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NDT Advance Access originally published online on November 1, 2005
Nephrology Dialysis Transplantation 2006 21(2):459-465; doi:10.1093/ndt/gfi213
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© The Author [2005]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Original Articles: Dialysis and Transplantation

Prevalence, clinical correlates and therapy cost of mineral abnormalities among haemodialysis patients: a cross-sectional multicentre study

Víctor Lorenzo1, Alejandro Martin-Malo2, Rafael Perez-Garcia3, José V. Torregrosa4, Nicanor Vega5, Angel L. M. de Francisco6 and Aleix Cases4

1 Nephrology Service, Hospital Universitario de Canarias, Santa Cruz de Tenerife, 2 Nephrology Service, Hospital Universitario Reina Sofía, Cordoba, 3 Nephrology Service, Hospital Gregorio Marañon, Madrid, 4 Nephrology Unit, Hospital Clinic I Provincial, Barcelona, 5 Nephrology Service, Hospital Universitario ‘Dr Negrín’, Las Palmas de Gran Canaria and 6 Nephrology Service, Hospital Universitario Marqués de Valdecilla, Santander, Spain

Correspondence and offprint requests to: Víctor Lorenzo, Division of Nephrology, University Hospital of Canary Islands, 38320 Ofra. La Laguna, Santa Cruz de Tenerife, Canary Islands, Spain. Email: viclorenzo{at}terra.es



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. This study evaluated the proportion of patients who met National Kidney Foundation Kidney Disease Outcomes Quality Initiative (NKF-K/DOQI) guidelines for mineral status, and assessed the cost of therapy for mineral management of patients under haemodialysis treatment in Spain.

Methods. Demographic and biochemical data were collected for 1312 patients undergoing standard three-times weekly maintenance haemodialysis at six Spanish centres during December 2003. Age, gender, diabetic nephropathy, haemodialysis duration, serum calcium, phosphorus, calcium–phosphorus product (Ca x P), and intact parathyroid hormone (iPTH) levels were monitored. Exploratory analyses of associations between demographic and biochemical parameters, were undertaken using bivariate and multivariate regression techniques.

Results. Mean age of patients was 62 years. 97% were Caucasian, 23% were diabetic. In total, 51% of patients received calcium binders, 21% sevelamer, 16% aluminium hydroxide, and 29% received no binders; 33% of patients received calcitriol. Prevalence of patients outside K/DOQI targets was: calcium 50%, phosphorus 46%; Ca x P 33%; iPTH 77%. Elevated phosphorus (>5.5 mg/dl) was independently associated with younger age [OR 0.972 (95% CI 0.963–0.980), P<0.001] and higher iPTH [OR 1.0005 (95% CI 1.0002–1.0008), P<0.001]. Elevated Ca x P (≥55 mg2 x dl2) showed a similar relationship. High iPTH levels (>300 pmol/l) were associated with female gender [OR 1.574 (95% CI 1.213–2.041), P<0.001], high serum phosphorus [OR 1.230 (95% CI 1.130–1.338), P<0.001], and longer duration of dialysis [OR 1.003 (95% CI 1.001–1.005), P<0.01]. Poorly controlled serum phosphorus, Ca x P and iPTH were associated with more expensive therapy for mineral management.

Conclusions. One in three haemodialysis patients in Spain remains above the upper target range defined in current mineral metabolism guidelines. This abnormal profile is more common in younger patients and females and therapy is more expensive in younger patients.

Keywords: calcium; calcium–phosphorus product; haemodialysis; parathyroid hormone; phosphate; renal osteodystrophy



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 References
 
End-stage renal disease is a chronic health care problem associated with multiple co-morbidities and escalating costs. Among patients receiving maintenance haemodialysis, 1-year mortality rates (unadjusted for patient demographic factors) have been estimated as 16% in Europe and 22% in the US [1]. Furthermore, after adjusting for age, gender, race and diagnosis of diabetes, mortality from cardiovascular disease is far higher in patients with kidney failure compared with the general population [2]. Recent evidence strongly suggests that abnormal mineral metabolism, in particular, a sustained increase in serum phosphorus and the calcium–phosphorus product (Ca x P), represents a risk factor for cardiovascular complications [3–5]. A large body of evidence also suggests that these abnormalities are associated with increased mortality and morbidity [6–9]. Thus, the true economic burden and social impact of end-stage renal disease may not as yet be fully appreciated.

