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J Thorac Cardiovasc Surg 1995;109:1075-1080
© 1995 Mosby, Inc.
CARDIAC AND PULMONARY REPLACEMENT |
St. Louis, Mo.
From the Division of Cardiothoracic Surgery, Department of Surgery,a Mallinckrodt Institute of Radiology,b and Respiratory andCritical Care Division, Department of Medicine,c WashingtonUniversity School of Medicine, Barnes Hospital, St. Louis, Mo.
Address for reprints: Sudhir Sundaresan, MD, Division of CardiothoracicSurgery, Suite 3107 Queeny Tower, One Barnes Hospital Plaza, St. Louis, MO63110.
Abstract
Lung transplantation is limited by a shortage ofsuitable donors. To address this shortage, we have begun using donor lungsthat do not meet all of our previous rigorous donor criteria. Of 133 consecutivelung transplants done between June 1991 and March 1994, 89 donors were consideredideal because they satisfied all of the following accepted donor criteria(group I): age younger than 55 years, smoking less than 20 pack-years, arterialoxygen tension greater than 300 mm Hg (using inspired oxygen fraction of 1.0and positive end-expiratory pressure 5 cm H2O), and chest radiographnegative for infiltrate or trauma (contusion or pneumothorax). Thirty-sevendonors failed to satisfy one of these criteria and seven donors failed tosatisfy two of them, yielding 51 criteria denoting marginal status in the44 donors in the marginal group (group II) as follows: age older than 55 years,2; smoking history 20 or more pack-years, 9; unsatisfactory chest radiograph,34; and arterial oxygen tension less than 300 mm Hg, 6. Sixty-three singlelung transplants were done (group I, 44 versus group II, 19) compared with70 bilateral sequential transplants (group I, 45 versus group II, 25). In24 cases in group II, at least one of the lungs actually being implanted containedcontusion or infiltrate. Evaluation of recipients from the two groups showedno significant difference in median duration of postoperative mechanical ventilation(3 days in both group I and group II) nor in alveolar-arterial oxygen gradientimmediately after transplantation (group I, 304 ± 14 mm Hg versus groupII, 275 ± 22 mm Hg; p = 0.266) or at24 hours (group I, 125 ± 12 mm Hg versus group II, 122 ± 18mm Hg; p = 0.933) (all values represent meanplus or minus the standard error). However, cardiopulmonary bypass was requiredto facilitate second graft insertion in bilateral sequential transplants moreoften in the marginal group (5 of 25, 20%) than in group I (6 of 45, 13%).There were three deaths within 30 days in group I (operative mortality, 3.4%)and none in group II. Currently, 74 (83.2%) of 89 remain alive in group Icompared with 38 (86.4%) of 44 in group II. On the basis of these data, weconclude that successful outcome of lung transplantation can be achieved withthe use of marginal donor lungs. (J THORACCARDIOVASC SURG1995;109:1075-80)
The exponential increase in the number of lung transplants being done 
1 has not been accompanied by a correspondingincrease in the number of donors. Currently still only about 15% to 20% ofmultiple organ donors have lungs suitable for transplantation. 2 This donor shortage remains the main limitation tomore widespread use of lung transplantation. The scarcity of suitable donorlungs arose in part from rigid application of strict donor criteria. 3-5 These criteria have evolved somewhat with experience. However, theever-increasing number of recipients has compelled us to consider the useof "marginal" donor lungs (i.e., donor lungs that fail to meet one or moreof the previous rigorous criteria). We report here our satisfactory resultswith the use of marginal donor lungs during a 2 1/2-year period and presentguidelines that have evolved regarding this approach as a means of addressingthe donor shortage.
METHODS
A total of 133 consecutive lung transplants done at our institutionbetween June 1991 and March 1994 were retrospectively analyzed and form thebasis of this report. Donors used for these transplants were placed into oneof two categories on the basis of several of our previously published donorassessment criteria listed in Table I 5 ; donors satisfying all of the accepted criteria wereplaced in group I ("ideal" donor group), whereas those failing to meet atleast one of the criteria were placed in group II ("marginal" donor group).
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Donor arterial oxygen tension (Pao2) was determined duringventilation at an inspired oxygen fraction of 10 and positive end-expiratorypressure of 5 cm H2O. Donor organs were judged of marginal qualitywhen, at these settings, Pao2 was less than 300 mm Hg.
