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Ann Thorac Surg 2007;83:257-263
© 2007 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Feasibility and Utility of a Lung Donor Score: Correlation With Early Post-Transplant Outcomes

Takahiro Oto, MD, Bronwyn J. Levvey, RN, Helen Whitford, MD, Anne P. Griffiths, FRCNA, Tom Kotsimbos, MD, Trevor J. Williams, MD, Gregory I. Snell, MD*

Department of Allergy, Immunology, and Respiratory Medicine, Lung Transplant Unit, The Alfred Hospital and Monash University, Melbourne, Australia

Accepted for publication July 18, 2005.

* Address correspondence to Dr Snell, Department of Allergy, Immunology, and Respiratory Medicine, The Alfred Hospital, Commercial Road, Melbourne, Victoria 3004, Australia (Email: g.snell{at}alfred.org.au).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: A lung donor score may provide a numerical value of overall donor lung "quality" to allow comparison among different organizations and research protocols. This study aims to develop a simple scoring system and investigate its applicability on predicting donor selection and early post-lung-transplant (LTx) outcomes.

METHODS: Data of all donors referred to our institution in 2001 were initially analyzed to create a LTx donor score. Five domains, age, smoking history, chest X-ray, secretions, and arterial blood gas results, were included. A larger cohort of transplant recipients (years 2002 to 2005) was analyzed to validate the score against early post-LTx outcomes.

RESULTS: In the initial 2001 cohort, 36 of 87 (41%) donors were used for 41 LTx (used group) and 51 (59%) were declined for medical (lung-exclusion group, n = 31) and general (general-exclusion group, n = 20) reasons. The median donor scores in the used, general-exclusion, and lung-exclusion groups were 2.0, 2.0, and 10.0, respectively (p < 0.0001). In multivariate analysis of the validation cohort, the donor score in bilateral LTx was significantly associated with post-transplant ratio of arterial oxygen tension and inspired oxygen fraction (coefficient = –16.19, p = 0.002), primary graft dysfunction grade (coefficient = 0.21, p < 0.0001), and intubation hours (coefficient = 0.05, p = 0.04); however, a significant association was not seen in single LTx.

CONCLUSIONS: A proposed simple donor scoring system, based on five major donor variables available at the time of donor selection, may be useful for data comparison between specific centers, quality control, evaluative research, and clinical decision making in donor selection and management in LTx.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
The availability of suitable donor lungs is the major limitation to increasing the overall provision of lung transplant services to patients with end-stage pulmonary diseases. Many different strategies have been employed to remedy the problem [1–10]. Donor acceptability criteria have been broadened and utilization of the so-called "extended" donors has contributed to significantly expanding the donor pool [2–12]. Several studies have described the utilization of these extended donors and demonstrated acceptable early outcomes in single centers [5, 7–14]. However, the full impact of these extended donors on early and late outcomes for all lung transplant centers remains unclear, as the lack of a standardized donor scoring system makes it difficult to compare the types of donors used across different lung transplant programs.

Nyberg and colleagues [15] have recently reported the successful application of a standardized donor scoring system in renal transplantation. The concept of a lung donor score can therefore be proposed as a potentially useful mechanism to better understand donor acceptability criteria and their impact on outcomes. Applying a numerical value of overall donor lung "quality" would allow comparison among different donor procurement organizations and across different investigational protocols. Ultimately, this would allow the prospect of expanding the lung donor pool using a validated donor evaluation tool. The specific aims of this study are to develop a simple lung donor scoring system and to investigate the applicability of the scoring system on donor selection and on prediction of early post-lung transplant outcomes.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Donor Scoring System
A lung donor score was created with five domains that represented the most important clinical criteria that defined lung donor organ quality [2, 3, 7–13, 17–19]. Each variable was subdivided and weighted between 0 and 3 based on perceived clinical importance, with the exception of the ratio of arterial oxygen tension and inspired oxygen fraction (PaO 2/FIO 2), which was prospectively given a double weighting because of its increased clinical significance [2, 6, 13, 16, 17] (ie, between 0 and 6) (Table 1).


