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European Journal of Heart Failure 2007 9(8):839-844; doi:10.1016/j.ejheart.2007.03.010
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© 2007 European Society of Cardiology

Heart transplantation in heart failure: The prognostic importance of body mass index at time of surgery and subsequent weight changes

Andrew L. Clarkc,*, Christoph Knosallad, Emma Birkse, Matthias Loebed, Constantinos H. Davosb, Sui Tsangf, Abdissa Negassag, Magdi Yacoube, Roland Hetzerd, Andrew J.S. Coatsb and Stefan D. Ankera,b

a Department of Cardiology, Franz-Volhard-Klinik (Charité, Campus Berlin-Buch) at Max Delbrück Centrum für Molekulare Medizin Berlin, Germany
b Clinical Cardiology, National Heart & Lung Institute, Imperial College School of Medicine London, UK
c Department of Cardiology, Univerity of Hull UK
d Deutsches Herzzentrum Berlin, Department of Cardiothoracic and Vascular Surgery Berlin, Germany
e Department of Cardiac Surgery, Royal Brompton and Harefield Hospitals London, UK
f Advanced Heart Disease Section in Brigham and Women's Hospital Boston, USA
g Epidemiology and Population Health, Albert Einstein College of Medicine New York, USA

* Corresponding author. Castle Hill Hospital, Castle Road, Cottingham, HU16 5JQ, UK. Tel.: +44 1482 624012; fax: +44 1482 624085 E-mail address: a.l.clark{at}hull.ac.uk.


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Limitations
 References
 
Background: Heart transplantation is an important treatment for end-stage chronic heart failure. We studied the effect of body mass index (BMI), and the effect of subsequent weight change, on survival following transplantation in 1902 consecutive patients.

Methods and results: Patients were recruited from: London (n=553), Berlin (N=971) and Boston (N=378). Patients suitable for transplantation due to symptoms, low left ventricular ejection fraction (≤30%) and peak oxygen consumption (≤16 ml kg–1 min–1) (N=237) were used as a comparator. In surviving transplanted patients, average duration of follow-up was 80 (SD 34) months. There were 805 deaths. One year survival was 72.7% (95% CI 72.68–72.72) and 5 year survival was 60.96% (61.94–61.99). Baseline BMI did not effect survival either as a continuous variable (hazard ratio (95% CI): 1.02; 0.99–1.04). Weight loss between transplant and 3 months was associated with worse survival (HR (95% CI) 2.6 (1.42–4.74)) compared with those who gained weight. In the reference group, increasing body mass index was related to survival.

Conclusions: Chronic heart failure patients with very low body weight can be transplanted successfully. The presence of underweight need not be an exclusion criterion for heart transplantation. Underweight patients appear to have a greater benefit from transplantation. Body weight increases after transplantation are not associated with adverse prognosis.

Key Words: Heart failure • Nutrition • Obesity • Transplantation

Received September 22, 2006; Revised January 25, 2007; Accepted March 5, 2007


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 5. Limitations
 References
 
Evaluation of patients with end-stage chronic heart failure plays an important role in optimising the results of heart transplantation. Typically, selection for transplantation is made on a combination of clinical features; the age and general condition of the patient; the severity of left ventricular dysfunction; and the exercise capacity are used to make a judgement of the chances of survival with and without transplantation.

One year survival following transplantation is 77-85% [1-3]. A number of variables is related to long term survival following transplantation. These include pre-, per- and post-operative factors. Patients with non-ischaemic heart disease fare better [1] and an early decline in allograft left ventricular function is associated with a poor outcome [4]. Worse outcomes are seen in recipients at the extremes of the age range, with ventilated recipients and with grafts from older and smaller donors [3,5,6].

Cachexia and morbid obesity may be considered relative contra-indications for transplantation. Conflicting results have been reported on the relationship between body weight and survival after transplantation. Carrier et al. found no relation between body mass at time of transplantation and 30-day mortality [7]. Lietz et al. [8] found that patients with a body mass index >30 kg/m2 and <20 kg/m2 had worse survival. In the largest study to date (n=4515), Grady et al. found no significant relationship between BMI and survival, but they reported that patients with very low or high "percentage ideal body weight" had a worse outcome [9].

