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European Heart Journal Advance Access originally published online on March 14, 2006
European Heart Journal 2006 27(9):1093-1099; doi:10.1093/eurheartj/ehi830
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© The European Society of Cardiology 2006. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Is pre-operative anaemia a risk marker for in-hospital mortality and morbidity after valve replacement?

Mercè Cladellas1,*, Jordi Bruguera1, Josep Comín1, Joan Vila2, Elisabeth de Jaime3, Julio Martí1 and Miquel Gomez1

1 Department of Cardiology, Hospital del Mar (IMAS-UAB), Passeig Marítim 25–29, E-08003 Barcelona, Spain
2 Institut Municipal d'Investigació Mèdica (IMIM)
3 Department of Geriatrics, Institut Municipal d'Investigació Mèdica (IMIM), Barcelona, Spain

Received 19 April 2005; revised 18 January 2006; accepted 23 February 2006; online publish-ahead-of-print 14 March 2006.

* Corresponding author. Tel: +34 93 248 3118; fax: +34 93 258 3398. E-mail address: mcladellas{at}imas.imim.es


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
 References
 
Aims To assess the level of pre-operative haemoglobin (HB) as a risk marker for morbidity and mortality in the early post-operative period of patients who underwent elective valve replacement.

Methods and results Between January 1998 and March 2004, clinical and outcomes data were collected for the 201 patients who had elective valve replacement. For each gender, the criterion to choose the best cut-off point was that which achieved the maximum likelihood after several General Additive Model models performed in a Bootstrap procedure. The best cut-off point obtained for pre-operative HB was 12 g/dL. Overall peri-operative mortality (deaths occurring during hospital period or within 30 days) was 9.5%. After adjusting well-known independent pre-operative risk factors for operative mortality, pre-operative HB <12 g/dL was identified as an independent predictor for in-hospital mortality (OR, 3.23; 95% CI, 1.09–9.55; P=0.03). Also adjusting for EuroScore, pre-operative HB remained significant (OR, 3.64; 95% CI, 1.32–10.06; P=0.01). The same model was applied to post-operative morbidity, and pre-operative HB <12 g/dL was identified as an independent predictor with and without EuroScore (OR, 4.67; 95% CI, 2.03–10.71; P<0.001), (OR, 5.18; 95% CI, 2.18–12.3; P<0.001), respectively.

Conclusion In patients undergoing elective valve replacement pre-operative HB <12 g/dL is a risk marker of in-hospital mortality and serious adverse outcomes.

Key Words: Anaemia • Heart valve prosthesis • Cardiac valve


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
 References
 
Over the last few years, many reports have identified some risk factors which provide an accurate estimate of the in-hospital mortality rate after cardiac valve replacement.1–3 Knowledge of risk factors and comorbidities such as NYHA functional class or left ventricular dysfunction has allowed physicians to improve post-operative outcomes because they indicate valve replacement at an early stage of severe valve disease. On the other hand, greater life expectancy, improvement in surgical technique, and post-operative management have conditioned an increase in elderly patients with good physical and mental health who have severe left-sided valve disease. In that setting, the demand for cardiac surgery in elderly patients has increased over the last few years, in spite of these patients having more comorbidity conditions.4,5 In this changing patient population, a number of ‘new’ risk factors may become more relevant or the relative risk associated with well-known risk factors might change over time.

Epidemiologic and clinical reports underline the importance of haemoglobin (HB) in the pathogenesis, prognosis, and complications of cardiovascular events. Low HB is a significant predictor of mortality for patients with chronic heart failure6,7 and it has been shown to be a risk factor in patients with end-stage renal disease for left ventricular hypertrophy.8 Moreover, the presence of anaemia in low-risk patients in the general population with ages between 45 and 64 years is associated with increased risk for developing cardiovascular events.9

In surgical procedures, anaemia has been associated with worse clinical outcomes. Non-cardiac surgery patients with low pre-operative HB and cardiovascular disease had a higher mortality rate after surgery than the patients who did not have cardiovascular disease.10 In a study by Zindrou et al.,11 patients with pre-operative HB ≤10 g/dL undergoing coronary revascularization with cardiopulmonary bypass (CPB), showed a five-fold higher in-hospital mortality rate after surgery than patients whose pre-operative HB was higher. Anaemic patients who underwent percutaneous coronary intervention had a greater in-hospital mortality rate and myocardial infarction after coronary angioplasty when compared with their respective non-anaemic cohort.12

