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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 62:1300-1305 (2007)
© 2007 The Gerontological Society of America

Is Modification of Diet in Renal Disease Formula Similar to Cockcroft–Gault Formula to Assess Renal Function in Elderly Hospitalized Patients Treated With Low-Molecular-Weight Heparin?

Isabelle Gouin-Thibault, Eric Pautas, Isabelle Mahé, Clotilde Descarpentries, Valérie Nivet-Antoine, Jean-Louis Golmard and Virginie Siguret

1 Hematology Laboratory, Charles Foix Hospital (AP-HP), Ivry sur Seine, France.
2 Geriatric Department, Charles Foix Hospital (AP-HP), Ivry sur Seine, France.
3 INSERM U765, Paris Descartes University, Paris, France.
4 Internal Medicine Department A, Lariboisière Hospital (AP-HP), Paris, France.
5 Biochemistry Laboratory, Charles Foix Hospital (AP-HP), Ivry sur Seine, France.
6 Physiology, Paris Descartes University, Paris, France.
7 Biostatistics Department, Pitié-Salpêtrière Hospital (AP-HP), Paris, France.
8 Paris 6 University, Paris, France.

Address correspondence to Isabelle Gouin-Thibault, PhD, Charles Foix Hospital (AP-HP), Hematology Laboratory, 7 Avenue de la République, 94205 Ivry sur Seine, cedex, France. E-mail: isabelle.gouin{at}cfx.aphp.fr


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. Repeated administration of low-molecular-weight heparin (LMWH) to elderly patients with an impaired renal function may lead to an accumulation effect with an increased risk of bleeding. In this setting, Cockcroft–Gault (CG) is the most widely used formula for glomerular filtration rate (GFR) estimation. In hospitalized patients over the age of 70, the six-variable Modification of Diet in Renal Disease (MDRD) formula was compared with the CG formula to detect patients with renal impairment who are at higher risk of bleeding when treated with LMWH.

Methods. We combined retrospective data from 366 patients aged 86.2 ± 6.6 years, treated with LMWHs. CG and MDRD GFR estimates were compared using the Bland–Altman method and the agreement between the two formulae by the {kappa} coefficient.

Results. The mean CG and MDRD estimated GFR were 45.9 ± 21.9 mL/min and 75.6 ± 32.6 mL/min/1.73 m2, respectively, with a mean bias of 29.6 mL/min. The concordance between the formulae to classify patients into stages of kidney disease was very poor (weighted {kappa} = 0.17): 21.8% patients had severe renal function impairment with the CG formula versus 1.3% with the MDRD formula. In our population, the MDRD thresholds that would correspond to CG estimates of 30 mL/min and 60 mL/min were found at 63 mL/min/1.73 m2 and 80 mL/min/1.73 m2, respectively.

Conclusions. In elderly patients, GFR estimates using MDRD and CG formulae differ widely and identify different numbers of individuals with kidney disease. Prospective comparative studies are needed to validate these formulae and their different thresholds to better detect elderly patients at higher risk of bleeding when treated with LMWH.

THE incidence of venous and arterial thromboembolism increases with age. As the population ages, the number of older patients that would benefit from anticoagulant treatment at therapeutic or prophylactic dose increases steadily. Low-molecular-weight heparins (LMWHs) are widely used in these situations, but as they are mainly excreted by the kidney, repeated administration to elderly patients with an impaired renal function may lead to an accumulation effect with an increased risk of bleeding. The pharmacokinetic effect of impaired renal function may differ among LMWHs, and the exact cutoff value in terms of creatinine clearance probably varies for different LMWHs, but a safe threshold of 30 mL/min, calculated using Cockcroft–Gault (CG) formula, has been proposed by Hirsh and Raschke (1). In these patients with renal function impairment, monitoring of anti-Xa activity may be recommended to detect an accumulation (1), and dose adjustment according to the level of glomerular filtration rate (GFR) could be considered, especially in case of curative treatment (2–4).