Accordingly, as part of the Kidney Disease Outcomes Quality Initiative (K/DOQI) programme, the National Kidney Foundation (NKF) has recently published revised and more aggressive targets for lower serum phosphorus [3.5–5.5 mg/dl (1.13–1.78 mmol/l)], calcium [8.4–9.5 mg/dl (2.10–2.37 mmol/l)], Ca x P [<55 mg2/dl2 (<4.44 mmol2/l2)] and intact parathyroid hormone (iPTH) [150–300 pmol/l (150–300 ng/l)] levels [10]. However, several studies still report a high prevalence of hyperphosphataemia [6,9] indicating that the proportion of patients who achieve K/DOQI recommendations is very low. As part of the Dialysis Outcomes and Practice Patterns Study (DOPPS), between 1997 and 2000, K/DOQI targets were applied to data gathered from a sample of patients from seven countries, Spain included [9]. All of the target levels of the K/DOQI were achieved by only 5.5% of patients, suggesting that adoption of the guidelines may require new approaches for the management of secondary hyperparathyroidism and mineral abnormalities. It also seems evident that the application of these guidelines remains inconsistent, although the therapeutic approach has moved towards the goal of restricting the calcium burden.

Epidemiologic studies evaluating mineral status and management in Spanish haemodialysis patients after implementation of the K/DOQI guidelines [10] have not previously been reported. The present study was, therefore, undertaken to describe the characteristics of mineral abnormalities in a cohort of treated haemodialysis patients from Spain, and to explore specific associations among demographic and biochemical parameters. We also conducted an economic analysis to document the cost of therapy and determine if this was associated with mineral status.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 References
 
Six dialysis centres from different regions in Spain participated in this cross-sectional study. All patients older than 18 years were included in the analysis. Parathyroidectomized patients constituted less than 5% and were also included in the analysis. The dialysis centres and the corresponding number (n) of patients from each centre were: the Hospital Universitario de Canarias of Tenerife (n = 201); Hospital Clinic I Provincial of Barcelona (n = 220); Hospital Universitario ‘Reina Sofía’ of Cordoba (n = 351), Hospital ‘Gregorio Marañon’ of Madrid (n = 225); Hospital Universitario ‘Marqués de Valdecilla’ of Santander (n = 127) and Hospital Universitario ‘Dr Negrín’ of Las Palmas de Gran Canaria (n = 188).

All patients were on 3.5–5.0 h standard bicarbonate haemodialysis, thrice-weekly, with a prescribed percent urea reduction equal to or higher than 65%. Dialysers were not reused. Phosphate binders were used according to individual medical criteria. In general, calcium-based phosphate binders were used as first therapy, and sevelamer alone or combined with calcium binders was regularly the second option. Aluminium hydroxide was recommended in resistant cases. The dialysate calcium concentration was adjusted in the range of 5–7 mg/dl, in order to facilitate the use of phosphate binders and calcitriol. Demographic and clinical data were collected from patients during December 2003. Parameters monitored for each patient included age, gender, underlying disease, date of first dialysis, total serum calcium, phosphorus and iPTH levels. Information was also recorded regarding therapy with phosphate binders and vitamin D analogues. Total calcium and phosphorus were measured by automated methods. Intact PTH was measured by immunoradiometric assay (IRMA) (Nichols Institute, San Juan Capistrano, CA, normal range 10–65 pmol/l). All blood samples were collected immediately before the midweek dialysis session.

A cost analysis was undertaken as a means of evaluating the economic burden of mineral regulating therapy. Drug costs were based on average wholesale prices in Spain. The distribution of therapy costs was compared among patients with different biochemical profiles based on predefined ranges of Ca x P and iPTH.

Statistical analyses
Results are expressed as means±SD. Significant differences were defined as P<0.05. Bivariate correlation analysis and one-way analysis of variance were used to estimate significant associations for biochemical and demographic parameters. Post-hoc analysis was performed using the Tukey test. Analyses to determine the independent predictors of phosphorus, Ca x P and iPTH levels over the target levels of the K-DOQI guidelines were completed using logistic regression analysis while adjusting for age, duration of dialysis, diabetes (yes/no) and gender. These analyses were conducted using SPSS (v12.0) for Windows (SPSS Inc., Chicago, USA). A two-way analysis of variance was applied to compare cost means between Ca x P (2 groups) and iPTH (4 groups), on costs. Post-hoc probabilities were obtained with Scheffe test. These analyses were performed using Statistica 5.5 (Tulsa, OK, USA).