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  		Table 1. Donor Scoring Criteria and Outcomes (Initial Cohort—2001)
 
Primary and Secondary Donor Score Outcome Variables
The primary outcome of the lung donor score was its utilization for transplantation and the secondary outcome for the donor score was the predictive value of score for early post-transplant outcomes. All donors referred in 2001 were included to investigate the primary outcome of the donor score (initial cohort) and then the predictive value of the score was validated with adjustment of other donor, recipient, and operative factors by multivariate analysis (validation cohort). For this purpose, outcome data of transplants performed from 2002 to 2005 were used. Institutional Ethics Committee advice was sought and specific consent was not required as no intervention was undertaken and the study represented clinical audit.

Initial Cohort
Data on all donors referred to The Alfred Hospital between January 2001 and December 2001 were collected prospectively and the donors were able to be divided into three groups. The three groups were the following: those used for transplantation (used group) and those who were not used for transplantation due to (1) specific general donor history exclusion criteria or logistic issues (general exclusion group) or (2) medically not suitable for transplantation or damaged (lung exclusion group).

Validation Cohort
For a larger validation cohort, data of 157 lung transplants, including 109 bilateral, 42 single, and 6 heart-lung transplants performed at the Alfred Hospital from January 2002 to December 2005, were retrieved retrospectively from a transplant database. A complete data set for multivariate analysis, including donor, recipient, operative factors, and early post-transplant outcomes, was available from 138 of 157 (88%) patients; thus, data from these 138 patients were included for validation analysis (Table 2). The PaO 2/FIO 2 ratio within 12 hours after final reperfusion [16], duration of intubation, length of intensive care unit (ICU) stay [17], The International Society for Heart and Lung Transplantation primary graft dysfunction grades at 72 hours after transplant [18], 30-day mortality, and one-year survival [19] were used as post-transplant outcomes. The donor score was calculated retrospectively for the purpose of this study and the actual score was not directly used in the decision-making process of donor selection.


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  		Table 2. Demographics of the Donor and Recipient for a Validation Cohort (2002 to 2005)
 
Donor Assessment and Management
The Australian system of lung donor assessment and management has been described elsewhere [1, 5, 6]. Donor information, including a standardized interview from the donor’s family, donor medical history details, and basic investigations, are collected by a donor transplant coordinator. Details include the respiratory history (asthma, cigarette intake, aspiration), sputum volumes and purulence, antibiotic therapy, donor height, blood group, blood gas results, and chest X-ray findings. The lung transplant physician aims to directly review the donor, their actual medical record and radiology, as well as to perform a bronchoscopy. Discussions regarding donor management, including repeated suctioning, physiotherapy, revisions of antibiotic therapy, and fluid management, occur with the intensive care staff to optimize the donor for transplantation. Repeat assessment, including chest X-ray and serial arterial blood gases may need to be undertaken after donor management changes, before a final decision is made to accept or decline donor organs.

Lung Donor Acceptability Criteria
To determine donor lung acceptability, locally modified standard criteria have been used at The Alfred Hospital [6]. Briefly, donors with the following modified criteria, age between 55 and 65, a smoking history between 20 and 60 pack-years, a PaO 2/FIO 2 ratio between 250 and 300, abnormality on chest X-ray, and abnormal findings on bronchoscopy (including purulent secretion and aspiration) may be considered for lung transplant as extended donors. Donors with bilateral abnormality on chest X-ray are preferentially considered for bilateral lung transplants and donors with unilateral abnormality can be considered for single lung transplants utilizing the unaffected side. Donors with significantly abnormal bronchoscopy findings (aspirated gastric material, excessive purulent secretions) might be acceptable when the donors also have a PaO 2/FIO 2 greater than 300 and a clear chest X-ray. These extended donor lungs are likely to be used for a potential recipient whose prognosis is poor and are unlikely to be transplanted otherwise, particularly if a bilateral transplant can be configured with two lungs available for that one recipient.

