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NDT Advance Access published online on June 27, 2007
Nephrology Dialysis Transplantation, doi:10.1093/ndt/gfm374
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© The Author [2007]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Time to target haemoglobin concentration (11 g/dl)—risk of hospitalization and mortality among incident dialysis patients

Areef Ishani1,2, Haifeng Guo1, David T. Gilbertson1, Jiannong Liu1, Stephan Dunning1, Allan J. Collins1,2,3 and Robert N. Foley1,2,3

1Chronic Disease Research Group, Minneapolis Medical Research Foundation, 2Department of Medicine, University of Minnesota and 3Department of Medicine, Hennepin County Medical Center, Minneapolis, MN, USA

Correspondence and offprint requests to: Areef Ishani, MD, MS, Chronic Disease Research Group, Minneapolis Medical Research Foundation, 914 South 8th Street, Suite S-253, Minneapolis, MN 55404, USA. Email: aishani{at}cdrg.org



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 
Background. Haemoglobin levels <11 g/dl are associated with increased costs, morbidity and mortality. We aimed to determine if time required to reach 11 g/dl was associated with increased risk of hospitalization or death among incident dialysis patients.

Methods. We studied 29 131 patients initiating dialysis in 2002 and surviving ≥9 months. Demographic, comorbid and health care use data were extracted from Medicare claims from months 4–9 post-dialysis initiation. Logistic regression was used to calculate a propensity score for odds of longer than mean time to target. Proportional hazard models were used to assess effects of longer time on hospitalization and death. Other models were stratified for quartile of propensity score.

Results. Mean time to target haemoglobin was 1.3 months and 36% of participants required longer. These were more likely to be younger and minority, to use a dialysis catheter, and to have more comorbidity and hospitalization days during the entry period. Longer time to target was associated with increased risk for hospitalization (hazards ratio 1.15; 95% confidence interval 1.12–1.19) and mortality (1.26; 1.20–1.33) in the following year. Associations did not change when stratified by quartile of propensity score.

Conclusions. Longer time required to reach the target haemoglobin level was associated with significantly higher risk of hospitalization and mortality. Whether observed associations resulted from residual confounding by more severe illness remains unclear. Future trials should determine if rapidity of haemoglobin correction influences outcomes.

Keywords: anaemia; haemoglobin; hospitalization; mortality; renal dialysis



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 
Anaemia is common among end-stage renal disease (ESRD) patients, with more than 95% of individuals on dialysis receiving some form of anaemia treatment [1]. In 1997, the National Kidney Foundation Dialysis Outcomes Quality Initiative (K/DOQI) recommended a haemoglobin target range of 11–12 g/dl [2]. Since publication of these guidelines, mean haemoglobin concentrations have increased. Associated with this increase has been a concomitant increase in erythropoietin and parenteral iron use [3,4]. It is well established that treatment of anaemia is associated with an improved quality of life [5–7]. However, studies evaluating the effect of anaemia treatment with recombinant human erythropoietin on regression of left ventricular hypertrophy have had conflicting results [8–13]. Numerous observational studies have demonstrated an association between haemoglobin concentrations <11 g/dl and cost, morbidity and mortality [14–21]. Whether longer time required to attain guideline haemoglobin targets in incident dialysis patients is associated with adverse health outcomes remains unknown. Using an incident dialysis cohort, we aimed to determine if longer time below the guideline haemoglobin target of 11 g/dl was associated with increased risk of death or all-cause hospitalization in the subsequent year.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 Acknowledgements
 References
 
Measurements
The Renal Beneficiary Utilization System identification and death notification files and Centers for Medicare & Medicaid Services Institutional Inpatient Standard Analytical Files were used. Comorbid conditions and health care utilization were identified from Medicare Part A institutional claims and Part B physician/supplier claims using International Classification of Diseases, Ninth Revision, Clinical Modification and Physicians’ Current Procedural Terminology codes. Haemoglobin data were obtained from the Medicare erythropoietin claims files and were converted by multiplying the hematocrit values by 0.33. For this analysis, Medicare charges generated by each patient during months 4 through 9 after dialysis initiation were used to define baseline characteristics and baseline health care utilization (hospital days and cumulative erythropoietin dose). Cumulative erythropoietin dose was determined by summing individual claims data for each patient over the 6-month observation period (months 4 through 9 after dialysis initiation). Cumulative dose was used to define exposure to erythropoietin as it represents the integrated exposure over time.