With an aging population and the decline in GFR with increasing age, it is of great importance to accurately estimate GFR in hospitalized elderly patients, especially in those older than 75 years, for drug-dosing purposes. Serum creatinine (sCr) is a poor screening test, leading to marked underinvestigation of renal failure in this population (5). Formulae that estimate GFR without requiring a timed urine collection have been developed. The CG formula is the most widely used formula (6), even though it is known to underestimate GFR in older patients (7). The six-variable Modification of Diet in Renal Disease (MDRD) formula and then its abbreviated four-variable version were recently described (8,9). The lack of required knowledge of body weight compared to the CG formula is a theoretical advantage and makes it easier to implement in a clinical laboratory. The MDRD formula was first designed in predominantly middle-aged patients. Its performance in elderly patients (75 years old or older) has not been extensively tested and has not yet been validated against a clearance measurement. Recent studies have found that CG and MDRD GFR estimates differ substantially in elderly patients and can not be used interchangeably to evaluate renal function in this population (10–12).

In the present study, we first checked the agreement between CG and simplified MDRD formulae in a cohort of elderly hospitalized patients treated with LMWHs. We then assessed the consequences of using the MDRD formula for GFR estimation in this population of elderly patients who were initially classified according to their GFR using the CG estimate. We also defined the threshold levels of the MDRD GFR estimate that would give the best fit with the CG GFR estimate, in our population, to detect patients with renal impairment who are at higher risk of bleeding when treated with LMWH. Finally, we evaluated if there was any relationship between peak anti-Xa activity level and GFR estimate using either the CG or MDRD formula.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
Patients and Treatment Regimen
In this retrospective study, we combined data from patients included in three previous published studies (13–15). Patients were older than 70 years and were hospitalized in acute, secondary, or tertiary care of the Charles Foix Hospital (Assistance Publique-Hôpitaux de Paris, France) or in the Department of Internal Medicine of the Lariboisière Hospital (Assistance Publique-Hôpitaux de Paris, France). All patients received LMWH either at prophylactic (enoxaparin 4000 IU daily) or at therapeutic doses (tinzaparin 175 IU/kg daily) for prevention or treatment of thromboembolic disease. Data recorded at inclusion included demographic characteristics, weight, and (sCr) value.

Laboratory Tests and Estimation of GFR
sCr was measured using a kinetic Jaffé colorimetric method, at the beginning of the treatment. GFR estimate was calculated as follows:

CG formula (Cockcroft) (mL/min) (6):

(140 – age (years)) x weight (kg) x (1.04 if female or 1.23 if male)/sCr (µM)
or (140 – age (years)) x weight (kg) x (0.85 if female)/72 x sCr (mg/dL)

Simplified MDRD (mL/min/1.73 m2) (9):

186 x (sCr (µM) x 0.0113)–1.154 x age (years)–0.203 x (1.212 if black) x (0.742 if female)
or 186 x sCr (mg/dL)–1.154 x age (years)–0.203 x (1.212 if black) x (0.742 if female)

Anti-Xa activity was measured at peak level as previously described (13–15).

Statistical Analysis
The agreement between CG and MDRD GFR estimates was analyzed using the Bland–Altman method, which is the difference between CG and MDRD formula plotted against their mean (16). Linear regression with the CG and MDRD difference as the dependent variable and the CG and MDRD mean as the independent variable was then performed.

The relationships between age, weight, and the difference between the CG and MDRD formulae, and between anti-Xa activity and GFR estimate were assessed using the Spearman correlation. The relationship between sex and the difference between the CG and MDRD formulae was tested using the Student t test.

The agreement between the two GFR estimation formulae to classify patients into different stages of kidney disease severity according to the K/DOQI CKD classification (Kidney Disease Outcomes Quality Initiative in patients with Chronic Kidney Disease), i.e., severe (< 30 mL/min), moderate (30–59 mL/min), and mild to normal (≥ 60 mL/min) (17) was analyzed by the weighted {kappa} coefficient.

Using an univariate logistic regression model, we defined MDRD values corresponding to CG GFR estimates of 30 mL/min and 60 mL/min. The MDRD thresholds were chosen such that sensitivity and specificity were approximately equal and around 80%. The statistical analysis was performed on SAS V8 software (SAS Institute Inc., Cary, NC).


