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(Chest. 2002;121:401-406.)
© 2002 American College of Chest Physicians

Impact of Body Weight on Long-term Survival After Lung Transplantation*

William F. Kanasky, Jr, MS; Stephen D. Anton, MS; James R. Rodrigue, PhD; Michael G. Perri, PhD; Thomas Szwed, MD and Maher A. Baz, MD

* From the Department of Clinical and Health Psychology (Mssrs. Kanasky and Anton, and Drs. Rodrigue and Perri), and the Division of Pulmonary and Critical Care Medicine (Drs. Szwed and Baz), University of Florida Health Science Center, Gainesville, FL.

Correspondence to: James R. Rodrigue, PhD, Department of Clinical and Health Psychology, PO Box 100165, University of Florida Health Science Center, Gainesville, FL 32610-0165; e-mail: jrodrigu{at}hp.ufl.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: The purpose of this study was to determine the impact of a pretransplantation determination of body mass index (BMI) on survival after lung transplantation.

Design and patients: Univariate and multivariate survival analyses of a single institution database consisting of 85 patients who had undergone lung transplantations between March 1994 and October 1998.

Setting: University of Florida Health Science Center.

Results: Kaplan-Meier survival curves showed that patients who were obese (ie, BMI, >= 30) at a pretransplantation assessment had a marked decrease in posttransplantation survival time (log rank, p < 0.05; Wilcoxon, p < 0.05). The final Cox regression model revealed that the most powerful predictors of mortality after lung transplantation were higher pretransplantation BMI and the development of obliterative bronchiolitis.

Conclusions: Our results suggest that the posttransplantation risk for mortality is possibly three times greater for obese patients than for nonobese patients. Additional study is needed to identify the mechanisms for such higher risk in obese patients. Our data also suggest that transplantation centers should not routinely reject underweight patients (ie, BMI, < 18.5) or overweight patients (ie, BMI, 25 to 29.9) for lung transplantation listing solely on the basis of weight, as their outcomes may not be significantly different than patients with normal BMIs.

Key Words: body mass index • lung transplantation • obesity • obliterative bronchiolitis • survival analysis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Based on the current World Health Organization (WHO) guidelines,1 over half of adult Americans are considered overweight or obese. Higher levels of body weight and body fat are associated with an increased risk of developing some of the most prevalent diseases in today’s society.2 Specifically, obesity is associated with increased risk of coronary artery disease, stroke, diabetes mellitus, gallbladder disease, degenerative joint disease, and hypertension.

The association between excess body fat and lung function has been widely investigated. Obesity has been found to increase the respiratory muscle demand requiring more oxygen consumption for any given task compared to patients with normal weight.3 This results in a decrease in performance, even in patients with normal lung function.4 Obesity can particularly affect the respiratory physiology in people with pulmonary disease because it alters the relationship between the lungs, the chest wall, and the diaphragm.5 6 Therefore, respiratory function and endurance may be further compromised by the increased pulmonary demands associated with obesity.7 8 Some individuals may be unable to compensate, leading to elevated PaCO2 levels, alveolar hypoventilation, and, consequently, to increased cardiopulmonary morbidity and mortality.9

While the relationship between obesity and impaired respiratory functioning is well-established, little research has been conducted on the effect of obesity on outcomes after lung transplantation. In a consensus statement published in 1998,10 the authors recommended that patients with an ideal body weight of < 70% or > 130% either gain or lose weight to become eligible for lung transplantation. In one study, Snell and colleagues11 showed that the pretransplantation body mass index (BMI) did not predict posttransplantation survival in a small (n = 45), mostly underweight (ie, mean BMI, 19.1; SD, 2.4) sample of lung transplantation recipients with prior cystic fibrosis (CF). However, currently there are no published studies addressing the effects of body weight, especially overweight, on the outcome of patients after undergoing lung transplantation.

