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Ann Thorac Surg 2002;73:1599-1604
© 2002 The Society of Thoracic Surgeons

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Original article: general thoracic

Pulmonary vein gas analysis for assessing donor lung function

^a Transplant Unit, Wythenshawe Hospital, Manchester, United Kingdom

Accepted for publication January 4, 2002.

* Address reprint requests to Mr Aziz, Cardiac Transplant Unit, Freeman Hospital, Freeman Road, High Heaton, Newcastle-upon-Tyne, NE 7 7DN United Kingdom
e-mail: tarekaziz55{at}hotmail.com

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Radial artery oxygenation (PaO₂) is the standard method for assessing potential lung donors. This study was proposed to assess the use of pulmonary vein gases (PvO₂) in selection of donor lung for transplantation.

Methods. We studied 170 lungs from 85 consecutive donors. Lungs were classified into group A, PaO₂ and PvO₂ > 300 mm Hg; group B, PaO₂ < 300 mm Hg, and PvO₂ > 300 mm Hg; and group C, PvO₂ < 300 mm Hg.

Results. Lungs retrieved from group A and group B were used for transplantation. Allograft function, assessed by the arterial and alveolar oxygen tension ratio, was similar at 12 hours and at 24 hours after operation (0.69, 0.73, vs 0.70, 0.71, for groups A and B, respectively (p = 0.8, 0.7, respectively). Similar radiologic appearance was seen in both groups (p = 0.2). Median duration of intubation was also similar (p = 0.6). The 30-day mortality rate was 12% versus 11.3% (p = 0.8), and 1-year survival rate was 80% versus 82% (p = 0.8) for recipient received lungs from group A and B donors, respectively.

Conclusions. Selective pulmonary veins analysis gives an accurate assessment of individual gas exchange in comparison with arterial PaO₂, identifying more potential donor lungs for transplantation.

	Introduction

Top Abstract Introduction Material and methods Results Comment References

 
Lung transplantation is a life saving therapy for selected patients with end-stage lung disease, but its application is severely constrained by the small number of suitable donors. The measurement of partial pressure of oxygen and carbon dioxide in peripheral arterial blood is the standard method for the assessment of donor lung gas exchange before lung transplantation [1, 2]. The criteria of arterial oxygen tension (PaO₂) of more than 300 mm Hg on an inspired oxygen fraction (FiO₂) of 100% is traditionally accepted as reflecting suitable donor lung function. A low PaO₂ generally excludes pulmonary donation regardless of the other function parameters of each individual lung [1–4]. Various pathophysiologic mechanisms (hemodynamic status, high cardiac output, and vascular resistance) affect the PaO₂ of peripheral arterial blood gas independent of individual lung function. A unilateral radiologic abnormality is also often considered to be an exclusion criterion for donating that isolated lung.

We have previously reported our preliminary findings that both pulmonary and nonpulmonary pathophysiologic mechanisms can affect the peripheral arterial PaO₂ [5]. In this study we suggested that direct sample measuring of oxygen partial pressure (PvO₂) from the pulmonary veins gives more accurate assessment of individual lung gas exchange when compared with peripheral arterial PaO₂. We have shown that pulmonary vein gas may allow the use of isolated lung donation, which normally would be considered unsuitable.

The purpose of this study was to investigate the possible role of pulmonary vein gas analysis in assessment and selection of donor lungs for transplantation.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Study population
This study was prospectively conducted and involved all donors who were considered for lung donation by Wythenshawe Hospital between August 1995 and August 1999. Lung re-transplantation (n = 2 recipients) and heart lung transplantation recipients (n = 6 recipients) were excluded from this study. Follow-up at our center was completed by September 2000 or by the time of recipient death. Data for recipients who underwent lung transplantation at other transplant centers were collected after operation.

Donor selection
In conformity with other United Kingdom transplant centers, donor selection criteria at our center was liberalized to attract a larger donor pool. It has already been demonstrated that marginal heart and lung donors can be optimized with careful intensive care management and successfully used for selected recipients. The criteria for selection of lung donors are widely established [6] and approved by the United Kingdom Transplant Support Service Authority (Table 1).

Intraoperative assessment
Donor oxygen tension was determined during mechanical ventilation at an inspired oxygen fraction of 1.0 and positive end expiratory pressure of 5 cm H₂O. Each lung was examined separately to exclude any focal pulmonary lesion, consolidation, or basal collapse. Samples from the pulmonary veins were taken starting from the left upper vein, then left lower vein, right lower vein, and right upper vein. Left-sided pulmonary vein gases were performed by sampling the left upper and left lower pulmonary veins through the pericardial cavity, whereas the right side veins were approached through the right pleural cavity. Both pulmonary vein gas (PvO₂) and peripheral arterial gas (PaO₂) were performed simultaneously. Fibro-optic bronchoscopy was used to assess the bronchial tree in marginal donors (n = 9 donors). Intraoperative exclusion criteria included extensive pleural adhesion, moderate and severe emphysematous lung changes, congested or edematous lungs, focal pulmonary lesion(s), and infection proven by bronchoscopic assessment.