   RESULTS
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 Abstract
 Methods
 Results
Discussion
 References
 
Three hundred sixty-six patients were included. The characteristics of the 366 patients are reported Table 1. Two hundred twenty-nine patients received a therapeutic dose of tinzaparin, and 137 received a prophylactic dose of enoxaparin. The clinical management and anti-Xa monitoring were based on CG GFR estimate. The mean estimated GFR was 45.9 ± 21.9 mL/min (range, 6–161) using the CG formula and 75.6 ± 32.6 mL/min/1.73 m2 (range, 8–255) using the MDRD formula.


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  		Table 1. Characteristics of Total Population (N = 366).

 
Figure 1A shows a Bland–Altman plot of the difference between MDRD and CG values against their mean. A linear regression was found with the following regression equation: y = 0.0487x – 0.0169 (p <.0001) (Figure 1A). As the variance increased with the increasing mean of GFR, we plotted the difference between the log values of MDRD and CG against the mean of the two log values (Figure 1B). The regression equation was the following: y = –0.077x – 0.818 (p <.0001). The analysis of the agreement between the two formulae showed a mean bias of 29.6 mL/min and a standard deviation of the differences of 21.3 mL/min. A strong positive correlation was found between age and the difference between the CG and MDRD formulae (p =.0008). A stronger negative correlation was found between weight and the difference between the CG and MDRD formulae (p < 10–4). No significant difference was found between sex and difference between the CG and MDRD formulae (p =.75). We then analyzed the agreement between the two GFR estimation formulae to classify patients into different stages of kidney disease severity (Figure 2, Table 2). The concordance was very poor with a weighted {kappa} of 0.17. Of the 366 patients we studied, 80 (21.8%) had a severe renal function impairment when using the CG formula compared to 5 (1.4%) when using MDRD formula (Table 2). Two hundred three (55.5%) and 110 (30%) had a moderate renal function impairment (i.e., 30 mL/min ≤ GFR < 60 mL/min) with the CG and MDRD estimate, respectively (Figure 2, Table 2). Finally, the MDRD thresholds that would correspond to CG estimates of 30 mL/min and 60 mL/min were found at 63 mL/min/1.73 m2 and 80 mL/min/1.73 m2, respectively.


Figure 01
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  		Figure 1. Bland–Altman plot of the difference between estimated simplified Modification of Diet in Renal Disease (MDRD) and Cockcroft–Gault (CG) glomerular filtration rate values (mL/min) against their mean (A) and the difference between the log values of MDRD and CG glomerular filtration rate estimates against the mean of the two log values (B). The 1.96 standard deviation (SD) limits (dotted line) are also plotted

 

Figure 02
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  		Figure 2. Classification of the study population according to Cockcroft–Gault (CG) and simplified Modification of Diet in Renal Disease (MDRD) glomerular filtration rate (GFR) estimates

 

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  		Table 2. Agreement Between the Two GFR Estimation Formulae to Classify Patients Into Three Stages of Kidney Disease Severity According to the Level of GFR, i.e., Severe (< 30 mL/min), Moderate (30–59 mL/min), or Mild to Normal (> 60 mL/min).

 
Two hundred ninety-one anti-Xa activity values were available for patients receiving a therapeutic dose of tinzaparin. The mean anti-Xa activity was 0.80 ± 0.29 IU/mL. No correlation was found between GFR estimates using either the CG or MDRD formula and anti-Xa values (r2 = 0.0065 and 0.0003, respectively). One hundred thirty-seven anti-Xa activity values are available for patients receiving a prophylactic dose of enoxaparin. The mean anti-Xa activity was 0.65 ± 0.24 IU/mL. No correlation was found between GFR estimates using either the CG or MDRD formula and anti-Xa values (r2 = 0.0104 and 0.0013, respectively).