Cardiac surgery with CPB entails anaemia for several reasons (haemodilution, blood loss, haemolysis, etc.), which is nearly instantaneous at the beginning of CPB. Previous reports, have shown that the haematocrit value <22% during CPB increases significantly and systematically the morbidity and mortality rate after coronary surgery.13,14 DeFoe et al.,15 have demonstrated a significant relationship between severe anaemia on CPB and low pre-operative haematocrit and worse outcomes after isolated coronary artery bypass. However, the prognosis and involvement of pre-operative HB in patients undergoing valve replacement is unknown. Consequently, the aim of this study was to assess the level of pre-operative HB as a risk marker for morbidity and mortality in the early post-operative period of patients who underwent elective valve replacement.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Conclusions
 Acknowledgements
 References
 
Database
This database was initiated in 1998 to include the patients for whom Department of Cardiology of the Hospital del Mar indicated cardiac surgery. It contains detailed clinical information of risk factors, clinical pre-operative characteristics, number of valves replaced and valve position, post-operative complications, operative mortality and post-operative length of hospitalisation.

Study patients
Elective valve replacement from January 1998 to March 2004 included 233 consecutive patients who underwent valve surgery at age 64±11 years (56% female). Standard CPB techniques were applied using normothermia (body temperature: 35–37°C). Cardiac arrest was achieved with crystalloid cardioplegia. Ninety percentage of patients were operated on by surgeons in our reference hospital and the rest in the other hospitals of our city. This study included those patients receiving either mechanical or biological prosthetic valve replacement with or without coronary artery bypass, but excluded six patients in whom mitral valve was repaired. In addition, 22 patient records were excluded from the study as the time period between pre-operative blood analysis and prosthetic valve replacement was over 3 months, and four patient records due to technical problems during cardiac surgery: these patients suffered peri-operative major bleeding (one diffuse haemorrhage, one rupture of lateral wall, one rupture of venue cavae, and the last coagulopathy), fact that disables the aim of the study.

Data definition
Pre-operative risk factors such as presence or absence of hypertension, diabetes, and hypercholesterolaemia were included. Diagnosis of these risk factors was carried out by a physician, and patients received the treatment to control them. We defined the habit of smoking as a risk factor when a patient was an active smoker at inclusion.

Pre-operative clinical symptoms were included as presence or absence of angina pectoris, syncope, New York Heart Association (NYHA) functional class, but only class III or IV were considered as risk factors in this study. In all patients, coronary angiography was performed except in females whose age was <55 years and males whose age was <45 years without risk factors.

Associated comorbidities
Chronic obstructive pulmonary disease (COPD) was included in the database if patient had undergone a functional respiratory function test. Diagnosis of COPD was made, if functional expiratory volume at 1 s (FEV1) <75% in this test. Renal failure was considered if serum creatinine level was >1.50 mg/dL. Atrial fibrillation or atrial flutter at inclusion was considered as comorbidities. History of paroxysm of atrial fibrillation in patients with sinus rhythm was included as a risk factor. The ejection fraction <50% evaluated by echocardiography was defined as a risk factor. History of cerebral vascular accident was considered in patients who suffered a stroke at any point of time. Other comorbidities included were body surface area, pre-operative HB level, and previous cardiac surgery. Global pre-operative risk of the patient was calculated by EuroScore.

We considered the post-operative period as the time that the patient remained in hospital before discharge or after hospital discharge within 30 days of valve replacement. In this post-operative period, we divided the outcomes into two categories. Group I included major adverse cardiovascular events (MACE). We considered as major complications the following: heart failure defined as need to receive inotropic drugs after coming off pump or during hospitalization; neurological complications such as new permanent stroke or transient ischaemic attack; acute renal failure such as oliguria with serum creatinine level >1.5 mg/dL or patients requiring dialysis or haemofiltration; reoperation for bleeding. Perioperative myocardial infarction was defined as either development of new Q wave in two or more leads on ECG or alterations of myocardial contractility that did not exist previously in echocardiography. Prosthesis thrombosis defined as any thrombus in the absence of infection or dysfunction; prosthesis dysfunction as any change in function as a result of an intrinsic abnormality, cardiac tamponade. Severe infection included sepsis or pneumonia or mediastinitis. Prolonged ventilation was defined as when mechanical ventilatory support lasted longer than 24 h. Operative mortality was defined as all deaths occurring during hospital period or after hospital discharge, but within 30 days of valve replacement. All MACE was summarized in one variable in patients who had one or more than one major complication.