Lung Transplant Surgical Technique and Perioperative Management
Lung procurement and preservation followed standard procedure [20]. Different lung preservation solutions have been used in the different era during the study period [21]. Cardiopulmonary bypass was not routinely performed in our institution and only considered when intolerance of single lung ventilation due to hemodynamic instability was seen. Prior to implantation, a limited volume of retrograde flush was performed to detect any unexpected pulmonary embolism in the donor lungs [22]. Postoperative management in ICU was performed to ensure satisfactory end organ perfusion while maintaining a relatively low filling pressure (cardiac index > 2.4, pulmonary capillary wedge pressure < 10 mm Hg, and central venous pressure < 7 mm Hg). Patients with primary graft dysfunction received standardized evaluation and therapy with increasing complexity depending on the degree of ventilatory and hemodynamic compromise [16–19, 23].

Statistical Analysis
Continuous data were initially assessed for normality and log-transformed if appropriate. Duration of intubation and length of ICU stay were both found to be well-approximated by a log-normal distribution. Comparison between groups was performed with the Mann-Whitney U test or the Kruskal-Wallis test for nonparametric continuous variables, the unpaired t test or one-way analysis of variance for parametric continuous variables, and the {chi}2 test or the Fisher exact test for categoric variables. Univariate analysis was performed on log-transformed intubation time, log-transformed ICU stay, post-transplant PaO 2/FIO 2, and primary graft dysfunction grades using linear regression. All variables (Table 2) suggested by the univariate analysis with a level of significance defined as p less than 0.2, or those judged to be clinically important, were included in the multivariate model. Multivariate models were constructed using a stepwise selection technique and validated using a backward elimination technique and further assessed for biological and clinical plausibility. Data were expressed as median and interquartile range, mean ± SD, and count and proportions if appropriate. Analysis was performed using the Statview 5.0 software package (SAS Institute Inc, Cary, NC). A p value of 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Initial Cohort-Donor Organ Utilization
The results focused on an initial cohort of 87 lung donors were offered to The Alfred Hospital from January 2001 to December 2001 (Fig 1). Thirty-six of 87 (41%) donors were used for lung transplantation (Used group) and 41 transplants, including 21 single, 19 bilateral, and 1 heart-lung were performed. Fifty-one donors (59%) were declined because 31 were medically unsuitable (lung exclusion group) and 20 had general exclusion criteria (general exclusion group).


Figure 1
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  		Fig 1. Results of all donor offers to The Alfred Hospital from January 2001 to December 2001.

 
Initial Cohort-Donor Score
Donor scoring criteria and scores of all donors offered for lung transplantation in 2001 are shown in Table 1. Donors in the lung exclusion group as expected tended to score higher in each category, especially in chest X-ray, secretions, and PaO 2/FIO 2 ratio. The PaO 2/FIO 2 in the lung exclusion group (median = 273 [interquartile range = 175 to 360]) was lower than that in the used (median = 505 [382 to 520]) and general exclusion (median = 447 [370 to 515]) groups (p < 0.0001). The PaO 2/FIO 2 ratios of all the donors in the used and general exclusion groups were higher than 300.

The numbers of donors at each cumulative donor score in this 2001 cohort are shown in Fig 2. In the used group, the number of donors was decreased in inverse proportion to the donor score, and no donor scored more than 7 [median = 2.0 (0.8 to 4.0)]. In the general exclusion group, all the donors except one scored less than 7 (median = 2.0 [1.0 to 5.5]). In contrast, the majority of the donors in the lung exclusion group scored more than 7 (median = 10.0 [7.2 to 11.0]). The difference in lung donor score among the three groups was statistically significant (p < 0.0001).


Figure 2
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  		Fig 2. The number of donors in each cumulative donor score in 2001.