   Results
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 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 References
 
Clinical and demographic characteristics
The demographic, biochemical and therapeutic data of the 1312 patients included in the study are shown in Table 1. In total, 71% of the patients received phosphate binders as follows: calcium-based 51%, sevelamer 21% and aluminium hydroxide 16%. Some of these patients were on double or triple therapy. The proportion of patients with double therapy was as follows: calcium binders + sevelamer 6.7%; calcium binders + aluminium hydroxide 5.7%; and sevelamer + aluminium hydroxide 1.5%. Triple therapy was prescribed to 1.5% of the patients. Intravenous or oral calcitriol was the only vitamin D derivative used, and was prescribed in 33% of the patients.


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  		Table 1. Demographic, biochemical and therapeutic data for all 1312 haemodialysis patients

 
Adherence to K/DOQI targets
Figure 1 shows the proportion of patients classified according to the recommended K/DOQI guidelines cut-off levels, i.e. in three groups for calcium and phosphorus, in two groups for Ca x P product, and in four groups for iPTH. This analysis indicates a relatively high prevalence of patients over K/DOQI targets: calcium [>9.5 mg/dl (>2.37 mmol/l)] 43%, phosphorus [>5.5 mg/dl (>1.78 mmol/l)] 34%, Ca x P [≥55 mg2/dl2 (≥4.44 mmol2/l2)] 33%, and iPTH [>300 pmol/l (300 ng/l)] 35%. A notable finding was that 42% of patients had PTH values below the target range [<150 pmol/l (150 ng/l)]. As shown in Table 2, only 16% of patients had the ideal combined target of serum phosphorus ≤5.5 mg/dl and iPTH between 150 and 300 pmol/l. A similar picture was observed when Ca x P were assessed instead of phosphorus levels, using a cut-off of 55 mg2/dl2, with only 17% of patients achieving target levels.


Figure 1
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  		Fig. 1. Proportion (%) of patients achieving K/DOQI target levels for calcium (8.4–9.5 mg/dl), phosphorus (3.5–5.5 mg/dl), Ca x P (<55 mg2/dl2), and iPTH (150–300 pmol/l).

 

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  		Table 2. Proportion (%) of patients assigned to groups of iPTH (4 groups), serum phosphorus (2 groups) and Ca x P (2 groups)

 
Association between demographic data and biochemical markers
Univariate analysis demonstrated a negative correlation between age and mineral parameters. Patients were divided into four groups of age in years: <55, 55–64, 65–74 and ≥75. The mean serum phosphorus, Ca x P and iPTH levels decreased with age (Figure 2). There was no significant difference in the mean serum calcium concentration among the different age groups. In addition, levels of iPTH were significantly higher in female (369±414 pmol/l) than in male patients (296±390 pmol/l; P<0.001), and in non-diabetic (354±435 pmol/l) than in diabetic patients (249±280 pmol/l; P<0.001). A positive correlation was found between serum phosphorus and iPTH (r = 0.191; P<0.001), but serum calcium did not show a correlation with phosphorus or iPTH.


Figure 2
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  		Fig. 2. Serum phosphorus, Ca x P and iPTH levels separated according to age. Results are expressed as mean±SD. One-way analysis of variance, and post-hoc analysis using Tukey test were used to estimate significant associations for biochemical parameters and age.

 
A logistic regression analysis was used to obtain associations between demographic and biochemical parameters. Younger age and higher iPTH levels were associated with high levels of serum phosphorus (>5.5 mg/dl), and also Ca x P (≥55 mg2 x dl2), while serum calcium, the presence of diabetes, time on dialysis and gender did not influence these parameters. Female gender, the duration of dialysis and higher levels of phosphorus, but not serum calcium, were associated with high iPTH levels (>300 pmol/l) in this model (Table 3). Age nearly reached significance in this model.