Group II included minor post-operative complications such as paroxysmal atrial fibrillation or atrial flutter developed in post-operative period or patients without events in this period.

Statistical analysis
Continuous variables were expressed as mean±SD and categorical data were expressed as real numbers and percentages.

Univariate analysis was performed by unpaired two-tailed t-test or Kruskall–Wallis. Categorical variables were analysed with the {chi}2 test or Fisher's exact test when appropriate.

The aim of this study was to assess whether HB is an independent predictor of outcome (MACE and death). Therefore, multivariable logistic regression analysis was used to adjust the HB effect for covariates known to be important predictors of early mortality after cardiac surgery, such as age, gender, myocardial function (ejection fraction <50%), functional class III or IV, coronary artery bypass, and renal dysfunction (serum creatinine >1.5 mg/dL) and EuroScore. Because EuroScore included some of the other predictors, two different sets of models were developed, one including risk factors without EuroScore and other with EuroScore.

The linearity of the continuous variables was tested in non-semi-parametric regression with a General Additive Model (GAM).16 P-value for non-linear effect of age and EuroScore did not achieve statistical significance, therefore, a linear relationship with the risk was assumed for those variables.

To find the best cut-off for HB that discriminates those who will have a MACE and death from those who will not, a GAM was performed with MACE and death as response variable, and gender and pre-operative HB as explanatory. Pre-operative HB was included after being smoothed by local regression smoother function. Plot of predicted values against HB showed the risk of these complications as increasing upto 12 g/dL, and after that as remaining stable. The criterion to choose the best cut-off point was that which achieved the maximum likelihood after several GAM models performed in a Bootstrap procedure.17 The Bootstrap did 1000 replicates. In each replicate equidistant pre-operative HB cut-off points between 9 and 14 g/dL were tested and the cut-off with the highest likelihood was retained. After the 1000 replicates, the most frequent highest value (i.e. the mode) was considered the best cut-off, and the 2.5 and 97.5 percentiles as the limits of the 95% CI. This cut-off point was pre-operative HB ≥12 g/dL for both genders.

All statistical tests with two-sided P-value <0.05 were considered statistically significant. Statistical analyses were done with R 2.0 (The R Foundation for Statistical Computing, Free Software Foundation Inc., Boston, MA, USA) and SAS 9.2 (SAS Institute, Cary, NC, USA).


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Conclusions
 Acknowledgements
 References
 
Valve replacement was performed in 201 patients with mean age of 65±11 years. The most frequent indication for surgery was single aortic valve disease in 102 patients (50.7%) and severe aortic stenosis in 65 patients (64%). The overall operative mortality was 9.5%.

In MACE group the patients were older (P=0.02) and there was greater incidence of hypertension (P=0.01), hypercholesterolaemia (P=0.04), COPD (P=0.01), NYHA class III or IV (P=0.004), and renal failure (P=0.005). In addition, the mean of pre-operative HB was significantly lower in MACE (Group I) than Group II, but within the normal range (Group I: 12.6±1.7 vs. Group II: 13.5±1.4; P<0.001). This group of variables was significantly associated with the post-operative outcomes, as was expected. All patients who died belonged to the MACE group and died in-hospital.

In a Bootstrap procedure, the best cut-off-point for HB was 12.0 (95% CI 10.9–13.9). Table 1 describes the clinical pre-operative characteristics in accordance with pre-operative HB <12 g/dL and HB ≥12 g/dL. Patient's age was significantly lower in the group with pre-operative HB ≥12 g/dL than in the group with pre-operative HB <12 g/dL. In addition, in this group there was a greater and significant prevalence of women (P=0.004), hypertension (P<0.001), hypercholesterolaemia (P=0.03), NHYA class III or IV (P=0.01), smaller body surface area (P=0.01) than in the group with pre-operative HB ≥12 g/dL. The increase in the risk factors and pre-operative comorbidities was reflected on the EuroScore, which was higher in the group with HB <12 g/dL than in the group with HB ≥12 g/dL (P<0.001). We found no significant differences in the site of the valve replacement and coronary artery bypass between the two pre-operative groups of HB. When we divided the pre-operative HB into quartiles, the group below HB <12 g/dL shows a higher and more significant mortality than other groups (Figure 1).