 
Initial Cohort-Donor Score and Post-Transplant Outcomes
In the initial cohort, the donor score was significantly associated with post-transplant PaO 2/FIO 2 (R = –0.71, p = 0.0005), duration of intubation (R = 0.75, p = 0.0003), length of ICU stay (R = 0.66, p = 0.002), and primary graft dysfunction grade (R = 0.57, p = 0.02) in bilateral lung (including heart-lung) transplants. In single lung transplants, the donor score was not significantly associated with post-transplant PaO 2/FIO 2 (R = –0.15, p = 0.56), duration of intubation (R = 0.09, p = 0.72), length of ICU stay (R = 0.14, p = 0.56), and primary graft dysfunction grade (R = 0.07, p = 0.83).

Validation Cohort-Donor Score and Post-Transplant Outcomes
In the validation cohort, median donor score in each transplant year was 3.0 (2.0 to 5.0) in 2002, 3.0 (2.0 to 4.0) in 2003, 3.0 (1.0 to 4.0) in 2004, and 4.0 (2.0 to 5.6) in 2005. A higher score (ranging from 0 to 10) was seen in the donors used in recent years compared with the donors used in 2001 (2.0 [0.8 to 4.0]) (p = 0.01). In univariate analysis, the donor score of the total lung transplants was significantly associated with post-transplant PaO 2/FIO 2 (R = –0.26, p = 0.0007), primary graft dysfunction grade (R = 0.20, p = 0.009), duration of intubation (R = 0.24, p = 0.002), and length of ICU stay (R = 0.22, p = 0.004). In bilateral lung (including heart-lung) transplants the donor score was also significantly associated with post-transplant PaO 2/FIO 2 (R = –0.39, p < 0.0001), primary graft dysfunction grade (R = 0.27, p = 0.003), duration of intubation (R = 0.38, p < 0.0001), and length of ICU stay (R = 0.27, p = 0.002) (Fig 3). In contrast, the donor score of single lung transplants was not associated with post-transplant PaO 2/FIO 2 (R = 0.07, p = 0.64), primary graft dysfunction grade (R = 0.01, p = 0.97), duration of intubation (R = 0.23, p = 0.12), and length of ICU stay (R = 0.03, p = 0.81).


Figure 3
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  		Fig 3. Regression analyses between donor score and post-transplant outcomes in the 2002 to 2005 validation cohort. (A) PaO 2/FIO 212 hours after transplantation (PaO 2/FIO 2 [y axis] = 409.2 – 19.1 donor score [x axis]). (B) Log-transformed intubation hours (log intubation hours [y axis] = 1.21 + 0.07 donor score [x axis]). (PaO 2/FIO 2 = ratio of arterial oxygen tension and inspired oxygen fraction.)

 
Validation Cohort-Multivariate Regression Analysis
Multivariate regression analysis for early post-transplant outcomes in bilateral lung transplant is shown in Table 3. The donor score was a significant and independent predictor for recipient PaO 2/FIO 2, primary graft dysfunction grades, and duration of intubation; however, not for length of ICU stay.


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  		Table 3. Multivariate Analysis for Early Post-Transplant Outcomes in Bilateral Lung Transplantation
 
Validation Cohort-Donor Score and Early Survival
Seven recipients died within 30 days of transplantation. The donor scores of these recipients were 1 (n = 1, died of nonspecific graft failure), 3 (n = 1, died of fungal infection), 4 (n = 1, died of pulmonary embolism), 5 (n = 2, died of multisystem organ failure), 7 (n = 1, died of liver failure), and 10 (n = 1, died of infection). Donor score tended to be associated with 30-day mortality (R = 0.16, p = 0.07). In bilateral lung transplant, the donor score was significantly associated with one-year survival (R = 0.23, p = 0.02). In single lung transplant, there was no significant association between the donor score and one-year survival (R = 0.12, p = 0.48).


