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(Chest. 1999;115:1305-1311.)
© 1999 American College of Chest Physicians

Ventilatory and Diffusion Abnormalities in Long-term Survivors After Orthotopic Heart Transplantation*

Ralf Ewert, MD; Roland Wensel, MD; Martin Bettmann, MD; Susanne Spiegelsberger, MD; Onnen Grauhan, MD; Manfred Hummel, MD and Roland Hetzer, MD

* From Deutsches Herzzentrum, Berlin, Germany.

Correspondence to: Ralf Ewert, MD, Deutsches Herzzentrum Berlin, Augustenburger Platz 1, 13353 Berlin, Germany


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: To investigate the long-term development of pulmonary diffusion abnormalities after orthotopic heart transplantation (oHT).

Design: Retrospective analysis of pulmonary function test results of different patient groups at different time intervals after oHT was performed.

Patients: This investigation included 642 patients who had undergone oHT for chronic heart failure. Patients were grouped according to the time elapsed after transplantation (group 1: n = 164; age, 47 ± 14 years; days after oHT, 324 ± 101; group 2: n = 100; age, 48 ± 15 years; days after oHT, 723 ± 104; group 3: n = 106; age, 52 ± 12 years; days after oHT, 1,092 ± 98; group 4: n = 84; age, 51 ± 13 years; days after oHT, 1,442 ± 99; group 5: n = 61; age, 50 ± 14 years; days after oHT, 1,819 ± 105; group 6: n = 101; age, 53 ± 12 years; days after oHT, 2,463 ± 303; and group 7: n = 26; age, 54 ± 14 years; days after oHT, 3,478 ± 246). In 56 (group 8) of the 642 patients, follow-up measurements were performed with tests before and at two time points after oHT (6.5 ± 1.7 and 12.5 ± 9.3 months).

Results: Of all patients, 39% showed restrictive and obstructive abnormalities with no differences between the groups. No significant differences in lung transfer factor for carbon monoxide (DLCO) were observed (61.2 vs 63.7 vs 65.5 vs 65.6 vs 64.5 vs 65.7 vs 67.6% predicted). Differences in transfer coefficient for carbon monoxide (KCO) were significant between group 1 and 4 (58.7 vs 64.1% predicted), and group 1 and 6 (58.7 vs 63.4% predicted). No differences occurred in the rate with which patients exhibited pathologic abnormalities for DLCO and KCO. After oHT, a marked reduction in diffusion capacity occurred in group 8. On follow-up, these measurements were only slightly restored in terms of the predicted DLCO percentage. No such improvement was observed in KCO or in the rate of pathologic changes for both DLCO and KCO. We conclude, therefore, that the impairment of diffusion does not improve even after a significant period has passed after the oHT. Whether this has any effect on symptoms and/or the prognosis for these patients is extremely unclear.

Key Words: chronic heart failure • diffusion capacity • heart transplantation • long-term follow-up • pulmonary function test


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Impairment of respiratory function is frequently observed in patients with chronic heart failure (CHF).1 2 3 4 5 It is caused by increased heart size and recurrent pleural effusions. Other contributing factors are pulmonary venous congestion with interstitial edema and progressive fibrosis as well as impaired alveolar perfusion.6 7 Although restrictive and obstructive changes occur early in the course of heart failure, diffusion capacity can still be normal or even increased.4 5 This is thought to result from an increased alveolar capillary blood volume. As the disease progresses, structural changes of the alveolocapillary membrane develop that lead to an impaired diffusion capacity.8 9

Changes in respiratory function correlate with hemodynamic changes and are useful parameters for the assessment of the stage and the severity of the disease in follow-up of CHF patients.4 5 10 Successful treatment of the underlying disease also results in normalization of respiratory function.11 12 13 Similarly, in patients who have undergone orthotopic heart transplantation (oHT), restrictive and obstructive ventilatory abnormalities, acquired in the course of heart failure, improve in the first year after transplantation.14 15 16 17 Interestingly, these patients show a persistent impairment of pulmonary diffusion capacity that is probably due to thickening of the alveolocapillary membrane.3 15 18 The view that a potential causative role17 20 21 of infection by the human cytomegalovirus (hCMV)18 19 or drug toxicity by cyclosporine is controversial. Previous studies, which have addressed the issue of diffusion capacity im-pairment in long-term survivors after oHT, did not yield conclusive results, mainly because of the limited time for follow-up and the small patient groups.16 17 20 However, there are studies that suggest a normalization of diffusion capacity does occur after oHT.