Due to the organ donor shortage, appropriate patient selection for lung transplantation requires a careful assessment of risk factors that may affect survival. Identifying BMI classifications that are associated with an increased mortality rate after lung transplantation may aid in the development of guidelines to assist transplantation centers in listing prospective candidates who have weight problems. Therefore, the purpose of this study was to determine the effect of pretransplantation BMI on posttransplantation mortality rate in a large, diverse group of lung transplantation recipients.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Patients
Eighty-five adults with end-stage lung diseases who had undergone lung transplantation at the University of Florida between March 1994 and October 1998 constituted the study population. The criteria for the listing of lung transplantation patients at this institution include the following: end-stage lung disease with a projected life expectancy of < 12 to 24 months; age < 65 years for single-lung transplantation or < 55 years for bilateral lung transplantation; no evidence of significant extrapulmonary disease; good compliance with a medical regimen; psychological stability; no active substance abuse or dependence; ambulatory with oxygen (if required); no history of malignancy in the last 5 years; adequate social support; adequate nutrition; and weight < 130% ideal body weight. Overall, the survival rates for this institution exceeded those reported by the International Society of Heart and Lung Transplantation (ISHLT), as follows: 82% at 1 year (ISHLT, 76%); and 63% at 3 years (ISHLT, 60%).

Pretransplantation demographic and medical data were obtained retrospectively from patients’ medical records. The majority of the patients were men (56.5%), white (100%), and married (70%), with a mean age of 48.6 years (SD, 11.3 years; range, 19 to 64 years). The mean level of education was 13 years (SD, 2.1 years). The most prevalent diagnoses were COPD (52.9%), idiopathic pulmonary fibrosis (27.1%), and CF (10.6%). Sixty-nine percent of the patients were past smokers, having smoked an average of 48 pack-years. The mean FEV1 for obstructive lung disorders (ie, COPD, bronchiectasis, CF, and lymphangiomyomatosis) at the time of transplantation was 20.5% predicted (SD, 11.1% predicted; range, 1 to 75% predicted), while the mean FVC for restrictive lung disorders (idiopathic pulmonary fibrosis and sarcoidosis) was 46.0% predicted (SD, 17.2% predicted; range, 10 to 98% predicted).

BMI Classification
Each patient’s BMI was determined by dividing the patient’s pretransplantation assessment weight by his or her height (kg/m2). According to new clinical guidelines of the WHO1 and the National Institutes of Health,12 underweight is currently defined as a BMI of < 18.5, with normal weight defined as a BMI between 18.5 and 24.9. While a person with a BMI >= 27 was considered to be obese by previous standards,13 the new classification system identifies individuals with a BMI > 30 to be obese, with three distinct classes of obesity specified. Individuals with BMIs between 25 and 29.9 are now classified as overweight. For the purposes of this study, patients were divided into the following four categories according to their pretransplantation BMI: underweight, < 18.5; normal weight, 18.5 to 24.9; overweight, 25 to 29.9; and obese, >= 30.

Infection and Obliterative Bronchiolitis
Patients carefully measured their airflows and temperature on a daily basis as outpatients. Patients with a temperature > 37.8°C were evaluated with blood cultures, chest radiographs, and, when indicated, with bronchoscopy. Infection was defined by the following indications: a positive culture response; changes in the chest radiograph (for the diagnosis of pneumonia); temperature > 37.8°C; and the use of IV antibiotic therapy. Obliterative bronchiolitis (OB) was diagnosed when patients had a progressive decline in their airflows (ie, > 20% from their baseline level), were unresponsive to augmentation in immunosuppression, and were without associated evidence of pulmonary infection. OB was considered as stage 1 when the FEV1 declined by 20 to 33% from baseline, stage 2 when the FEV1 declined 33 to 50% from baseline, and stage 3 when the FEV1 declined > 50% from baseline.14

Statistical Analysis
The length of survival (in months) was calculated from the time of lung transplantation to the time of death or, for those still living, to the date of data analysis. Univariate comparisons between BMI groups were performed using independent-sample t tests, {chi}2 statistics, or one-way analysis of variance with post hoc tests and Bonferroni corrections. Survival estimates were calculated according to the Kaplan-Meier method,15 and curves were compared by the Wilcoxon and log-rank tests. Survival data were analyzed using the Cox proportional hazards model.16 A statistical software package (SPSS for Windows, version 9.0; SPSS; Chicago, IL) was used for analysis of the data. A p value of 0.05 was used as the criterion for statistical significance.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Descriptive Statistics
Eighty-five patients underwent single-lung transplantation (n = 60) or bilateral lung transplantation (n = 25). The mean waiting time for transplantation was 7.1 months (SD, 5.9 months; range, 0.25 to 26 months). Table 1 shows the patient and disease distribution for the four BMI classifications. Twenty-nine patients (34%) were either overweight or obese when placed on the transplantation waiting list.


