of urea from the blood by the dialyzer, the length of the individual dialysis treatment, and the volume of distribution of urea in a particular patient. Therefore, the urea reduction ratio is a quantitative measurement of an individual patient's urea clearance during a single hemodialysis treatment and can be used as a proxy for the adequacy of solute clearance during a treatment10-12.
The 13,473 study subjects were selected from among adult patients with end-stage renal disease who were receiving hemodialysis three times per week in the 358 National Medical Care facilities on October 1, 1990, and who were still receiving dialysis therapy six months later (March 31, 1991) or who had died. Patients who underwent kidney transplantation, transferred to other dialysis facilities or to other forms of long-term dialysis, or were lost to follow-up during that interval were excluded. A subgroup of 12,170 patients were treated from October through December 1990 (early period) and January through March 1992 (late period).
Laboratory-data files were examined to identify patients who had one or more determinations of the serum albumin concentration and the urea reduction ratio between June and September 1990, the four months before the start of the study. The results of all determinations during this interval were averaged for each patient. During this time, the serum albumin concentration was measured a mean (±SD) of 2.3 ±1.0 times per patient and the urea reduction ratio was determined 2.3 ±1.1 times per patient. Our retrospective analyses used these results for the patients who met the specified follow-up criteria.
Statistical Analysis
The initial data analysis used a forward stepwise logistic-regression process13-15 to evaluate the odds ratios of death in terms of 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 the odds ratios were then fixed in the regression model. The urea reduction ratio and the serum albumin concentration were then added to the model. In addition, the patients were grouped according to both the urea reduction ratio and serum albumin concentration as dichotomous variables, and patient profiles were constructed by treating the groups as binary variables in the model.
Finally, we compared the urea reduction ratios and serum albumin concentrations in 4758 patients with diabetes mellitus with those in 8715 nondiabetic patients. Group values were adjusted for age, sex, and race, and the statistical differences between them were evaluated by analysis of covariance.
Results
Patients
A total of 13,473 patients were undergoing hemodialysis on October 1, 1990, and fulfilled the entry criteria. Their mean age (±SD) was 59 ±15 years; 48 percent were women, 48 percent were nonwhite, and 35 percent had diabetes. The median duration of hemodialysis 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 ratio for death is shown in Table 1Table 1
Relation of the Patients' Characteristics to the Odds Ratio for Death.. After a mean age of 59 years, each year of advancing age was associated with an approximately 3 percent increase in the odds ratio. The odds ratios were higher among whites and diabetic patients. A similar analysis was performed that included the serum albumin concentration and the urea reduction ratio in the model. Both the serum albumin concentration and the 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 in this model. Given the range of times during which hemodialysis was performed (lower-quartile group, three hours; upper-quartile group, four hours), the length of treatment was not associated with a risk of death.As compared with a reference urea reduction ratio of 65 to 69 percent, values less than 60 percent were associated with a higher odds ratio for death (Table 2Table 2
Adjusted Risk of Death According to the Urea Reduction Ratio or Serum Albumin Concentration in Patients with End-Stage Renal Disease.). The serum albumin concentration was an even more powerful predictor of risk. As compared with patients who had serum albumin concentrations ranging from 4.0 to 4.4 g per deciliter, patients with serum albumin concentrations below 4.0 g per deciliter had increased odds ratios for death (Table 2).The patients were also grouped according to their combined values for urea reduction ratio and serum albumin concentration (Figure 1Figure 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.). Considering patients with a urea reduction ratio of ≥ 65 percent and a serum albumin concentration of ≥ 4.0 g per deciliter as the reference group, lower serum albumin concentrations were associated with significant increases in the risk of death for all the urea-reduction-ratio groups. The odds ratios increased at lower urea reduction ratios for the patients who had serum albumin concentrations of 3.5 to 3.9 g per deciliter or 3.0 to 3.4 g per deciliter, but not for the patients whose serum albumin concentrations were ≥ 4.0 or <3.0 g per deciliter. Thus, both the urea reduction ratio and serum albumin concentration were important determinants of the odds of death, but factors associated with the serum albumin concentration had a greater effect.Frequency Distribution and Temporal Trends for Urea Reduction Ratio Values and Serum Albumin Concentrations