One of the key features of end-stage heart failure is the development of body wasting and inflammatory and immune activation. The origins of immune activation remain unclear, but may be related to cardiac cachexia [10,11], itself associated with a particularly poor prognosis [12]. In contrast, obese patients with chronic heart failure demonstrate a trend towards improved survival [13]. No previous study has tried to assess weight changes after transplantation and to compare survival of transplanted patients to that in patients of similar disease severity and BMI without transplantation. The immunosuppressive therapy used following transplantation could cause weight gain. These effects may be most beneficial in patients who are underweight and most likely to have the worst immunological status, i.e. in cachectic heart failure patients.

The present study was designed to assess the effect of body mass, and the effect of change in body mass following the operation, on survival following cardiac transplantation.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 5. Limitations
 References
 
We retrospectively collected data on 1902 consecutive patients undergoing cardiac transplantation in one of three institutions between 1984 and September 1999; London (n=553), Berlin (N=971) and Boston (N=378). Approval for the study was granted by the ethics committees of each of the three institutions. For all patients, height, weight and age at transplantation were known. For a subset of patients, weight at 3 months (N=798) and 12 months (N=719) was also known. Limited data on other clinical variables at the time of transplantation were also available. Follow-up was censored on 31st March, 2000.

In order to compare outcome in patients without transplantation, we interrogated the Royal Brompton Heart Failure and Deutsches Herzzentrum Berlin databases, and selected a population of patients suitable for cardiac transplantation on the basis of New York Heart Association class III or IV symptoms, a low left ventricular ejection fraction (≤30%) and peak oxygen consumption (≤16 ml kg–1 min–1) (N=237). None of these patients underwent transplantation.

For both datasets, the patients were divided into 5 groups on the basis of their body mass index at entry. Ideal body weight was calculated from standard tables [14]. Patients were divided into four groups by percentage ideal body weight (<80%, 80-100%, 101-120%, and >120%) [9].

Data are given as mean±SD. Normality of distribution for continuous variables was tested using the Kolmogorow-Smirnov test. The unpaired Student's t-test was used to compare mean values between groups. Proportions were compared using {chi}2-test and Fisher's exact test. Cox proportional hazard analyses that take into account heterogeneity due to centres [15] were used to assess prognostic associations. The hazard ratio (HR) with 95% confidence intervals (CI) and p-values as derived from the appropriate model are given. Hazard ratios for continuous variables apply per unit of the analysed variable. Kaplan-Meier cumulative survival plots were constructed to illustrate the results (StatView 5.0, Abacus Concepts, Berkeley, USA).


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 5. Limitations
 References
 
Follow-up was complete, with an average duration of follow-up of 80 (SD 34; range 6-191) months in survivors. Minimum follow-up in survivors was 6 months. There were 805 deaths during follow-up. Data relating to the patients at the time of transplantation are shown in Table 1. Limited data are available on left ventricular ejection fraction (N=193; 21.6 (8.2)%) and peak oxygen consumption (N=251; 11.6 (3.6) ml min–1 kg–1).


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  		Table 1 Patient details at time of cardiac transplantation

 
Body mass index was normally distributed for both men (mean 24.8, median 24.7, standard deviation 0.5) and women (mean 25.0, median 25.0, standard deviation 0.5), as was percentage ideal body weight for men (mean 108.3, median 108.4, standard deviation 3.5) and women (mean 107.9, median 106.2, standard deviation 4.1). There was a weak correlation between body mass index and age (r=0.2, p<0.0001).

One year survival was 72.7% (95% CI 72.68-72.72) and 5 year survival was 60.96% (61.94-61.99). There was no effect of body mass index on survival expressed either as a continuous variable (hazard ratio 1.02 (0.993-1.04)) or as a categorical variable with the patients divided into quintiles (95% confidence intervals of all comparisons between quintiles cross 1.0). Similarly, there was no effect on survival of weight either as an absolute value (1.0 (0.991-1.01)) or expressed as percentage ideal body weight (1.0 (0.998-1.01)).

Data on weight change following transplantation was available for some patients (Table 2). At 3 months (N=798), there was an average weight gain of 0.37 (6.3) kg, at 1 year (N=719) 6.67 (8.50) kg, and between 3 months and 1 year (N=708) 6.18 (6.27) kg. Patients were divided into three groups for each weight change period: those with any weight loss (group 1); those with weight gain of 0 to 5 kg (group 2); and those with weight gain greater than 5 kg (group 3). For those patients with complete follow-up weight data, weight at transplant was 72.4 (13.7) kg, at 3 months was 72.8 (12.8) kg and at 1 year was 79.0 (15.0) kg (p<0.0001 for the comparisons between weight at transplant and 1 year and between weight at 3 months and 1 year).