Donors older than 55 years or having a confirmed smoking history greaterthan 20 pack-years were also judged marginal.
Parameters used to evaluate early recipient outcome included the alveolar-arterialoxygen difference (a-aDo2) immediately on return to the intensivecare unit after transplantation and also at 24 hours after operation, numberof days of mechanical ventilation required, and death occurring within 30days of the transplantation. The percentage of patients currently alive ineach group was used as a parameter of late outcome. Statistical comparisonof values between the groups was done with the unpaired t test or the Fisher exact test. Values were considered significantlydifferent when p was less than 0.05.
RESULTS
Comparison of group I (ideal donors) versus group II (marginal donors)
There were 89 donors in group I and 44 in group II (see TableII). Thirty-seven of 44 group II donors were deemed marginalon the basis of failure to satisfy only one of the listed criteria, whereas7 of 44 failed to satisfy two of these criteria. As previously stated, designationof marginal status on the basis of chest radiograph was made when unsatisfactoryradiographic findings (infiltrate, contusion, pneumothorax, or a combinationof these conditions) were present in either lung (even in proposed SLTs whenthe radiographic changes were confined to the contralateral lung). Among the34 donors in group II deemed marginal on the basis of these unsatisfactoryradiographic findings, the lung or lungs actually being implanted containedcontusion or infiltrate in 24 of the 34 cases.
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Table III compares several clinical variables betweenthe donors of the two groups. Mean donor age and duration of donor mechanicalventilation did not differ between the groups. The major causes of death inthe two groups varied somewhat, with a greater frequency of blunt trauma andassociated closed head injury in group II. Of note, clinically evident chesttrauma (in addition to the documented radiographic changes ensuing from trauma,used as a criterion of marginal status in 
Table II),such as chest wall abrasions, thoracic stab or gunshot wounds, and chest tubesinserted for other indications, were far more prevalent in the marginal group(see Table III).
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Early recipient outcome
Table IV shows that there was no significant differencein recipient outcome between the groups with respect to A-aDo2(either immediately or at 24 hours after operation),median duration of mechanical ventilation, or 30-day operative mortality.
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Table IV shows that 74 (83.2%) of 89 group I recipientsare currently alive compared with 38 (86.4%) of 44 group II recipients (p = 0.802).
Influence of donor Pao2 on subsequent outcome
We focused on the subgroup of marginal donors with Pao2 valuesless than 300 mm Hg (comparing their recipient outcomes with those havingmarginal donors with Pao2 values greater than 300 mm Hg and withthose recipients of ideal donor lungs) to evaluate the impact of this particulartransgression of the rigorous donor criteria on subsequent recipient outcome. Fig. 1, which shows the A-aDo2 (immediately andat 24 hours after operation), shows no significant difference among thesethree subgroups at either time point.
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This retrospective study has demonstrated that satisfactory outcomeof lung transplantation can be achieved with the use of lungs from marginaldonors. None of the parameters used in this study to evaluate early and laterecipient outcome showed any significant difference between the groups. Therewere, however, discernible differences between the two groups. First, cardiopulmonarybypass appeared to be necessary to facilitate second graft implantation inBSLT more often in the marginal donor group than in the ideal donor group,although the difference between groups did not achieve statistical significance.The need for bypass was invariably based on unsatisfactory oxygenation orhemodynamics, or both (i.e., unacceptably elevated pulmonary artery pressure)after pulmonary artery clamping during excision of the second native lung.Second, our subjective impression is that the early postoperative recipientchest radiographs in the marginal donor group often demonstrated worseningof any preexisting infiltrate or contusion before resolution of these changes,which was usually discernible within about 72 hours. These findings are allcompatible with a tolerable degree of reversible donor lung dysfunction, manifestedmainly as reperfusion-related pulmonary edema. Nonetheless, these phenomenaobserved in the marginal donor group did not have any effect on the objectiveparameters used in this study and hence did not have an adverse impact onthe early or late results for those recipients.