   DISCUSSION
Top
 Abstract
 Methods
 Results
 Discussion
References
 
In our study, we found that in a population of elderly hospitalized patients (mean age 86.2 ± 6.6 years), GFR estimates using the MDRD and CG formulae differ widely, with the MDRD formula giving much higher values of GFR than the CG formula. As we did not perform a GFR measurement, we cannot state which formula is the most appropriate for GFR estimation in such elderly patients. True measurement of GFR is difficult in routine geriatric practice. Indeed, in frail elderly patients, age, comorbidity, and polypharmacy affect continence (18). Incontinence and cognitive impairment lead to difficulties with collection of a timed urine sample and thus introduce their own inaccuracies in GFR measurement. Even though it has been shown that the CG formula underestimates by about 20%–30% GFR in patients older than 80 years (19,20), it is one of the earliest and most widely used formulae published for GFR estimation, especially in clinical trials with LMWHs (3). International recommendations suggest that physicians should estimate the level of GFR from prediction equations such as MDRD or CG formulae (17). However, it is stated that new formulae should be validated against a gold standard body surface area (BSA)-corrected GFR measurement in a large sample of an appropriate population (17).

The six-variable MDRD formula was the product of a retrospective reanalysis of the MDRD study, a multi-center, controlled trial of effects of dietary protein restriction and blood pressure control on the progression of kidney disease. The GFR was determined, using 125I-iothalamate, in 1628 predominantly middle-aged patients with known kidney disease. An abbreviated four-variable version of the formula (which does not require albumin and urea measurements and which did not result in appreciable loss of accuracy) was then proposed and has become widely used (7).

Two studies, comparing the CG and MDRD formulae to a measured GFR, found that the MDRD formula was more precise and accurate than the CG formula in elderly patients (21,22); however, in those studies, the authors compared subgroups of patients over or under a cutoff of 65 years, thus the mean age of their elderly patients is about 72 years, i.e., 14 years younger than our patients. In a recent study, relationship of age to error of GFR prediction with CG and MDRD formulae compared to inulin clearance was analyzed (23). The authors found that the MDRD estimate was slightly more precise than the CG estimate. Unfortunately, among the 380 participants included in this latter study, only 35 were older than 65 years and none were older than 88 years (23). Indeed, the characteristics of our patients who are quite old and who have substantial comorbidity cannot be compared to those of the elderly patients included in these studies (21–23). In 52 older patients (mean age: 79.7 ± 4.9 years), Lamb and colleagues (24) found that MDRD overestimated GFR compared to 51Cr EDTA clearance measurement and did not improve the estimate of GFR compared with the CG formula. Finally, in a recent study performed on a cohort of patients similar to ours, Laroche and colleagues (10) found a poor concordance between MDRD and CG formulae for GFR estimation, with the mean MDRD value being 1.66 times that of the CG value. Our results are in agreement with the latter study. We found, as did others, that the magnitude of the difference between the two formulae is influenced by age and weight (11,12). As most of our patients are frail and have a low weight, the magnitude of the discrepancy is probably greater in our population than in a population of younger elderly patients (21,22). Interestingly, in a study including a large cohort of patients with a mean aged of 85 years, it was shown that the risk of having low GFR increased with age but depended upon whether the CG or MDRD formula was used. The prevalence of low GFR increased more dramatically when using the CG GFR estimate than when using the MDRD GFR estimate in patients older than 80 years (25).

The CG provides a GFR in terms of milliliters per minute. Ideally, the CG should be adjusted for BSA, but this adjustment does not reflect standard clinical practice. The MDRD provides a GFR in terms of mL/min/1.73 m2, consequently, at the extreme of body size such as in elderly patients whose BSA differs from the 1.73 m2 accepted BSA of an average individual, the MDRD formula should also be corrected for BSA (26). BSA adjustment requires weight and height values, which can not be measured accurately in elderly hospitalized patients and thus would limit the accuracy of the BSA-adjusted GFR estimates (7). However, not adjusting the CG GFR estimate for BSA in our study does not likely account for the wide difference we found using the two formulae, as similar differences in GFR estimates using BSA-corrected CG were found in a comparable population of elderly patients (mean age: 87 years; range 75–105) (10). Indeed, in that study, the mean BSA of the patients was 1.74 m2 and 1.61 m2 for men and women, respectively (10).