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
A standardized lung transplant donor scoring system is the only way that results between transplant centers can be compared while also establishing a solid platform for quality control purposes and specific research projects. In addition, it can be a useful adjunct for individual clinical decision making for donor selection, management, and evaluative analysis. The current study describes a proposed lung donor scoring system based on five clinical donor variables that are widely used in donor acceptability criteria [2–12]. These variables encompass factors that relate to background lung quality (age, smoking history), current clinical status (chest X-ray findings, amount of secretions), and overall lung performance (arterial blood gases). These five variables are routinely available at the time of donor referral and the score is simple to calculate. As might be expected, a higher donor score was seen in the donors who were medically unsuitable for transplantation compared with those donors where lungs were transplanted, or were not transplanted due to logistic or general exclusion criteria. Additionally, the donor score was significantly associated with early post-transplant outcomes in bilateral lung transplantation. The study therefore suggests, if applied prospectively, this scoring system may be useful in the selection of potential organ donors for lung transplantation and in the prediction of early post-transplant outcomes.

Regarding the primary outcome of the donor score, the single largest number of all donors used for transplantation in 2001 had a donor score of 0, with a decrease in the number of donors used decreased in inverse proportion to the donor score to a maximum of 7 or less (Fig 2). All the donors, except one in the general exclusion group who was potentially medically suitable for transplantation, had a lung donor score 7 or less. In contrast, 74% of the donors in the medically unsuitable lung exclusion group scored greater than 7 in this 2001 analysis. A lung donor score of 7 therefore seems to be a cutoff score that could aid in distinguishing donors medically unsuitable for transplantation (sensitivity = 74.2%, specificity = 98.4%). However, when considering our overall LTx experience between 2002 and 2005, there is an impression that some lungs may be useable beyond this arbitrary cutoff, even up to a score of 10. A larger prospective study is necessary for further validation and determination of acceptable cutoff scores that could actually distinguish unsuitable donors.

To validate the utility of the lung donor scoring system, multivariate regression analyses were performed. In bilateral lung transplantation, the donor score was significantly associated with early post-transplant outcomes even after adjustment of recipient and operative factors. In single lung transplantation, the association between the donor score and the early post-transplant outcomes was not significant. This difference between the types of transplant may be due to the influence of the native lung in single lung transplantation, as theoretically the donor score could predict only the performance of the one transplanted lung. Oto and colleagues [23] previously described the difference between the type of transplant in postoperative oxygenation, duration of intubation, and the prevalence of primary graft dysfunction grade after lung transplantation. Another possible explanation relates to the confounding effect of unilateral pathology in donor lungs. The donor score in this study was calculated for bilateral lungs and the individual donor score of each side was not available. Actually, in 4 of 87 used donors the contralateral lung was not used for transplant due to unilateral pathology. Blood gas analysis from donor pulmonary veins could potentially be used for unilateral donor scoring; however, this information is usually not available at the time of donor selection.

In the current study, the lack of correlation between the donor score and 30-day mortality is not surprising being consistent with the previous literature and the small number of early deaths that are analyzed. Previous reports have not been able to consistently link donor factors with an adverse effect on early or late post-transplant survival [2, 4, 5, 8–10, 14], even when comparing "ideal" and "extended" donors [11, 12, 14]. This does not mean donor factors are unimportant, but rather reflects the larger effect of other factors on post-transplant survival and the lack of statistical power in these studies. Consistent with this view, larger paired organ studies have been done in renal transplantation and suggest donor factors explain approximately 60% of the variable of early and 6-month graft function and may have an impact on long-term graft function [24, 25].

The possibility and relative importance of donor factors in predicting a variety of lung transplant outcomes has been considered in several previous studies. In a study of paired single lung transplants from the same donor, Sommers and colleagues [26] noted only relevance to donor variables in the first 24 hours with no relevant late sequel. By contrast, Snell and colleagues [27] reported a study of 38 paired single lung transplants that suggested no obvious relationship between donor variables and early functional outcomes, acute rejection, or bronchiolitis obliterans syndrome.

Taken together, it is likely that to assess and truly validate outcomes further from transplant than the first week, further development of a more sophisticated multivariate analysis is required. Ideally, this process will need to control for recipient and potentially intraoperative and postoperative variables, and will require a large number of subjects to circumvent the huge clinical variability in lung transplantation as it is currently practiced. As an example of just this strategy, Nyberg and colleagues [15] used statistical techniques based on mathematical modeling of a large number of potential predictor variables to select and score categories for a renal transplant donor scoring system [15]. The authors concluded that the donor scoring system based on the donor information available at the time of procurement could be used to estimate early graft function after renal transplantation.