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  		Table 1 Pre-operative clinical characteristics and operative procedures divided into HB ≥12 g/dL and HB <12 g/dL

 

Figure 8301
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  		Figure 1 The relationship between pre-operative HB divided into quartiles and post-operative mortality. The group with pre-operative HB <12 g/dL showed a 23.8% mortality rate higher than other groups in which the rates were 6, 7, and 3.8% respectively.

 
The in-hospital mortality rate was 23.8% in the group with pre-operative HB <12 g/dL, significantly higher than in the group with pre-operative HB ≥12 g/dL, which was 5.7% (P=0.001).

The main post-operative complication was acute renal failure in 40 of 201 patients (19.9%), followed by heart failure in 35 (17.4%), prolonged mechanical ventilation in 27 (13.4%), and severe infection in 16 (12.9%). These major events were significantly higher in the group with low pre-operative HB than the group with pre-operative HB ≥12 g/dL (Table 2). Furthermore, the overall frequency of the MACE in the anaemic group was 73.8%, a considerable increase in comparison with the non-anaemic group, which was 31.4% (P<0.001). Likewise, 83 of the 159 patients (52.2%) of the group with pre-operative HB ≥12 g/dL and only 9 of 42 patients (21.4%) of the group with HB <12 g/dL (P<0.001) were discharged without any event. Figure 2 shows the summary of post-operative outcomes according to the severity of different degrees of complications between the two groups of pre-operative HB. Finally, post-operative length of hospital stays increased proportionally and significantly with severity of post-operative events in both groups. Furthermore, the longest stays were in patients who died in-hospital and belonged to the anaemic group (Figure 3).


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  		Table 2 Post-operative outcomes divided into HB ≥12 g/dL and HB <12 g/dL

 

Figure 8302
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  		Figure 2 In the group with pre-operative HB <12 g/dL there was a significant increase in the in-hospital mortality rate and a lower proportion of patients without any complications when compared with the group with pre-operative HB ≥12 g/dL. C: complications.

 

Figure 8303
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  		Figure 3 Estimated post-operative length of stays according to different types of post-operative outcomes divided into two groups of pre-operative HB. Median, Q1–Q3.

 
Multivariable logistic regression analysis was used to identify pre-operative HB <12 g/dL as an independent predictor of in-hospital mortality. The first model of multivariable analysis was performed without the EuroScore scoring system and includes the risk factors that have demonstrated to be independent for operative mortality. In a second model, the EuroScore was added to determine the potential effect of this score system on risk of in-hospital death (Table 3). In both models, the pre-operative HB <12 g/dL (P=0.02) remained the independent predictor for in-hospital mortality for both sexes. The same models were performed for MACE (Table 4) and pre-operative HB <12 g/dL was identified as significantly associated with MACE in both models.


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  		Table 3 Predictors of post-operative mortality after valve replacement by multivariable logistic regression

 

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  		Table 4 Pre-operative predictors for all major post-operative complications (MACE) after valve replacement by multivariable logistic regression

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusions
 Acknowledgements
 References
 
In this study, the pre-operative HB <12 g/dL was identified as an independent predictor for in-hospital mortality and morbidity with and without EuroScore after cardiac valve replacement (Tables 3 and 4).