The existence of renal impairment is important to consider in the management of thromboembolic disease for the following reasons: (i) renal impairment has been shown to be an independent risk factor for bleeding, (ii) most anticoagulants undergo renal clearance and therefore may accumulate in the presence of renal impairment, and (iii) most anticoagulants do not have antidotes (27). In a recent meta-analysis, Lim and colleagues (3) showed that when a therapeutic dose of LMWH (enoxaparin) was used in patients with severe renal insufficiency—CrCl ≤ 30 mL/min, calculated with the CG formula in most studies—the risk for major bleeding events was increased 2- to 3-fold compared to risk in patients with CrCl > 30 mL/min. This situation is frequently encountered in a geriatric hospital, because 20%–30% of patients with thromboembolic disease requiring anticoagulant treatment have a severe renal impairment (14,28). In order to improve the safety of LMWHs in patients with renal impairment, monitoring of anti-Xa activity may be recommended to detect an accumulation effect (1,4). LMWH dose adjustment based on CrCl values have also been considered with some starting at CrCl of 50 mL/min (2,3). Hence, appropriate knowledge of the pharmacokinetic alterations associated with renal impairment and accurate estimation of GFR is of great importance to physicians treating patients with LMWH. In most of these studies, as well as in guidance of drug dosing, the non-BSA-adjusted CG formula was used.

Even though expert recommendations suggest monitoring anti-Xa activity to detect an accumulation in patients with renal function impairment, the relationship between anti-Xa level and clinical outcomes is not clear-cut and the appropriate anti-Xa threshold below which clinicians should be concerned about the risk for LMWH accumulation is not well defined (1). We had previously shown that there was no correlation between the CG GFR estimate and anti-Xa level in patients treated with a therapeutic dose of tinzaparin (14,15); in the present study, we found that there was no correlation between the MDRD GFR estimate and anti-Xa level, as well. Concerning patients treated with enoxaparin, Lim and colleagues (3) showed in a meta-analysis that when therapeutic doses of enoxaparin were used in patients with severe renal insufficiency, the risk for major bleeding events was increased and the anti-Xa activities were higher than in patients with no severe renal insufficiency. Unfortunately, in this meta-analysis, data were insufficient to assess the relationship between anti-Xa level and renal function for prophylactic doses of enoxaparin. In the present study, we found no correlation between GFR estimates using either the CG or MDRD formula and anti-Xa values in patients treated with prophylactic doses of enoxaparin.

In our population of very elderly hospitalized patients treated with LMWH, when using the MDRD formula, many patients would have not been considered at high risk (i.e., severe renal function impairment) or at moderate risk of bleeding (i.e., 30 mL/min ≤ GFR < 60 mL/min). Thus, as mentioned by others, we think that the use of the MDRD formula may lead to a misclassification of patients (26) and a lack of awareness of a high bleeding risk in patients treated with LMWH.

Because there is a growing interest in MDRD formula use (29) and before more data are available on its performance for estimating renal function in "very" elderly patients, we were interested in defining the threshold levels of the MDRD GFR estimate that would give the best fit with the CG GFR estimate to detect patients with renal impairment who are at higher risk of bleeding when treated with LMWH: a threshold of 63 mL/min/1.73 m2 for patients at high risk and of 80 mL/min/1.73 m2 for patients at moderate risk of bleeding were thus determined. These new and very different thresholds highlight the great discrepancy between the two GFR estimates in our elderly patients.

Conclusion
We found that, in a population of elderly hospitalized patients treated with LMWH, GFR estimates using the MDRD and CG formulae differ widely. So far, no data have validated one formula over the other to estimate GFR in very old patients, and studies to clarify which method is valid in this population are necessary.

We showed that the discrepancy between the two estimates leads to an absence of concordance and may cause misclassification of patients in terms of bleeding risk. In such a population, if the MDRD formula is used, then different thresholds than those defined with the CG formula may be used in order to better detect elderly patients at a higher risk of accumulation when treated with LMWH. The clinical relevance of these new thresholds should be validated in prospective studies in octogenarian and nonagenarian patients.


   Footnotes
Top
 Abstract
 Methods
 Results
 Discussion
 References
 
Decision Editor: Luigi Ferrucci, MD, PhD

Received October 25, 2006

Accepted January 13, 2007


   References
Top
 Abstract
 Methods
 Results
 Discussion
 References
 

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