In lung transplantation, Sekine and colleagues [14] assessed donor, recipient, and perioperative factors to identify risk factors for 30-day mortality and prolonged ICU stay. In univariate analysis a marginal donor was significantly associated with 30-day mortality or prolonged ICU stay; however, in multivariate analysis, the association did not reach statistical significance. Therefore, donor factors were not considered further in their scoring system. The authors therefore concluded that a scoring system based entirely on recipient and perioperative factors could be used to predict early outcomes.

In conclusion, a proposed simple donor scoring system based on five major donor variables, all of which are available at the time of donor selection was significantly and independently associated with early post-transplant outcomes even after adjustment of recipient and operative factors. The donor score may have a useful role to play for data comparison among specific centers, quality control, evaluative research, and clinical decision making in donor selection and management in lung transplantation. A larger prospective study is necessary for further validation and extension of this proposed donor scoring system.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Snell GI, Griffiths A, Macfarlane L, et al. Maximizing thoracic organ transplant opportunities: the importance of efficient coordination J Heart Lung Transplant 2000;19:401-407.[Medline]
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  7. Pierre AF, Sekine Y, Hutcheon MA, Waddell TK, Keshavjee SH. Marginal donor lungs: a reassessment J Thorac Cardiovasc Surg 2002;123:421-428.[Abstract/Free Full Text]
  8. Oto T, Griffiths A, Levvey B, et al. Donor history of asthma is not a contraindication to lung transplantation: 12-year single center experience J Heart Lung Transplant 2004;23:309-316.[Medline]
  9. Oto T, Griffiths AP, Levvey B, et al. A donor history of smoking affects early but not late outcome from lung transplantation Transplantation 2004;78:599-606.[Medline]
  10. Sundaresan S, Semenkovich J, Ochoa L, et al. Successful outcome of lung transplantation is not compromised by the use of marginal donor lungs J Thorac Cardiovasc Surg 1995;109:1075-1079.[Abstract/Free Full Text]
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  14. Sekine Y, Waddell TK, Matte-Martyn A, et al. Risk quantification of early outcome after lung transplantation: donor, recipient, operative, and post-transplant parameters J Heart Lung Transplant 2004;23:96-104.[Medline]
  15. Nyberg SL, Matas AJ, Rogers M, et al. Donor scoring system for cadaveric renal transplantation Am J Transplant 2001;1:162-170.[Medline]
  16. Oto T, Levvey B, Pilcher DV, Bailey MJ, Snell GI. Evaluation of the oxygenation ratio in the definition of early graft dysfunction post lung transplantation J Thorac Cardiovasc Surg 2005;130:180-186.[Abstract/Free Full Text]
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  18. Christie JD, Carby M, Bag R, Corris P, Hertz M, Well D. Report of the ISHLT working group on primary lung graft dysfunctionPart II: definition. A consensus statement of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 2005;24:1454-1459.[Medline]
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  21. Oto T, Griffiths AP, Rosenfeldt F, Levvey BJ, Williams TJ, Snell GI. Early outcomes comparing Perfadex, Euro-Collins and Papworth solutions in lung transplantation Ann Thorac Surg 2006;82:1842-1848.[Abstract/Free Full Text]
  22. Oto T, Rabinov M, Griffiths AP, et al. Unexpected donor pulmonary embolism affects early outcomes after lung transplantation: a major mechanism of primary graft failure? J Thorac Cardiovasc Surg 2005;130:1446-1452.[Abstract/Free Full Text]
  23. Oto T, Griffiths AP, Levvey BJ, Pilcher DV, Williams TJ, Snell GI. Definitions of primary graft dysfunction after lung transplantation: differences between bilateral and single lung transplantation J Thorac Cardiovasc Surg 2006;132:140-147.[Abstract/Free Full Text]
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