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  		Table 2 Distribution of weight changes following transplantation

 
At 12 months follow-up, there were 31 deaths in the 798 patients with weight change data at 3 months. Change in weight from transplant to 3 months was related to survival (group 1 relative to group 3 hazard ratio: 5.2 (1.2-22.3) and group 2 relative to group 3: 3.9 (0.9-17.6)).

At 5 year follow-up, there were 107 deaths in these 798 patients. Diagnosis (ischaemic heart disease v non-ischaemic) affected survival (hazard ratio 1.29 (1.11-1.51) for ischaemic v non-ischaemic). Increasing age predicted decreased survival (hazard ratio 1.02 (1.01-1.02) for each increment of 1 year). Sex of recipient was not related to survival (0.88 (0.72-1.08)).

Change in weight from transplant to 3 months was related to survival at 5 years: group 1 relative to group 3 hazard ratio 2.69 (1.47-4.90) and group 2 relative to group 3, 1.90 (1.01-3.60). The Kaplan-Meier survival plot is shown in Fig. 1. Weight change between 3 and 12 months also predicted survival. Compared with those who gained weight, those who lost weight (N=84) had a hazard ratio of 1.9 (0.98-3.59, p=0.057). Change in weight from transplant to 3 months was a predictor of outcome independent of age, sex, centre and diagnosis (see Table 3).


Figure 01
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  		Fig. 1 Survival to 5 years follow-up following transplant. Patients are grouped by pattern of body weight change in the first 3 months following transplantation: those with any weight loss (group 1); those with weight gain of 0 to 5 kg (group 2); and those with weight gain greater than 5 kg (group 3). Survival figures at 5 years (with 95% confidence intervals) are given.

 


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  		Table 3 Potential predictors of outcome at 5 years in the transplanted population

 
There were 181 deaths overall in the group of 798 patients with weight change data at 3 months. In Cox proportional hazard analysis, only age remained a significant predictor of outcome (hazard ratio 1.02 (1.00-1.03)). Sex, weight change, centre and underlying diagnosis fell out of the model.

The reference group of heart failure patients (n=237) were older than the transplant group (mean age 54.8 (8.7) years). Weight was 79.2 (13.8) kg, and BMI 26.1 (3.9) kg m–2. Left ventricular ejection fraction was 19.0 (5.3)% and peak oxygen consumption 11.7 (2.9) ml kg–1 min–1. In the reference heart failure patients, survival was 78.1 (72.8-83.4)% at 12 months and 46.6 (32.5-60.7)% at 5 years.

Increasing body mass index was significantly related to survival in the patients without transplantation: each increment in BMI of 1.0 carried a hazard ratio of 0.92 (0.87-0.98); p=0.006. Percentage ideal body weight was also related to survival (1 year survival: each increment of 1.0% carried a hazard ratio of 0.98 (0.96-0.99); p=0.017).

Comparisons of survival times at 1 year for the two populations are shown in Tables 4 and 5. As there was a strong relation between survival and body mass in the reference population, but not in the transplanted population, there is a much greater survival benefit for the patients with low body mass at transplantation.


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  		Table 4 Comparison of survival rates at 2 years between transplanted and reference groups by body mass index (BMI)

 


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  		Table 5 Comparison of survival rates at 2 years between transplanted and reference groups by percentage ideal body weight (IBW)

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
5. Limitations
 References
 
This study shows that heart failure patients with very low body weight, i.e. with cardiac cachexia, can be transplanted successfully and that the presence of cardiac cachexia need not be an exclusion criterion for heart transplantation. This study suggests that underweight patients, because of the underlying extremely poor prognosis [12,16], have a greater benefit from transplantation compared to patients with higher body weight. Body weight increases in the first year after transplantation are not associated with adverse subsequent prognosis.

Low body mass is a risk factor in cardiac surgery [17-19] and in univariate analysis of the Cardiac Transplant Research Database Group [9]. We have found no relationship between body mass and survival following cardiac transplantation. This was true when body mass was indexed to height (BMI) or when expressed as a proportion of ideal weight as calculated from actuarial survival tables. In contrast, in a reference population who were not referred for transplantation, we found a strong relationship between body mass and survival. Without transplantation, obese patients with advanced heart failure have a much better survival than patients with low body weight. This is in agreement with results from the UCLA Advanced Heart Failure Database (n=1203) [13], as well as with new data from the COPERNICUS trial (n=2251) [20].