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  		Table 1.. Patient and Disease Distribution According to Pretransplantation BMI

 
Descriptive statistics for each BMI category were calculated for all of the demographic and medical variables, and are shown in Table 2 . No significant differences between BMI groups existed with respect to age, gender, marital status, smoking history, alcohol use, education, 6-min walk, time since diagnosis, transplantation type, or time spent on the waiting list (all F statistics, > 0.05). However, lung disease type (ie, obstructive, restrictive, or vascular) differed as a function of BMI category ({chi}2 = 20.73; p < 0.01). Table 1 illustrates that overweight and obesity were more prevalent in individuals with restrictive lung disease, while patients with obstructive lung disease tended to be underweight or of normal weight.


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  		Table 2.. Baseline Demographic and Medical Variables by BMI Category*

 
Univariate Analysis of Survival
Patients who were still living (n = 53) at the time of data analysis had been alive at least 22 months after transplantation, with the longest survival time being 74 months. Those patients who had died (n = 32) lived from 1 to 53 months after undergoing transplantation. Kaplan-Meier survival distributions (Fig 1 ) showed that there were significant differences among the survival curves. Patients who were obese at the pretransplantation assessment had a marked decrease in posttransplantation survival time (log rank test, p < 0.05; Wilcoxon test, p < 0.05). Overall, normal weight and overweight patients displayed no significant differences in posttransplantation survival time. Underweight patients had a superior survival curve to those of normal and overweight patients throughout the first 50 months after undergoing transplantation, although these patients had a noticeable decrease in survival thereafter.



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  		Figure 1.. Kaplan-Meier survival distributions by BMI category.

 
Considering the heterogeneity of the sample, Kaplan-Meier survival distributions also were conducted to examine the possible differences in survival among the obstructive, restrictive, and pulmonary vascular lung disease groups. We found that patients with pulmonary vascular disease displayed a steep drop in survival through 20 months posttransplantation. Patients with obstructive and restrictive diseases had similar survival probabilities at 2-year after undergoing transplantation. However, the survival curve for those with restrictive disease had decreased beyond the 2-year mark. Despite these observations, no statistically significant differences were found between the disease groups (log rank test, p = 0.30; Wilcoxon test, p = 0.30)

The freedom from OB was 0.55 at 4 years after transplantation, as calculated by the Kaplan-Meier method. There was no significant difference in the freedom from OB between the obese and nonobese recipients. The incidence of OB was 23 of 75 (32%) in the nonobese group and 2 of 10 (20%) in the obese group. The mean survival time after the onset of OB was 7 months in obese patients and 11 month in nonobese patients. The mean survival time after the diagnosis of infection was 1 and 15 months, respectively, in obese and nonobese patients. Neither of these differences reached statistical significance. There was no significant difference in the prevalence of infection between the obese and nonobese recipients.

Multivariate Analysis of Survival
Cox regression analyses were performed to test the association of specific demographic and medical variables with posttransplantation survival time. Variables with either empirical or theoretical association with lung transplantation survival were included in the analyses. Age, gender, disease, transplantation type, time spent on transplantation list, the development of OB after undergoing transplantation, and pretransplantation BMI were entered into an initial Cox regression model. Six-minute walk test data were available for only 40 patients and, therefore, were not considered as a covariate. Variables showing even a slight trend (p < 0.20) toward significance were considered for inclusion in the final Cox regression model.

In the initial model, higher BMI, double-lung transplantation, and the development of chronic rejection (OB) were associated with decreased survival time after transplantation. No other variables, including age, disease type, time spent on the transplantation list, or gender, contributed significantly to the model. The Cox regression then was rerun with only the significant variables from the initial model. The final model ({chi}2 = 15.07; p = 0.001) revealed that the most powerful predictors of mortality after lung transplantation were higher pretransplantation BMI (p < 0.02; risk of death increases by 7% for each 1.0-unit [kg/m2] increase in BMI) and the development of OB (p < 0.005; odds ratio, 2.85). Double-lung transplantation remained a nonsignificant predictor of survival. Additionally, a model dichotomizing BMI at > 30 (ie, obese vs nonobese patients) was tested to determine whether the effect of BMI was significant, regardless of whether BMI was used as a continuous or dichotomous variable. This analysis ({chi}2 = 19.54; p = 0.0002) revealed that individuals with a BMI of > 30 had a mortality risk that was three times greater than that for nonobese individuals (p < 0.002) [Table 3 ].