We observed a high prevalence of diffusion abnormalities among long-term survivors of oHT.22 To add evidence to the debate over the development of diffusion abnormalities after oHT, we analyzed the prevalence and the severity of the diffusion abnormalities in a large number of patients who have undergone transplantation at our institute over the last 11 years.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
Between 1994 and 1997, we carried out pulmonary function tests on 642 patients who had undergone oHT. Patients were grouped according to the number of years that had elapsed after transplantation (groups 1 through 7). To obtain a sufficient number of patients in each group, patients at years 5 to 8 and 9 to 11 after oHT were assigned to groups 6 and 7, respectively. Patients who suffered a rejection or infection 3 months prior to examination or those with a history of smoking were excluded from the study. Routine chest radiographs revealed that there was no evidence of pulmonary interstitial disease in any of the patients.

Patient characteristics and the time elapsed after oHT at the time of pulmonary function tests are given in Table 1 . Groups were matched for gender and the etiology of their heart failure. Data for the hCMV status of the recipients prior to transplantation were incomplete, and there were no data for hCMV infection following oHT. Episodes of graft rejection were analyzed in all patients. Dependent on the time that had elapsed after oHT, the percentage of patients who experienced three or more episodes of acute rejection increased by 5.5% in group 1 and 12%, 9.4%, 13.1%, 26.2%, 33.3%, and 30.8% in groups 2 through 7, respectively. Twelve months prior to this study, cyclosporine, azathioprine, and corticosteroids were used for immunosuppression in all patients.


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  		Table 1. Patient Characteristics*

 
In 56 of the 642 patients (group 8: 9 female, 47 male; 14 with coronary heart disease, 42 with cardiomyopathy), we undertook follow-up measurements. In these patients, respiratory function tests were performed prior to (6.5 ± 4.2 months; range, 0.1 to 16.9 months) and after transplantation (6.5 ± 1.7 months; range, 2.6 to 11.9; and 12.5 ± 9.3 months; range, 8.3 to 41.2 months). The serologic hCMV status was available for 53 of the 56 patients prior to transplantation (26 anti-hCMV-IgG positive and 27 hCMV-IgG negative). Data concerning hCMV infection after transplantation were not available. Episodes of rejection were analyzed in all patients (we found 11 patients with no acute rejection episodes and none with more than three rejection episodes in the period of observation). In all patients, immunosuppressive therapy consisted of cyclosporine, azathioprine, and corticosteroids.

Pulmonary Function
Spirometry and body plethysmography were performed using a constant-volume body plethysmograph (Master Lab; Jäger; Würzburg, Germany). For final analysis, the following parameters were selected: vital capacity (VC), FVC, the ratio of FEV1 to FVC, total lung capacity (TLC), and the ratio of RV to TLC (RV:TLC). For the measurement of diffusion capacity, the single-breath technique that uses carbon monoxide (CO) was employed (Transferscreen; Jäger). For final analysis, the lung transfer factor for CO (DLCO) and the CO transfer coefficient (KCO, as transfer factor for CO per alveolar volume; DLCO/alveolar volume) in mmol/min/kPa (1 kPa = 7.502 mm Hg) were selected. Because DLCO is dependent on the hemoglobin concentration, patients with anemia were excluded. Dependent on the values of DLCO and KCO as a percentage of predicted impairments of diffusion capacity, a classification system was established: mild (60 to 79%), moderate (40 to 59%), and severe (< 40%).