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  		Table 3. Predictors of high levels of phosphorus, Ca x P and iPTH by logistic regression analysis. All models were adjusted for age, gender, time on dialysis and mineral parameters as required

 
Cost analysis
Figure 3 presents the cost per treatment-day according to mineral status and shows that patients with poorer control of Ca x P and iPTH received the most expensive therapy. Patients with Ca x P ≥55 mg2/dl2 and iPTH >300 pmol/l incur a 65–117% higher treatment cost than those patients who are controlled within the parameters according to K/DOQI guidelines. Table 4 shows individual costs of phosphate binders and calcitriol as a function of biochemical mineral profile. Individual costs by drug indicate that sevelamer, calcitriol and other binders represent 58, 36 and 7%, respectively, of the mean total price of the therapy for mineral disorders in this series. Differences were especially relevant in patients with iPTH 300–800 and Ca x P ≥ 55, where sevelamer markedly contributed to the higher cost of therapy. Calcitriol was more frequently used in patients with high iPTH. These results suggest that both formulations are often employed in resistant patients.


Figure 3
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  		Fig. 3. Cost of therapy per day as a function of mineral status – calcium–phosphorus product (Ca x P) and intact parathyroid hormone (iPTH). Two way analysis of variance was used, and post-hoc probabilities were obtained with Scheffe test. Analysis of variance showed an interaction effect between (Ca x P) and iPTH on cost (P = 0.005).

 

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  		Table 4. Relationship between mineral status according to K/DOQI targets for Ca x P product (2 groups) and iPTH (4 groups), and individual cost of treatment for maintenance of mineral balance

 
Figure 4 presents the cost of treatment per day according to age groups and sex. The figure shows that younger patients, especially those below 65 years, received the most expensive therapy (P<0.001). Intergroup age analysis (Tukey test) showed highly significant differences between all groups (P<0.001), except for the 65–74 years and >74 years groups. This significant increase in cost as a function of age was evident in both sexes.


Figure 4
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  		Fig. 4. Cost of therapy per day as a function of age groups and sex. Results are expressed as mean values. One way analysis of variance for the full population and intergroup age analysis (Tukey test) showed highly significant differences (P<0.001) between all groups except for the 65–74 vs >74 year old age groups. Patients below 65 years received the most expensive therapies. This pattern was similar in both sexes.

 


   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
References
 
This cross-sectional study of a cohort of unselected prevalent haemodialysis patients clearly indicates that, even with the introduction of sevelamer, approximately one in three patients have levels of serum phosphorus, Ca x P and iPTH above the upper target values defined in the K/DOQI guidelines. It appears that this abnormal profile is more likely to occur in younger patients, and in women for the case of hyperparathyroidism.

Despite substantial improvements over the last decade in the management of dialysis patients, little progress has been achieved in serum phosphorus control. In 1988, Lowrie and Lew [11] analysed data from 12 000 haemodialysis patients and found a mean serum phosphorus of 6.2 mg/dl. Twelve years later, Block et al. [6] showed that hyperphosphataemia remains a relevant clinical problem. In this study, 39% of patients had a phosphorus level greater than 6.5 mg/dl, 30% greater than 7 mg/dl, and 10% greater than 9 mg/dl. In Europe, a report from southern Italy described the current status of biochemical markers of renal osteodystrophy in a large number of haemodialysis patients, who followed dietary and dialysis schedules differing from those of the US patients [12]. Mineral levels in this cohort appeared to be slightly better controlled than in the US population, with 35% of patients having Ca x P >55 mg2/dl2 (>4.44 mmol2/l2) and 25.4% having evidence of hyperparathyroidism. Very recent data from the DOPPS study [9] demonstrate that the percentage of patients within K/DOQI guideline range remains surprisingly low, with 56.5% of patients having Ca x P <55 mg2/dl2 (<4.44 mmol2/l2) and only 22.4% of patients having iPTH levels between 150 and 300 pmol/l. Our results showed slightly better results for Ca x P control and similar results for iPTH, proving again that difficulties still exist in achieving the recommended levels of Ca x P and iPTH.

It is also remarkable that 42% of patients failed to meet the target guidelines because of low PTH values. This observation was reported by our group in 1995 [13] and confirmed in the DOPPS report [9], which also describes a high prevalence of patients with iPTH <150 pmol/l. This low iPTH level is more prevalent in the elderly dialysis population. In this respect, we previously suggested [14] that a lower serum phosphorus level, due to spontaneous reduction of protein intake, might contribute to the relatively low iPTH levels observed in these elderly patients.