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  		Table 3.. Cox Proportional Hazards Model

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
The last 9 years has seen no significant improvements in the 1-year and-3-year survival rates for lung transplantation recipients (73.5% and 59.2%, respectively).17 In addition, lung transplantation survival rates have not kept pace with those for the transplantation of other organs.18 Various comorbid conditions, including obesity, may adversely affect the success of lung transplantation. While several empirical studies in heart, liver, and kidney transplantation patients have identified obesity as a risk factor for poorer postoperative outcome,19 20 21 22 23 this effect has not been found consistently.24 25 Thus, the effects of obesity on organ transplantation survival remain unclear.

Our results are consistent with those of studies finding that preoperative obesity has a strong association with posttransplantation mortality.19 20 21 22 23 The 5-year actuarial survival rate of our obese patient group was remarkably different from those of the underweight, normal, and overweight groups. This significant difference emerged early after transplantation and remained throughout the posttransplantation follow-up period. Furthermore, this association between a BMI of >= 30 and mortality remained even after controlling for the presence of OB. Specifically, the risk for mortality was found to be three times greater in obese individuals compared to nonobese lung transplantation recipients.

The possible factors contributing to the higher mortality rate in the obese group may be associated with their increased mechanical work of breathing and their decreased inspiratory strength and ventilatory efficiency. This impaired respiratory physiology may be especially magnified and deleterious in the obese patients experiencing acute infections or OB. Although the prevalence of infections was not statistically significant between the obese and the nonobese patients, there was a trend toward increased case fatality following infections in the obese group.

Our study sample was small (n = 2) for statistical analysis of the time of survival of obese patients after the onset of OB compared to that for the nonobese population. Obese patients have less respiratory reserve and may not be able to tolerate the progressive decline in lung function associated with OB as well as nonobese recipients. Trends in increased mortality rates after infection and after the onset of OB that were noted in the obese group, although not statistically significant, indicate that those patients with BMIs >= 30 may have higher mortality rates. Thus, significant results may have been found with a larger sample.

Surprisingly, our overweight patients (ie, BMI, 25 to 29.9) also were found to have a survival rate similar to that for normal weight patients (ie, BMI, 18.5 to 24.9). Our results suggest that being overweight does not increase the mortality rate after lung transplantation. This suggests that overweight and obese classifications should not be regarded as equally detrimental when considering risk factors for lung transplantation. One might expect the overweight and obese groups to have similar mortality rates, considering that the previous classification system would have labeled many of our overweight patients as obese. Given our results, further research is needed to determine whether there is a differential impact for overweight and obesity on mortality rates.

The results of this study should be interpreted within the context of a few limitations. While our sample was relatively large (n = 85) for this population, only 10 of our patients were classified as obese (8.5%), and 2 of the 10 had OB. However, this proportion of obese to nonobese patients is similar to transplantation samples in other BMI studies22 24 using the WHO classification system.1 Also, due to the small number of obese patients and the time frame in which the study was conducted, we were unable to determine whether the postoperative mortality risk persisted in the long term for obese patients. This question awaits empirical scrutiny. It is also important to note that we were able to obtain pretransplantation 6-min walk data only on approximately half of our sample. Low 6-min walk distance test results have been found to be an important predictor of survival for patients on the lung transplantation waiting list.26 Finally, the generalizability of these results may be limited, as this was a single-site study.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
The listing of lung transplantation candidates with weight problems remains a difficult task. No published studies currently exist regarding the suitable BMI ranges that will increase the probability of favorable lung transplantation outcome. We have demonstrated that obesity has significant negative effects on survival after lung transplantation. More research is needed to better understand the mechanisms responsible for this increased risk among obese patients. Furthermore, providing obese patients with exercise and weight loss programs to encourage weight loss (ie, to BMI < 30) may be an effective method for increasing their suitability for transplantation. Our data also suggest that transplantation centers should not routinely reject underweight patients (ie, BMI, < 18.5) or overweight patients (ie, BMI, 25 to 29.9) for lung transplantation listing, considering their favorable posttransplantation survival rates.


   Footnotes
 
Abbreviations: BMI = body mass index; CF = cystic fibrosis; ISHLT = International Society of Heart and Lung Transplantation; OB = obliterative bronchiolitis; WHO = World Health Organization

Received for publication January 2, 2001. Accepted for publication September 11, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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