All measurements were done in accordance with the guidelines of the European Respiratory Society, and for each individual, the values were also expressed as a percentage of the predicted values derived from age- and sex-matched healthy control subjects.23

Statistical Analysis
Data are expressed as mean ± SD. To test for significance between different groups, an analysis of variance (ANOVA) was applied; if normal distribution tests failed, the nonparametric Kruskall-Wallis ANOVA was used. Follow-up data of group 8 were analyzed by a repeated measure ANOVA. To isolate significant differences between groups, the Dunn's procedure was used. For evaluation of nominally structured data, the {chi}2 test was applied. The p level of significance was < 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Ventilatory Parameters
In the 642 patients of groups 1 through 7, restrictive abnormalities (defined as VC < 80% predicted) were observed in 39% (range, 31 to 45%; Table 2 ). Body plethysmographic measurements gave pathologic values for TLC (defined as a value of < 80% predicted) in 28% (range, 23 to 33%). There were no significant differences between the groups for VC, FVC, and TLC in absolute or percentage predicted values or in the rate of incidence of patients with pathologic abnormalities. Obstructive abnormalities (defined as FEV1; VC < 75%) were found in 39% of these patients (range, 27 to 44%; Table 3 ). For both ratios of FEV1:VC and RV:TLC (pathologic when 120% over the predicted level), there were no significant differences in the percentage predicted values or in the rate of incidence of patients with pathologic abnormalities between the different groups of patients.


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  		Table 2. Restrictive Abnormalities

 

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  		Table 3. Obstructive Abnormalities

 
In the 56 patients of group 8, we observed restrictive abnormalities (defined as VC < 80% predicted) in 43% preoperatively (Table 4) . Body plethysmographic measurements gave pathologic values for TLC (defined as the value of < 80% predicted) in 27%. Obstructive abnormalities were found in 41% when defined as the ratio FEV1:VC that was < 75% of that predicted and in 43% of patients when the ratio RV:TLC was > 120% of that predicted was used.


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  		Table 4. Pulmonary Function Abnormalities in Group 8

 
Although the mean percentage predicted values of VC and TLC (p < 0.05; Table 4 ) increased after transplantation, the number of patients with pathologic abnormalities in VC and TLC did not change significantly when compared with pretransplant values. There was no improvement in obstructive abnormalities in the rate of pathologic change or in the mean percentage predicted values after oHT (Table 4) .

Diffusion Capacity
Of the 642 patients in groups 1 through 7, 83% (range, 74 to 90%) and 90% (range, 83 to 96%) showed pathologic diffusion abnormalities as measured by DLCO and KCO, respectively (Table 5) . These changes were mild in 36% (DLCO) and 40% (KCO), moderate in 36% (DLCO) and 44% (KCO), and severe in 6% (DLCO) and 3% (KCO). There were no significant differences in DLCO (percentage predicted and the rate of incidence of patients with pathologic changes) between groups 1 through 7 (Fig 1) . Changes in KCO (percentage predicted) were significant only when comparisons were carried out between group 1 and 4 (58.7% vs 64.1%; p < 0.05) and groups 1 and 6 (58.7% vs 63.4%; p < 0.05; Fig 2 ). The rate of incidence for patients with pathologic changes in KCO did not differ significantly among all groups. Linear regression of the KCO values (percentage predicted) of all patients is given in Figure 3 . Although significant (p < 0.05), the slope of the regression is fairly low (0.0015)—the correlation coefficient is 0.11.


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  		Table 5. Diffusion Abnormalities in Groups 1 Through 7

 


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  		Figure 1. DLCO in percent predicted (dotted line = mean: solid line = median).

 


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  		Figure 2. KCO in percent predicted (dotted line = mean: solid line = median).

 


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  		Figure 3. Linear regression of KCO vs time after oHT (mean 95% confidence interval; 95% prediction interval).