The only study that evaluated pre-operative HB as a risk factor in cardiac surgery is reported by Zindrou et al.11. They showed that in anaemic patients who underwent coronary artery bypass on-pump, the mortality rate increased five-fold after cardiac surgery. These researchers found the best cut-off point of the pre-operative HB to be below 10 g/dL. The difference in the level of the pre-operative HB between the two studies may be due to population characteristics and type of cardiac surgery. In the current study, the patients were older and the main indication of the surgery was for valve replacement and in 19.1% concomitant coronary artery bypass. Valve replacement has higher post-operative mortality and morbidity than isolated coronary artery bypass as described in previous studies18,19 and the elderly patients have more pre-operative comorbidities. Both factors could be the reason for the different level of HB between the two studies. In the current study, baseline characteristics in the group with pre-operative HB below 12 g/dL had a significantly higher proportion of females (76.2 vs. 51.5), older patients (69 SD 10 vs. 64 SD 11), more hypertension (66.7 vs. 35.2), and dyslipemia (41.9 vs. 25.8), smaller body surface (1.66 SD 0.17 vs. 1.75 SD 0.19) than the group with pre-operative HB ≥12 g/dL (all, P<0.05). These different findings were reflected in the EuroScore, which was higher in the anaemic group than in the other group (6.7 SD 1.7 vs. 5.2 SD 2, P<0.001).

Similar untoward effects of anaemia have been observed in cardiovascular patients undergoing non-cardiac surgical procedures. Carson et al.10 found that patients with anaemia and cardiovascular disease who decline blood transfusion had a much higher in-hospital mortality rate after non-cardiac surgery than do patients who do not have cardiovascular disease. Previous studies in patients with coronary heart disease that assessed the HB concentration on-pump as low as that described by Fang et al.,14 have demonstrated an increase of adverse outcomes in the immediate post-operative period. These authors separated low- and high-risk coronary artery bypass and concluded that haematocrit value on CPB below 14% in low-risk patients and below 17% in high-risk patients was associated with double peri-operative mortality.

The main determinants of the nadir haematocrit on CPB were smaller body surface area, age, females.14,15,20,21 In addition, these studies reported an association between low haematocrit level on CPB and worse outcomes after cardiac surgery. In a recent study, Habib et al.,1 in isolated coronary artery bypass divided the post-operative outcomes into five groups according to the lowest haematocrit during CPB. They reported that a low haematocrit on CPB increased in-hospital mortality and risk of subsequent major post-operative events. Both adverse outcomes increased proportionally when the nadir of haematocrit decreased during CPB, particularly when the haematocrit value was less than 22% on CPB. The significant post-operative events include stroke, myocardial infarction, low cardiac output, cardiac arrest, renal failure, prolonged ventilation, pulmonary oedema, reoperation due to bleeding, sepsis, and multiorgan failure after adult cardiac surgery, in spite of patients receiving intra-operative and post-operative blood transfusions. The lowest haematocrit quintiles on CPB showed greater age, a higher proportion of females, and more pre-operative comorbidities than other groups. The nadir of haematocrit in this group on CPB was 15.9±1.4% and baseline haematocrit was 32.9±4.4%. Furthermore, the highest mortality was observed in this quintile (first quintile 7.5% vs. last quintile 1.6%, P<0.001). The nadir of haematocrit in the last quintile on CPB was 27.5% and baseline haematocrit was 42.6%. These results have shown that the relationship between the decrease of haematocrit on CPB was proportional to pre-operative haematocrit.

After adjusting for independent risk factors for operative mortality by logistic regression analysis without EuroScore, we identified pre-operative HB <12 g/dL as an independent predictor for in-hospital mortality (OR, 3.23; CI, 1.09–9.55) and post-operative MACE (OR, 5.18; 95% CI, 2.18–12.3). In addition, when EuroScore was added to the same model, the HB remained an independent predictor for in-hospital mortality (OR, 3.64; 95% CI, 1.32–10.05), and for post-operative morbidity (OR, 4.67; 95% CI, 2.14–10.36). EuroScore is a pre-operative scale that establishes distinct levels of risk in quantitative terms and includes a number of risk factors that contribute to the prediction of hospital mortality in cardiac surgery.1 Age, female, advanced functional class, and ejection fraction is included in this quantitative stratification in contrast to the pre-operative HB.

The present study showed a significant increase of in-hospital mortality in the group with pre-operative HB below 12 g/dL (23.8%) in relation to the group with pre-operative HB ≥12 g/dL (5.7%; P=0.001). In addition, when we divided the pre-operative HB into quartiles as shown in Figure 1, we can observe a significant increment of mortality in the group with HB <12 g/dL in comparison with the rest of the groups. Another difference in the post-operative period was the incidence of patients without any complication. In the anaemic group, only 21.4% of patients did not show events within 30 days of the post-operative period when compared with 52.2% of patients in the group with HB over 12 g/dL (P=0.001) (Figure 2).