Among previous studies, Lietz et al. [8] report poor survival post-transplantation in cachectic patients. These results are similar to those of Deng et al. [21], who have suggested that the survival benefit of heart transplantation is greatest in patients with the poorest prognosis as assessed by a validated score [22].

Two year use of a left ventricular assist device prolongs survival in patients with end-stage heart failure [23]. We have previously shown that survival following implantation of a ventricular assist device is strongly related to body mass at the time of implantation — there is poorer survival in patients with low BMI [24]. Both transplantation and LVAD implantation are major surgical interventions which improve cardiac output substantially. One important difference between the two is the use of immune modulatory therapy after transplantation. Loss of skeletal muscle tissue is a relatively early event in the pathogenesis of chronic heart failure [25], whereas loss of fat tissue is a late event and characteristic for patients with cardiac cachexia [26]. Steroid hormones, as used after transplantation, cause an increase in fat tissue mass. In the present study, weight loss after transplantation was related to poor outcome. Cachectic heart failure patients show major immunological abnormalities [10,11], and it might be that the immune modulatory drug therapy after transplantation exerts additional direct benefits in cachectic patients. This could only be tested in a prospective intervention study.

Obesity is an independent risk factor for death from coronary artery disease [27,28], and patients who have undergone cardiac transplantation frequently put on weight [29,30]. In chronic heart failure, obesity is not associated with adverse prognosis [13]. Previous work has suggested that overweight subjects [31], and those at the extremes of the weight range [9] have a worse prognosis following transplantation.

Two studies [3,7] did not find a significant relationship between obesity and outcome, whereas Lietz et al. [8] reported that patients with a BMI >30 kg/m2 had reduced survival. There may be differences between the study populations, but compared with cachectic patients, the survival benefit of transplantation in the obese seems to be less. Other workers have shown that obesity increases in frequency following heart transplantation [32] and that post-transplant cachexia and obesity are adverse risk factors.

The present study has investigated survival after transplantation in 3 major surgical centres from 3 countries. Individual selection criteria for patients to undergo transplantation, allocation of donor organs, and post-transplantation medical care differ between units. In the involved centres, there were no active procedures to exclude cachectic or obese patients from consideration for heart transplantation. All the involved physicians and surgeons in these centres aim to transplant patients with very advanced disease status.

Survival post-transplant in the present study is lower than might be expected from International Registry data. The phenomenon of the higher mortality in a population of German patients undergoing transplantation has been noted before [21]. The explanation for this might be that the donors are older than those in the registry.

We conclude that underweight is not an exclusion criterion for heart transplantation. The results of our study suggest that the relative survival benefit of transplantation is greatest in those patients with end-stage heart failure with the lowest body mass index. Weight gain after transplantation, from a prognostic stand point, is not a clinical problem. Weight loss after transplantation should be regarded as a simple but important sign of adverse prognosis. These findings point the way to a hypothesis that interventions specifically designed to prevent weight loss might influence outcome following heart transplantation.


   5. Limitations
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Limitations
References
 
We do not have complete data on the pattern of weight change following transplantation. It is possible that the number of missing values could introduce biases into the analysis due to imbalances between patients with and those without follow-up weight data. Nevertheless, we have data on more than 700 patients, representing the largest reported dataset of weight change following heart transplantation. These 798 patients were representative of the group as a whole inasmuch as there was no statistically significant difference in age, body mass index, sodium, or ejection fraction (data not shown) between the group for whom weight change data were available and the others.

Our comparator population in no sense represents a randomised control population, but is included to illustrate the potential effects of weight in a non-transplanted population. We do not know why individual patients were not transplanted and assume the major limiting factor was the availability of organs rather than some other variable that might have impacted on the relation between weight and survival. Since this study was completed, medical therapy for non-transplanted patients has improved, and so the survival in the comparator population is probably an underestimate.

The post-operative immunosuppressive regimen differed between centres and changed over time; however, there was no systematic difference in that regime based on an individual's body mass index. We have no data on cause of death.

We do not have complete data on the baseline left ventricular ejection fraction and peak oxygen consumption, precluding their use in multivariate analysis.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 5. Limitations
 References
 

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