The frequency distribution of the mean urea reduction ratio for each patient from June through September 1990 is shown in Figure 2Figure 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 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, 33 percent of the patients had urea reduction ratios that were below 55 percent, and 16 percent had values below 50 percent. For individual patients, the average urea reduction ratios from June through September 1990 were not significantly different from the values obtained from October 1990 through March 1991 (58 ±10 percent vs. 59 ±9 percent, P>0.05).The distribution of values for the serum albumin concentrations for each patient from June through September 1990 is shown in Figure 2. The mean serum albumin concentration was 3.8 ±0.4 g per deciliter. Sixty percent of the serum albumin concentrations were below 4.0 g per deciliter, 13 percent were below 3.5 g per deciliter, 2 percent were below 3.0 g per deciliter, and less than 1 percent were below 2.5 g per deciliter. There was no correlation between the serum albumin concentration and the urea 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 albumin concentration. During the early period, preliminary data concerning the influence of the urea reduction ratio and the serum albumin concentration on the risk of death among patients treated with hemodialysis were disseminated to facility medical directors, and they were urged to respond to these data in their individual facilities. The mean urea reduction ratio increased from 58 ±9 percent during the early period to 62 ±8 percent during the late period (P<0.001). The lower-quartile group of urea reduction ratios increased from 53 to 56 percent (Figure 3Figure 3
Trends in Median Urea Reduction Ratios in Patients with End-Stage Renal Disease Treated with Hemodialysis from October 1990 through March 1992.). The mean serum albumin concentration during this interval decreased from 3.9 ±0.3 to 3.7 ±0.3 g per deciliter (P<0.001). Each patient's early-period urea reduction ratio and serum albumin concentration were subtracted from the corresponding late-period values. Although the correlation of the change in serum albumin with the change in the urea reduction ratio was direct and statistically significant (r = 0.044, P<0.001), the r2 statistic (0.002) indicated a weak association.We identified a subgroup of 178 patients in whom the urea reduction ratio was ≤ 50 percent during the early period and increased to ≥ 60 percent in the late period. The mean urea reduction ratio in this group increased from 43 ±3 percent in the early period to 67 ±8 percent in the late period, and the mean serum albumin concentration fell from 3.8 ±0.5 to 3.7 ±0.4 g per deciliter (P = 0.01). In contrast, we identified 37 patients with urea reduction ratios of ≥ 65 percent in the early period that fell to ≤ 55 percent during the late period. The mean urea reduction ratios during the early and late periods in this group were 71 ±14 percent and 50 ±7 percent, respectively. The mean serum albumin concentrations in these patients were 3.7 ±0.5 and 3.6 ±0.5 g per deciliter, respectively (P not significant). There was no correlation in the magnitude of the change in serum albumin concentration between the patients in whom the urea reduction ratio increased and the 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 reduction ratio in the statistical model was associated with a reduction in the odds ratio for death in the diabetic patients. Hence, we evaluated potential differences in the distributions of the serum albumin concentration and urea reduction ratio in patients with and those without diabetes. Women had higher urea reduction ratios than men during treatment (61 ±9 vs. 56 ±9 percent, P<0.001), and nondiabetic patients had higher values than diabetic patients during treatment (59 ±10 vs. 57 ±10 percent, P<0.001). The nondiabetic patients had higher 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 that inadequate dialysis and poor nutrition are major factors contributing to the excessive mortality of patients treated with hemodialysis in the United States. We used the urea reduction ratio as a measure of the adequacy of dialysis8-12,16. When the urea reduction ratio was included in the statistical model, the odds of death were not associated with the duration of dialysis treatments (range, three to four hours) commonly used in these patients. This finding seems to contradict previous studies suggesting that treatment time itself is a critical determinant of survival for patients undergoing hemodialysis6,7. In these earlier studies, however, no direct measure of solute clearance was reported. The National Cooperative Dialysis Study4,5,17 also found that the length of dialysis had a significant effect on patient survival,5,18 whereas we did not. Our results suggest that the intensity of treatment should be sufficient to result in a urea reduction ratio of ≥ 60 percent, whereas a urea reduction ratio of >50 percent was implied to be adequate by the National Cooperative Dialysis Study4,5,9,17. The majority of patients currently treated with hemodialysis would not have been eligible to participate in the cooperative study because of age and coexisting conditions such as diabetes mellitus19,20. Our data suggest that this patient population may require more intensive dialysis to achieve greater clearance.