Outcomes
Patients were longitudinally followed for up to 1 year beginning 10 months after initiating dialysis. Mortality and first hospitalization data were obtained. The follow-up time for each event was defined as the time from the start of the study outcome follow-up period (month 10 of dialysis) until the outcome (death or hospitalization) or 1 year. For all models, individuals were censored if they obtained a kidney transplant or had a change in their primary form of health insurance. For the hospitalization analysis, individuals were additionally censored if they were lost to follow-up. Deaths were ascertained from the ESRD Death Notification (Centers for Medicare & Medicaid Services form 2746). Information on first hospitalizations during the follow-up period was obtained from the Medicare Part A claims data.

Statistical analysis
Continuous variables were compared using t-tests; categorical variables were compared using chi-squared testing. Logistic regression was used to define the odds of being included in our final study cohort.

Propensity score
Number of months with haemoglobin concentration below 11 g/dl was calculated for each patient. The unit of analysis for the overall study was the effect of having greater than the mean number of months with haemoglobin below 11 g/dl. A logistic regression model was used to calculate a propensity score, the estimated probability that an individual would require more than the mean time to reach the target haemoglobin concentration. Propensity scores are used to ‘pseudo-randomize’ individuals on measured confounders [22]. The predictors in the model for the propensity score were age, gender, race, ethnicity, comorbid conditions during the entry period, number of hospital days during the entry period, dialysis catheter use, total erythropoietin dose and a number of interactions between covariates.

Cox models
Cox proportional hazard models were used to assess the associations between time to target haemoglobin concentration (11 g/dl) and time to first hospitalization or all-cause mortality. Cox models were adjusted for age, gender, race, ethnicity, selected comorbid conditions during the entry period, number of hospital days during the entry period, dialysis catheter use and total erythropoietin dose. Additionally, Cox models were constructed by strata of propensity score quartile. Proportionality assumptions were checked for both the hospitalization and mortality models. For mortality, the assumption of proportionality was not violated. For hospitalization, the assumption was violated for age, race and ethnicity. Additional models were constructed that stratified for these three variables. Estimates from the stratified models were similar to the original model, and only the simplified model is presented.

Reported P-values are based on two-sided tests and were considered significant with {alpha} < 0.05. All analyses were performed using the SAS system for Windows, version 9.01 (SAS Institute, Cary, NC, USA). The Hennepin County Medical Center Human Subjects Research Committee approved this study.



   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 Acknowledgements
 References
 
The cohort comprised incident dialysis patients during calendar year 2002 who had Medicare Parts A and B as primary payer, survived at least 9 months after dialysis initiation, and had monthly haemoglobin values for 6 months.

Of the 57 144 patients who satisfied the 90-day rule [23] and had Medicare Parts A and B coverage, 56 689 (99.2%) maintained Medicare coverage for at least 6 months. Of these, 8630 patients died and 500 received a transplant or were lost to follow-up within the first 6 months, leaving 47 559 patients (83.2%). Those without a haemoglobin value every month for the 6-month entry period were then excluded (n = 18 376), as were those with any haemoglobin concentration value >18.3 g/dl or <3.3 g/dl (n = 36), leaving 29 147. Finally, 16 individuals were excluded because they did not have an allowable payment during the entry period. The final study cohort included 29 131 dialysis patients incident during 2002 (51.0%).

Table 1 compares the baseline characteristics of included and excluded individuals and gives the multivariate odds of being included. Included patients were more likely to be older and female, to use a dialysis catheter, to have been hospitalized between 1 and 7 days during the entry period (but less likely to have been hospitalized more than 7 days) and to have a greater prevalence of all measured comorbid conditions.