 
Preoperative testing of the patients of group 8 revealed an impaired diffusion capacity in 46% (DLCO) and 59% (KCO) of the patients. At the first control test after oHT, these values were significantly increased to 95% (DLCO) and 96% (KCO), respectively. Mean percentage predicted values were decreased when compared with pretransplant values (Table 4) . During the posttransplant follow-up period, there was a slight but significant improvement in DLCO (percentage predicted values) that, however, was still markedly below pretransplant values. Neither absolute nor percentage predicted values for KCO (Fig 4) changed over this period. The same applies for the rate of pathologic changes for both KCO and DLCO.



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  		Figure 4. KCO values in group 8 pre-oHT and post-oHT (mean ± SD).

 
In groups 1 through 7, as well as in group 8, hCMV status and the occurrence and frequency of rejection did not cause a significant difference in any of the respiratory function parameters.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Impairment of pulmonary function, secondary to CHF, is well known.1 5 8 9 14 17 18 24 25 26 We observed restrictive abnormalities in 43% (VC) and 27% (TLC) of our patients; other authors have reported rates of 8 to 50%2 3 16 26 for TLC. Of our study population, 41% (FEV1:FVC) and 43% (RV:TLC) showed obstructive ventilatory abnormalities. Other studies have reported rates of 4 to 32%.2 3 4 16 Both restrictive and obstructive abnormalities recovered within the first postoperative year in our patients, which is comparable to previous studies that demonstrated a significant increase in FVC, FEV1, TLC, and FEV1:VC after transplantation.14 16 17 19 26 One study showed an improvement in the spirometric parameters of up to 30% in the first year after transplantation.15 In our long-term survivors (groups 1 through 7), we observed a constant prevalence for restrictive and obstructive ventilatory abnormalities with no subsequent improvement after the first year. This implies that after the initial restoration of ventilatory function, which occurs within the first year of oHT, no further improvement occurs.

Depending on the severity of the disease, patients with CHF show a prevalence for pulmonary diffusion abnormalities ranging from 36 to 93%.3 4 5 8 9 15 16 17 18 19 24 26 We observed diffusion abnormalities in 46% (DLCO) and 59% (KCO) of our patients. Our study sought to demonstrate the prevalence and the time course for pulmonary diffusion abnormalities after transplantation. This was done by the investigation of seven patient groups that were at different time points after transplantation. In addition, we investigated one group of patients before and at two time points after transplantation. The main result was that transplantation produces a major increase in the rate and the severity of pulmonary diffusion abnormalities. This is comparable to the results of other authors who have described diffusion abnormalities as a problem that occurs after oHT.17 18 20 21 Also, the data from groups 1 through 7, as well as the follow-up data from group 8, demonstrate that no relevant restoration of diffusion capacity occurs, but that there is a persistence of these alterations in the long term after oHT. A comparison between the seven groups of patients studied after oHT showed no significant differences in DLCO (percentage predicted) or in the frequency of pathologic changes. Although there has been no difference in the frequency of pathologically decreased KCO values among the groups, a significant increase occurred between groups 1 and 4 and groups 1 and 6 when considering only the percentage predicted values. However, this increase was 3.4% and 4.7%, respectively, and mean values were still clearly within the pathologic range. Comparable data from the follow-up investigation in group 8 showed a slight improvement of the diffusion capacity of 5.1% (DLCO) at the second time point after transplantation, but there was still no decrease in the frequency of the pathologic values. Therefore, the clinical relevance of these changes is rather questionable.

This is in contrast to other studies, that suggests that a time-dependent restoration of pulmonary diffusion capacity after oHT occurs.16 17 20 However, our data, particularly with regard to KCO, do not support this. The slight improvement in DLCO, observed at the second time point after transplantation, results mainly from an increase in TLC that is attributable to improved rib cage mechanics.27 28 29 30 31 Therefore, the actual diffusion capacity remains persistently impaired, which suggests that the structural changes of the alveolocapillary membrane that develop in the natural course of CHF do not regress, even in the long term, although the leading stimulus, pulmonary venous congestion, is readily removed by transplantation. Possibly there are other factors that are specific to transplantation that prevent the restoration of the diffusion capacity. The role of subclinical alveolitis caused by hCMV infection, vasopressor and proliferative effects of cyclosporine, episodes of rejection, and fibrotic residues of recurrent pulmonary infections are possible factors but remain controversial. Since hCMV infection, rejection, and cyclosporine are part of the immunosuppression problem, there are data that suggest that there is no relationship between these conditions and the impairment of diffusion in patients with heart transplant over the long term.22