The increased odds ratio for death with urea reduction ratios below 60 percent and the original frequency distribution of values for the urea reduction ratio suggest that dialysis mortality may decrease with more intensive dialysis. Beginning in late 1990, National Medical Care provided facilities and medical directors with local and national data about the odds ratio for death and the distribution of urea reduction ratios. A subsequent upward trend in urea reduction ratios was probably the result of a revised definition of adequate dialysis -- that is, a target urea reduction ratio of ≥ 60 percent.
Like the authors of previous studies of patients with renal and other diseases,7,8,21,22 we found that the serum albumin concentration was the most powerful predictor of death. However, the urea reduction ratio and serum albumin concentration were independent predictors. For the approximately 60 percent of patients at risk because of a low serum albumin concentration (<4.0 g per deciliter), the odds ratios associated with inadequate nutrition (as reflected by low serum albumin concentrations) may be magnified by the presence of suboptimal dialysis. Some investigators suggest that augmentation of urea clearance will improve a patient's nutritional status23,24. We did not find this to be the case, and the correlation between the adequacy of dialysis and nutritional status (as measured by serum albumin concentration) was weak. Of course, the persistence of a low serum albumin concentration despite an increased urea reduction ratio could have been due to many factors other than malnutrition, including hepatocellular dysfunction, hypervolemia, and exposure to pyrogenic cytokines.
Our analysis confirms the observation that differences in nutrition and the intensity of dialysis explain part of the excess mortality among diabetic patients with end-stage renal disease25. Patients with diabetes have lower serum albumin concentrations and urea reduction ratios than nondiabetic patients. Possible factors contributing to the lower urea reduction ratios in these patients include compromised blood flow during a dialysis treatment as a result of hemodynamic instability, poor flow through the vascular access for hemodialysis, the provision of less intensive dialysis because of inappropriate reliance on low prehemodialysis blood urea nitrogen or serum creatinine values as measures of the adequacy of dialysis, and the prescription of suboptimal therapy because of prejudices that excessive morbidity and mortality are unavoidable in diabetic patients. Women treated with hemodialysis had higher urea reduction ratios and a reduced odds ratio of death. Physicians may have prescribed dialysis treatment independently of a patient's body size, resulting in increased urea reduction ratios in women, who are generally smaller than men.
Because our study was retrospective, a causal relation between the urea reduction ratio, serum albumin concentration, or both and the risk of death should be inferred from these data with caution. However, these results may have practical implications for the care of patients being treated with hemodialysis. Nephrologists may have only limited success in improving nutritional status by augmenting dialysis. Thus, both these components of care must be monitored and independently corrected when they are suboptimal -- a urea reduction ratio below 60 percent and a serum albumin concentration of less than 4.0 g per deciliter. Strategies that improve solute clearance during hemodialysis include using more efficient dialyzers, increasing the time of hemodialysis, and optimizing the blood and dialysate flows during each dialysis treatment. The nutritional status of patients undergoing hemodialysis should be monitored routinely, and when inadequacies are identified, corrective measures must be instituted. These measures include augmenting the patient's caloric intake by providing hyperalimentation during dialysis treatments, correcting dental deficiencies, improving gastrointestinal abnormalities, and supplementing finances for nutritious foods.
Supported in part by a grant (DK45656-01) from the National Institute of Diabetes and Digestive and Kidney Diseases (to Dr. 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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