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  		Table 1. Comparison of patient characteristics for those included and excluded by less than 6 months of haemoglobin values

 
Of the entire cohort, 10 468 (35.93%) had more than the mean number of months with haemoglobin concentration below the target value (Tables 2 and 3). These patients were more likely to be younger, female and black or Hispanic; to use more erythropoietin; and to have more hospital days during the enrolment period, a dialysis catheter and more comorbid conditions. They also had significantly lower haemoglobin values at dialysis initiation compared with patients who required less time to reach target haemoglobin concentrations (9.66 ± 1.76 vs 9.90 ± 1.76, P < 0.001). Table 4 demonstrates the baseline characteristics of the cohort when stratified by propensity score. Within each propensity score strata, individuals who needed a longer time to achieve target haemoglobin concentrations are more similar to those who needed a shorter time.


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  		Table 2 Mean number of months below target haemoglobin value, mean haemoglobin values

 

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  		Table 3 Patient characteristics

 

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  		Table 4 Patients characteristics by quartile of propensity score (c-statistic = 0.706)

 
Rates of hospitalization and mortality were calculated for the overall cohort and stratified by quartile of propensity score. The overall rate of hospitalization was 121.5 per 100 patient-years and the overall rate of mortality was 25.1 per 100 patient-years. There was a monotonic increase in the rates of both hospitalization and mortality by quartile of propensity score (Figure 1).


Figure 1
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  		Fig. 1. Raw rates of first hospitalization and mortality per 100 patient-years by quartile of propensity score.

 
In the overall adjusted Cox model, individuals with more than the mean number of months with a haemoglobin concentration below target were more likely to be hospitalized (hazard ratio 1.15; 95% confidence interval 1.12–1.19) and more likely to die (1.26; 1.20–1.33) during the 1-year follow-up period (Table 5). The risk of hospitalization and death associated with more than the mean number of months with haemoglobin concentration below target was similarly increased in models stratified by propensity score quartile (Figure 2).


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  		Table 5 Relative risk (RR) for first all-cause hospitalization and all-cause mortality

 

Figure 2
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  		Fig. 2. Adjusted relative risk (RR) for first all-cause hospitalization and all-cause mortality by quartile of propensity score, adjusted for all variables in Table 5.

 


   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
Acknowledgements
 References
 
With an incident dialysis cohort followed prospectively using Medicare claims data, we found that longer time required to achieve target haemoglobin values was associated with increased risk for subsequent hospitalization and mortality. Longer time required was more likely in patients with more comorbidity and more frequent and longer hospitalizations, in those using catheters as their dialysis access and in those with higher erythropoietin doses. In addition to standard analytic techniques using Cox models, we attempted to further adjust for these differences using a propensity score for time required to achieve target haemoglobin values. Within strata of propensity scores, individuals requiring a longer time to achieve target haemoglobin values were more similar to those requiring less time, though some differences persisted. After stratifying for propensity score, time to target haemoglobin concentration continued to be associated with both mortality and first hospitalization, with similar increases in risk across propensity score quartiles.

Numerous observational studies have demonstrated that below-target haemoglobin concentrations among both incident and prevalent dialysis patients are associated with increased risks of mortality and hospitalization and higher costs [14–21]. The results of observational studies are in contrast to those from randomized controlled trials, which generally have not demonstrated survival or hospitalization benefits. Two studies, while not definitive, had to be stopped prematurely because of an increased risk of adverse events in those randomized to supra-target haemoglobin concentrations [7,24]. Numerous controlled trials have demonstrated that treatment of anaemia improves quality of life. Given the prevailing evidence and the current K/DOQI guidelines, clinicians have become more aggressive in treating anaemia to target levels with overall haemoglobin concentrations improving over time among US dialysis patients [25]. These improvements have been demonstrated using both cross-sectional and incident populations [26]. While overall haemoglobin concentrations are improving, it is unknown if the time to target haemoglobin concentrations among incident dialysis patients impacts outcomes. The results of our study suggest that, in an incident dialysis cohort, a longer time to target haemoglobin concentration is associated with an increased risk of mortality and hospitalization.