Puskas and associates 4have previously reported on the utility of unilateral lung assessment in theevaluation of donors with unilateral infiltrates and unsatisfactory gas exchange.That report emphasized that assessment of the unilateral donor lung did notalter the strict criteria applied to potential lung grafts, but rather verifiedthat the lung under scrutiny did satisfy these criteria even if the contralaterallung had been damaged by aspiration or trauma. It was demonstrated that successfulSLT could be achieved under such circumstances and that this might be a usefulstrategy to increase the availability of single lung grafts from otherwiseunsuitable donors. 4 In ourstudy, six of the marginal donors had a Pao2 value less than 300mm Hg. We did not do unilateral lung assessments (as described by Puskas andassociates 4 ); thus we couldnot determine whether the reason for the poor donor oxygenation was due toa problem in the transplanted (ipsilateral) or contralateral lung. However,our study does represent an extension of that strategy for expanding the donorlung pool, in that greater clinical experience and careful judgment have permittedus, in selected circumstances, to relax the necessarily strict criteria normallyapplied to potential lung grafts and yet still achieve satisfactory results.Our data support this concept, in that there was no significant differencein recipient a-aDo2 values for ideal donors, marginal donors withPao2 values less than 300 mm Hg, and marginal donors with Pao2 values greater than 300 mm Hg, either immediately after transplantationor 24 hours later.
Clearly proper judgment is the critical factor in determining what degreeof donor lung dysfunction is tolerable and in what circumstances this approachis acceptable. We continue to believe that the donor bronchoscopic examinationis of paramount importance and that the findings of copious purulent secretionsor evidence of aspiration (foreign matter, tracheobronchitis) represent strongcontraindications to the use of that lung. As we have stated previously, 5 the presence of a chest tube (fortreatment of iatrogenic pneumothorax as a result of central venous line insertion)or mild contusions or infiltrates are all of some concern, but such casesoften yield quite acceptable grafts. Similarly, donor hypoxemia related tofluid overload or simple mucus plugging can usually be resolved by diuresisand bronchoscopy, respectively, again providing satisfactory lung grafts.We are increasingly in favor of implementing early antibiotic therapy (consistingof intravenous vancomycin and ceftazidime) in marginal donors with pulmonaryinfiltrates or contusions before commencement of the multiple-organ retrieval.
Ultimately, the use of a marginal donor lung is dictated by the recipient'sunderlying disease and anticipated procedure, as well as the aforementionedconsiderations. For bilateral lung transplants, a mild contusion or infiltratein one lung may be acceptable. As long as the recipient does not have anyprofound inequalities in distribution of ventilation or perfusion, then itmay be preferable to implant the more "normal" lung first to minimize therequirement for cardiopulmonary bypass during implantation of the marginalgraft. Similarly, some degree of reversible lung dysfunction is usually tolerablein SLT for emphysema, in which the native lung can oxygenate satisfactorilyuntil the graft recovers. The duration of graft ischemia (generally confinedto less than 8 hours) also has an impact on graft quality, and in the aforementionedsituations we have occasionally extended the ischemic interval beyond 10 hourswith satisfactory results. Under no circumstances, however, do we compromisedonor lung quality in SLT for primary pulmonary hypertension, in which thegraft will receive essentially all of the postoperative perfusion immediately.In these cases, the chest radiograph must be clear on the side of the proposedharvest; gas exchange, bronchoscopy, and size match must all meet the establishedcriteria perfectly; and graft ischemic time is limited to 6 hours or less.With careful consideration of all these matters, it appears that the use ofmarginal donor lungs represents a safe method of enlarging the potential donorlung pool and does not compromise the subsequent early or late recipient outcome.
We gratefully acknowledge the help of Richard B Schuessler, PhD, inperforming the statistical analysis.
Appendix: DISCUSSION
Dr. Joseph LoCicero (Boston, Mass.). This is an important preliminary report that is necessitated by the fact that our record of recovering lungs from cadaver donors is abysmal. The 1992 statistics that were given show that about 20% of all donors have contributed lungs. In fact, the preliminary data for 1993 are considerably worse.
Donors have three opportunities to have lung injury: first is the initial trauma that they receive; second is the additional lung injury from the resuscitation period or the time during donor preparation; and third is the obligatory ischemia/reperfusion injury that all lungs must go through before transplantation. In addition, the authors have pointed out that there can also be underlying chronic preexisting lung damage, such as a heavy smoking history or possibly advanced age of the donor. Advanced age may lead to a statistically significant difference in outcome.