In patients with CHF,5 8 30 impairment of diffusion capacity has been shown to correlate with exercise capacity. However, it has also been shown as not limiting exercise capacity in CHF patients and in transplant patients.20 31 So far only ventilatory abnormalities have been reported that correlate with a decreased exercise capacity after oHT.31 Furthermore, to our knowledge, there are no data available that investigate whether or how impaired diffusion capacity affects the prognosis in patients who have undergone transplantation.

In conclusion, diffusion abnormalities acquired in the course of CHF are not cured by heart transplantation, but there is a deterioration, and there is no significant improvement with time after transplantation. The clinical relevance of this impaired diffusion capacity in terms of symptoms and prognosis of patients with transplants is extremely unclear.


   Acknowledgements
 
We are indebted to Gisela Tonn for her technical assistance in the pulmonary function tests, to Stefanie Heins for the support in the data management and statistical analysis, and to Tonie Derwent for assistance with this article.


   Footnotes
 
Abbreviations: ANOVA = analysis of variance; CHF = chronic heart failure; CO = carbon monoxide; DLCO = lung transfer factor for carbon monoxide; hCMV = human cytomegalovirus; KCO = transfer coefficient for carbon monoxide; oHT = orthotopic heart transplantation; RV = residual volume; TLC = total lung capacity; VC = vital capacity