Several factors contribute to the time required to attain target haemoglobin concentrations among incident dialysis patients. These include the starting haemoglobin concentration, which frequently is dependent on the use or non-use of erythropoietin in the period before beginning dialysis [27]. Additionally, heterogeneity in the quality of care at US dialysis facilities may contribute to the increased time to target haemoglobin concentrations for some patients. A recent Medicare sample demonstrated that between 67% and 81% of patients achieved the lower boundary of the K/DOQI target range [28]. This variability is likely due in large part to institutional policies that are likely modifiable [29]. Also, physician-related factors, such as lack of aggressiveness in changing doses in response to previous haemoglobin concentration readings, may also contribute. Finally, other influencing factors include variability in patient response to erythropoietin dose, adequacy of iron stores, use of catheters for vascular access, inflammatory and infectious disease processes, haemodialysis adequacy and gastrointestinal bleeding [30]. Among our incident cohort, we found an association between catheter use at baseline and the likelihood of a longer time required to achieve target haemoglobin concentrations. Previous studies have suggested that the use of occult catheters for vascular access may be a factor in erythropoietin resistance [31]. Whether the catheter itself leads to the resistance or is a marker of greater comorbidity is unknown. Additional studies are required to determine if removal of catheters or prevention of their use leads to improved erythropoietin sensitivity and a faster time to target haemoglobin concentration.

Limitations
Baseline imbalance
Our study results are limited in several ways. Our primary hypothesis was that individuals who need a longer time to reach target haemoglobin concentration would have an increased risk for hospitalization and death during the follow-up period. However, these individuals were at greater risk for these outcomes based on baseline characteristics. They tended to have more comorbidity and higher rates and duration of hospitalization during the entry period than those with a shorter time to target haemoglobin concentration. It is no surprise that individuals with more comorbidity and hospitalizations during the entry period would have more hospitalizations and a higher risk of death in the follow-up period. We attempted to adjust for these baseline imbalances using a propensity score, which modelled time to achieving target haemoglobin concentration. The propensity score has been previously demonstrated to improve the predictive ability of Cox models [32]. In both the fully adjusted Cox model and within each stratum of propensity score, the risks of mortality and hospitalization were similar for those requiring a longer time to target haemoglobin concentration.

Observational design
The second major limitation of our analysis is its reliance on observational design; while this study can test the associations between time to target haemoglobin concentrations and outcomes, it cannot determine whether these associations are causal.

Generalizability
Our study is also limited regarding the generalizability of the study cohort. Our final cohort comprised 51% of incident dialysis patients during calendar year 2002. Patients were excluded for two primary reasons: they did not survive for 9 months after initiating dialysis or they did not have monthly haemoglobin measures from months 4 to 9. The first reason for exclusion could potentially lead to survivor bias. The second reason may impact the generalizability of our results. Because of these exclusion criteria, included patients differed significantly from excluded patients on key variables such as age, race, vascular access type and comorbid conditions. The effect of these restrictions on our overall study results is unclear.

An additional potential concern is the increased risk of access thrombosis associated with too rapid a rate of haemoglobin correction. Two randomized controlled trials targeting aggressive correction of haemoglobin have demonstrated an increased risk of access thrombosis [7,33]. The CHOIR trial recently demonstrated an increased risk of the composite endpoint of cardiovascular disease and death among individuals randomized to a higher haemoglobin target of 13.5 g/dl [24]. Given these uncertainties, it seems prudent for future randomized controlled trials to determine if aggressive treatment of haemoglobin among incident dialysis patients, without exceeding the target range, can improve longitudinal outcomes.

Whether time below haemoglobin target itself is associated with a greater risk of mortality or hospitalization, or whether the risk relates to residual confounding from unmeasured factors or unadjusted comorbid conditions, remains unclear. Should time required to achieve target haemoglobin concentrations be associated with adverse health outcomes, then interventions aimed at improving individual responses to erythropoietin, decreasing resistance to erythropoietin, or more aggressively treating anaemia before or at the time of dialysis initiation may lead to a decrease in hospitalizations and mortality.



   Acknowledgements
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
References
 
This study was supported by a research contract with Roche Laboratories, Nutley, NJ, USA. The contract provides for the authors to have final determination of the manuscript content. D.T.G., A.J.C. and R.N.F. have received consulting fees from Roche. The authors wish to thank Chronic Disease Research Group colleague Nan Booth, MSW, MPH for manuscript editing.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Acknowledgements
 References
 

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Received for publication: 16. 2.07
Accepted in revised form: 21. 5.07


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