The measures of function used in this study both before and after operation are fairly crude but can supply some information about whether these lungs may have preexisting injuries. In addition to the a-aDo2 and Pao2 values, pulmonary mechanics can also be measured. Have you had any opportunity to measure pulmonary mechanics in donors before harvest? If so, has that provided any information about the eventual outcome? Second, do you know of any other objective measures besides these fairly crude measures of function? Have any biopsy samples been taken from these lungs? Is there any information on shed antigens in the donor plasma that we could use to begin to get some handle on whether these lungs have a significant injury? Finally, how bad can a donor organ be and still be acceptable for transplantation? What about multiple problems in the marginal donor? Would it be acceptable to use a 62-year-old heavy smoking donor with blunt trauma to the chest whose chest x-ray film shows bilateral infiltrates, with a Pao2 of 200 mm Hg on 100% oxygen and white blood cells on bronchoscopy, but no bacteria?
Dr. Sundaresan. Concerning the first question related to evaluation of pulmonary mechanics before harvest of the donor, we can get a subjective impression about the pulmonary mechanics from airway pressures during mechanical ventilation. Other than that we have not pursued more sophisticated ways of evaluating that issue.
The second question had to do with other objective ways of measuring the possibility of underlying or perhaps unappreciated lung injury in the donor lungs, for example, the use of biopsies. Again, we have not used such methods on a regular basis. We have in the past done biopsy studies of donor lungs during a multiple organ retrieval when some clinical finding suggested that there might be a serious problem, such as diffuse granulomatous infection. In fact, we have managed to avoid using what we would consider unacceptable lungs through the use of frozen section when that was available. In terms of evaluating the grafts after transplantation, of course these recipients are subjected to regular follow-up bronchoscopic examination, but I do not think that exactly relates to your question.
The final question had to do with how bad a donor lung can be before it is turned down. There are two issues that have to do with when a marginal lung can be used. One issue concerns factors related to evaluation of the lungs, such as the x-ray films, the blood gas values, and bronchoscopic examination. The other issue concerns the recipient's disease and the procedure planned. The 62-year-old smoker in the example given, with blunt trauma and bilateral contusions, might not be acceptable for any recipient except one who was moribund. Ultimately it is a judgment call related to the patient, the underlying disease, and whether the patient will receive a single or bilateral lung transplant.
Dr. Thomas M. Egan (Chapel Hill, N.C.). If I understand the data correctly, a large number of the marginal donors were marginal on the basis of an abnormal radiographic finding. The issue for those of us retrieving lungs is how to tell whether that abnormality is an abnormality caused by infection versus an abnormality caused by something else.
An interesting study was published 3 years ago that looked at the incidence of pneumonia in survivors of closed head injury who required intubation (Hsieh AH-H, Bishop MJ, Kublis PS, Newell DW, Pierson DJ Pneumonia following closed head injury. Am Rev Respir Dis 1992;146:290-4). These authors determined that 40% of patients who required intubation because of a closed head injury ultimately had pneumonia at some time during the first week of hospitalization. Our problem is that we come on the scene on day 2 or day 3 after the injury and are trying to determine whether the lung from this head-injured patient will result in pneumonia 2 days later in our recipient.
Do you have any guidance for us in terms of how to tell whether the abnormality that we are seeing on chest x-ray films is infectious versus an area of contusion versus an area of interstitial pulmonary edema? Have you used lungs that had an infectious area that appeared to be localized to either one segment or one lobe that could then be resected?
Dr. Sundaresan. Your first question concerned the differentiation of infection versus contusion when there is an abnormality on the chest radiograph. I think that the limited history obtained on the donor and the knowledge of the clinical circumstances are probably the most useful things in determining whether there has been a traumatic contusion or an infectious or inflammatory problem in the lung. The bronchoscopic examination might also be useful, because purulent secretions on the side of the radiographic abnormality might correlate more closely with a septic problem.
Dr. Egan. Have you ever resected an area that you thought by palpation was infected?
Dr. Sundaresan. I am not aware that that has been done in this series of patients or, in fact, at all in our experience. We have encountered some lungs that had substantial injuries or inflammatory problems, but our subjective impression is that when left alone they tend to clear up quite rapidly.
Footnotes
Read at the Seventy-fourth Annual Meeting of The
American Association for Thoracic Surgery, New York, N.Y., April 24-27, 1994. 
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