Received for publication May 28, 1998. Accepted for publication December 22, 1998.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Siegel, JL, Miller, A, Brown, LK, et al (1990) Pulmonary diffusing capacity in left ventricular dysfunction. Chest 98,550-553[Abstract/Free Full Text]
  2. Ohar, J, Osterloh, J, Ahmed, N, et al (1993) Diffusion capacity decreases after heart transplantation. Chest 103,857-861[Abstract/Free Full Text]
  3. Wright, RS, Levine, MS, Bellamy, PE, et al (1990) Ventilatory and diffusion abnormalities in potential heart transplant recipients. Chest 98,816-820[Abstract/Free Full Text]
  4. Naum, CC, Sciurba, FC, Rogers, RM (1992) Pulmonary function abnormalities in chronic severe cardiomyopathy preceding cardiac transplantation. Am Rev Respir Dis 145,1334-1338[ISI][Medline]
  5. Kraemer, MD, Kubo, SH, Rector, TS, et al (1993) Pulmonary and peripheral vascular factors are important determinants of peak exercise oxygen uptake in patients with heart failure. J Am Coll Cardiol 21,641-648[Abstract]
  6. West, JB, Mathieu-Costello, O (1992) Stress failure of pulmonary capillaries: role in lung and heart disease. Lancet 340,762-767[CrossRef][ISI][Medline]
  7. Davies, SW, Bailey, J, Keegan, J, et al (1992) Reduced pulmonary microvascular permeability in severe chronic left heart failure. Am Heart J 124,137-142[CrossRef][ISI][Medline]
  8. Puri, S, Baker, L, Dutka, DP, et al (1995) Reduced alveolar-capillary membrane diffusing capacity in chronic heart failure. Circulation 91,2769-2774[Abstract/Free Full Text]
  9. Puri, S, Baker, BL, Oakley, CM, et al (1994) Increased alveolar/capillary membrane resistance to gas transfer in patients with chronic heart failure. Br Heart J 72,140-144[Abstract/Free Full Text]
  10. Ettlinger, NA, Trulock, EP (1991) Pulmonary considerations of organ transplantation, part 3. Am Rev Respir Dis 144,433-451[ISI][Medline]
  11. Ohno, K, Nakahara, K, Hirose, H, et al (1987) Effects of valvular surgery on overall and regional lung function in patients with mitral stenosis. Chest 92,224-228[Abstract/Free Full Text]
  12. Braun, S, Birnbaum, ML, Chopra, PS (1978) Pre- and postoperative pulmonary function abnormalities in coronary artery revascularization surgery. Chest 73,316-320[Abstract/Free Full Text]
  13. Mustafa, KY, Nour, MM, Shuhaiber, H, et al (1984) Pulmonary function before and sequentially after valve replacement surgery with correlation to preoperative hemodynamic data. Am Rev Respir Dis 130,400-406[ISI][Medline]
  14. Hosenpud, J, Stibolt, TA, Atwal, K, et al (1990) Abnormal pulmonary function specifically related to congestive heart failure: comparison of patients before and after cardiac transplantation. Am J Med 88,493-496[CrossRef][ISI][Medline]
  15. Ravenscraft, SA, Gross, CR, Kubo, SH, et al (1993) Pulmonary function after successful heart transplantation. Chest 103,54-58
  16. Bussières, LM, Pflugfelder, PW, Ahmad, D, et al (1995) Evolution of resting lung function in the first year after cardiac transplantation. Eur Respir J 8,959-962[Abstract]
  17. Groen, HJM, Bogaard, JM, Balk, AH, et al (1992) Diffusion capacity in heart transplant recipients. Chest 102,456-460[Abstract/Free Full Text]
  18. Egan, JJ, Kalra, S, Yonan, N, et al (1993) Pulmonary diffusion abnormalities in heart transplant recipients. Chest 104,1085-1089[Abstract/Free Full Text]
  19. Egan, JJ, Lowe, L, Yonan, N, et al (1996) Pulmonary diffusion impairment following heart transplantation: a prospective study. Eur Respir J 9,663-668[Abstract]
  20. Jahnke, AW, Leyh, R, Guha, M, et al (1994) Time course of lung function and exercise performance after heart transplantation. J Heart Lung Transplant 13,412-417[ISI][Medline]
  21. Mouly-Bandini, A, Badier, M, Guillot, C, et al (1995) Functional evolution after cardiac transplantation. Transplant Proc 27,2524[ISI][Medline]
  22. Ewert, R, Walde, T, Wensel, R, et al (1998) Long term persistence of lung function abnormalities after heart transplantation. Transplant Proc 30,1889-1891[CrossRef][ISI][Medline]
  23. . European Community for Steel and Coal (1993) Standardized lung function testing. Eur Respir J 6 (suppl 16),1S-100S
  24. Bussieres, LM, Cardella, CJ, Daly, PA, et al (1990) Relationship between preoperative pulmonary status and outcome after heart transplantation. J Heart Transplant 9,124-128[ISI][Medline]
  25. Sullivan, MJ, Higginbotham, MB, Cobb, FR (1988) Increased exercise ventilation in patients with chronic heart failure: intact ventilatory control despite hemodynamic and pulmonary abnormalities. Circulation 77,552-559[Abstract/Free Full Text]
  26. Casan, P, Sanchis, J, Cladella, M, et al (1987) Diffusion lung capacity and cyclosporine in patients with heart transplants. J Heart Transplant 6,54-56[Medline]
  27. Locke, TJ, Griffiths, TL, Mould, H, et al (1990) Rib cage mechanics after median sternotomy. Thorax 45,465-468[Abstract]
  28. Louagie, Y, Gonzalez, E, Jamart, J, et al (1993) Postcardiopulmonary bypass lung edema. Chest 103,86-95
  29. Sinclair, DG, Haslam, PL, Quinlan, GJ, et al (1995) The effect of cardiopulmonary bypass on intestinal and pulmonary endothelial permeability. Chest 108,718-724[Abstract/Free Full Text]
  30. Wasserman, K, Zhang, YY, Gitt, A, et al (1997) Lung function and exercise gas exchange in chronic heart failure. Circulation 96,2221-2227[Abstract/Free Full Text]
  31. Brubaker, PH, Brozena, SC, Morley, DL, et al (1997) Exercise-induced ventilatory abnormalities in orthotopic heart transplant patients. J Heart Lung Transplant 16,1011-1017[ISI][Medline]



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