An important insight obtained in this study is that the degree of this anaemia was slight. The mean of HB in the anaemic group was 10.8±1 g/dL and when we divided HB according to MACE and minor post-operative complications, HB was lower in the group with MACE (12.6±1.7 g/dL), but it was within the normal range.

Finally, post-operative hospital stays were the longest in anaemic group patients who died, as reported in previous studies.11,13 These patients died gradually during the first few weeks after surgery with many complications in the intensive care unit (Figure 3).

To our knowledge, no studies have previously reported an association between pre-operative anaemia and early post-operative outcomes in valve replacement. The relationship between pre-operative anaemia and post-operative adverse outcomes remains uncertain, as the balance of oxygen supply and demand during CPB is complex and dynamic. Nevertheless, there are potential reasons why pre-operative anaemia may be a risk factor for post-operative outcomes. Reduction in arterial oxygen content is usually well tolerated because of compensatory increase in cardiac output. This compensatory mechanism may be affected by several factors such as age, pre-operative comorbidities, and pre-operative anaemia itself.22,23 On the other hand, at the start of CPB or during re-warming in 29% of the patients who underwent cardiac surgery at least one episode of oxygen desaturation was demonstrated.24 In addition, a significant relationship has also been demonstrated between an increase of lactate level as an indicator of systemic hypoperfusion and higher incidence of heart failure, increased length of hospital stay, and higher mortality rates after cardiac surgery.25 Moreover, erythropoietin is a primary regulator of erythropoiesis during anaemia and increases exponentially in response to a linear decrease of the haematocrit. In ischaemic heart disease, patients with normal renal function who underwent extracorporeal perfusion, a relative deficiency has been demonstrated in the response of erythropoietin to surgical blood loss.26 Finally, tolerance of hypoxia in human myocardial patients is reduced in the elderly or in hypertensive patients.27 These findings allow us to extrapolate that the probable mechanism could include impaired oxygen delivery to tissues causing tissue hypoxia.

Study limitations
The current study is retrospective and is, therefore, subject to limitations inherent, in this type of clinical investigation. However, the present study was designed from a database that includes consecutive patients from 1998, and in this context, the patients were not selected. Furthermore, all data were 99% complete except COPD, which was 34% complete. Hence, to include this in the database a respiratory test had to be performed. In this study, there are no haemodynamic data or other parameters included during cardiac intervention but the purpose of this study was to find pre-operative risk factors.

Clinical implications
The results of the present study offer additional insights into several important points after valve replacement surgery. First, anaemic patients should be considered a high-risk group where several pre-operative comorbidities coexist. In this context, anaemia is a risk marker of early poor outcomes after valve replacement surgery. Secondly, the degree of this pre-operative anaemia is slight. Thirdly, at the same EuroScore, anaemic patients have a greater risk of in-hospital mortality and post-operative morbidity. Finally, among the risk factors demonstrated to be independent predictors for operative mortality like age, female gender, renal failure, or coronary heart disease,1–4 pre-operative anaemia is a new risk factor and a clinically modifiable factor. In patients with mild anaemia and gastrointestinal cancer28 or orthopaedic surgery,29,30 the treatment with erythropoietin and iron has demonstrated a reduction of post-operative complications. In this setting, the results of this study could also provide new opportunities for treatment in these patients. It remains to be determined whether optimisation of HB levels before elective valve replacement may improve the clinical results after valvular surgery and requires further study.


   Conclusions
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
Acknowledgements
 References
 
The main message of this study is that our data provides evidence that pre-operative HB <12 g/dL is associated with an increase of in-hospital mortality and post-operative MACE, independent of the EuroScore after valve replacement. The impact of therapies such as erythropoietin and iron in anaemic patients to increase haemoglobin before valve replacement is currently under study.


   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
References
 
The authors gratefully acknowledge Prof. Jaume Marrugat for his valuable critical comments and Francis McCabe for his assistance in the translation of the manuscript.

Conflict of interest: none declared.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 Acknowledgements
 References
 

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