The direct association between Ca x P, serum phosphorus and iPTH is evident in Table 2. The proportion of patients with Ca x P ≥ 55 ({chi}2 = 26.3, P<0.001) and serum phosphorus >5.5 ({chi}2 = 33.5, P<0.001) increased for each iPTH group.

While the direct association between phosphorus and iPTH found in this report is widely recognized, the association between calcium and iPTH is less constant. In a previous study performed by our group, PTH also failed to correlate with Ca in the univariate analysis [14]. Currently, there is an inverse relationship between Ca and iPTH, but besides this, there are patients with advanced hyperparathyroidism, in which high PTH drives the serum Ca up. This artefact may obscure the natural inverse association between calcium and iPTH.

While previous studies have shown a high prevalence of mineral abnormalities in the global dialysis population, information regarding its prevalence stratified by age is lacking. Based on our own analysis, it appears that hyperphosphataemia and high Ca x P are more likely to occur in younger patients. This supports the findings of previous studies in which we demonstrated that serum phosphorus levels decreased significantly with age in haemodialysis patients [14]. In a study including 207 haemodialysis patients, we showed that serum phosphorus and iPTH levels decrease with age, and both factors were related to the spontaneous decrease in caloric and protein intake observed in the elderly population [14,15]. The close relationship between protein and phosphorus content in the diet [16] may explain this association. Although phosphorus levels are more easily controlled in the elderly using lower doses of phosphorus binders, we observed that 25% of patients >65 years still had serum phosphorus and Ca x P over the upper limit of normal.

The association between iPTH and gender has previously been reported in primary hyperparathyroidism [17]. Experimental in vivo studies have reported that estrogens directly increase PTH gene expression and PTH secretion [18]. In addition, Almaden et al. provided experimental evidence indicating that differences in gender may affect the PTH response to calcitriol treatment [19]. Malberti and colleagues [20] demonstrated that female haemodialysis patients more often required treatment for hyperparathyroidism than males. The results of our epidemiological survey confirm the possibility of an independent association between gender and serum iPTH.

The number of patients included in this study probably represents almost 10% of the haemodialysis patients in Spain. However, it is not possible to know for certain if the results obtained in this cohort reflect the findings in the Spanish population with end-stage renal disease as a whole. In particular, the high prevalence of Caucasian patients in our cohort means that it is not possible to extrapolate our findings to other ethnic groups.

Although this study did not collect information about therapy compliance, our survey presents information about the mineral status in maintenance haemodialysis patients, reflecting common clinical practice in dialysis units in Spain. The analysis provides an opportunity to contrast observations made in controlled clinical trials with experience in every day practice in the real-world prescribing arena.

This study recorded data on drug doses, so it was possible to establish the real cost of mineral metabolism therapy. The mean cost of the therapy per day was, in general, less than four euros. This apparent low burden may be explained because the proportion of patients receiving calcitriol and sevelamer – the most expensive drugs – was relatively low, as compared with other reports.

The relationships between therapy costs and biochemical indices identified in this survey may reflect several factors, but the results unequivocally demonstrate that those patients with biochemical indices outside the ranges recommended by the K/DOQI guidelines generate significantly higher cost of therapy than the patients within target guidelines. In other words, despite the use of more medication and greater costs, target goals were still not met in a considerable proportion of patients. Stratification by age (Figure 4) shows that, this is particularly evident in patients younger than 65 years. These findings may be helpful in defining target cohorts for more rigorous therapeutic approaches. Additional interventions in the form of new formulations and cost-effectiveness protocols may be needed in this sizeable subgroup, which represents approximately 30% of the total haemodialysis population, in order to protect them against the high cardiovascular morbidity and mortality. Cost effectiveness studies are also needed to justify the increasing use of expensive medication.



   Acknowledgments
 
We wish to thank Ray Ashton and Michael McLean for their assistance in the preparation of the text. Mr Alejandro Jimenez from the Research Unit, Hospital Universitario de Canarias participated in the study as statistical adviser.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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  2. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 2004; 351: 1296–1305[Abstract/Free Full Text]
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Received for publication: 5. 3.05
Accepted in revised form: 18. 9.05


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