Pulmonary preservation was carried out using antegrade perfusion of Euro-Collins (Fresnius, AG, Hamburg, Germany) solution (60 mL/kg) at infusion pressure of 10 to 15 cm H₂O at a temperature of 4°C. The retrieved lungs were kept inflated at 25% to 75% of the maximum lung capacity. Ischemic time was defined as the interval from donor cross clamping to reperfusion and was recorded for each lung. Intraoperative and postoperative hemodynamic data were obtained with an indwelling pulmonary artery catheter.

Standard previously described techniques were used for single and double lung transplantation. Recipients underwent standard pulmonary function testing before transplantation, and determination of left and right ventricular ejection fractions were made by noninvasive examination.

Assessment of allograft function
Donor lungs were classified into 3 groups:

1. group A (n = 67 lungs) with PvO₂ more than 300 mm Hg and radial artery PaO₂ more than 300 mm Hg;
   

2. group B (n = 42 lungs) with radial PaO₂ less than 300 mm Hg and PvO₂ more than 300 mm Hg; and

3. group C (n = 43 single lungs from 43 donors plus 18 lungs from 9 donors) with PvO₂ less than 300 mm Hg.

Lungs retrieved from only groups A and B have been used for transplantation. Chest roentgenograms were obtained at zero and then every 24 hours after the operation. A semiquantitative scale was used to assess the degree of pulmonary allograft injury, with scoring as follows: 0 = no abnormal findings; 1 = perihilar infiltrate; 2 = infiltrate localized to a limited lung field; 3 = diffuse moderate interstitial and alveolar infiltrate; 4 = diffuse severe interstitial and alveolar infiltrate. Each lung was graded independently, and a mean score was calculated.

Arterial blood gases were obtained at multiple intervals after transplantation and used to calculate the arterial and alveolar oxygen tension ratio and the PaO₂/FiO₂ ratio. The alveolar oxygen tension (PAO₂) was calculated as follows: PAO₂ = (760 - PH₂O) FiO₂ - 1.25 PaCO₂, where PH₂O is the water vapor partial pressure assumed to be 47 mm Hg at 37°C, FiO₂ is the inspired fraction of oxygen, and PaCO₂ is the arterial partial pressure of carbon dioxide.

The diagnosis of diffuse alveolar damage was based on histology from transbronchial biopsy or autopsy specimens stained by hematoxylin and eosin. Diffuse alveolar damage was always diagnosed in the early exudative phase by microscopic appearance of necrosis of both alveolar membrane and alveolar endothelium and pulmonary capillary microthrombosis. Time of intubation, length of intensive care unit stay, and patient survival at 30 days and 1 year after transplantation were recorded.

Single lungs that were not accepted on the basis of inadequate pulmonary vein gas testing (group C [n = 43], lungs retrieved from 43 donors) were perfused in the same way and underwent a complete histopathologic and microbiologic examination at Wythenshawe Hospital.

Statistical analysis
Statistical computations were carried out using SPSS software (Windows 7.5; SPSS, Inc, Chicago, IL). Results are expressed as mean ± standard deviation. Comparisons between patient characteristics mean allograft ischemic times, perioperative blood transfusion requirements, arterial and alveolar oxygen tension ratios, and PaO₂ and FiO₂ ratios in the two groups were carried out using the unpaired t test.

Comparison of mean chest roentgenogram scores and death were calculated with the ² likelihood ratio. The Kruskal-Wallis rank sum test was applied to assess duration of intubation and length of intensive care unit stay. Survival was assessed using the Kaplan-Meier method and compared by log-rank test. A p value of less than 0.05 was defined as statistically significant.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Donor population
Between August 1995 and August 1999, 115 donors were offered to our center for lung donation consideration Twenty-seven donor offers were excluded at the initial stage because of aspiration and proven chest infection history (n = 18 donors), pulmonary edema (n = 10 donors), or chest injury (n = 2 donors). The remaining donor offers (n = 85 donors) were inspected by our donor retrieval team. One hundred and nine lungs were considered suitable for transplantation. Bilateral lungs were retrieved from 33 donors, 43 single lungs were retrieved from 43 donors, whereas both lungs (n = 18 lungs) were considered unsuitable in 9 donors.

After operative assessment, pulmonary vein samples from the suitable lungs (n = 109) showed PvO₂ of more than 300 mm Hg (329–587; mean, 444.65 mm Hg); sixty-seven of these lungs (group A) gave a radial PaO₂ of more than 300 mm Hg (202.2–279; mean, 232 mm Hg). The remaining 42 lungs (group B) gave a radial blood PaO₂ of more than 300 mm Hg (307.6–422.3; mean, 362.7 mm Hg).

Recipient and donor characteristics
Comparisons of recipient and donor-related characteristics between group A and group B are detailed in Table 2. There were no significant differences in donors or recipients demographs. All cystic fibrosis patients received double lung transplantation. For chronic obstructive airway disease, 2 patients from group A and 4 patients from group B (1 from cryptogenic fibrosing alveolitis group) received double lung transplantation. The remaining recipients from both groups received single lung transplantation.

View larger version (11K): [in this window] [in a new window]   Fig 1. Chest roentgenogram (CXR) scores at 0, 24, and 72 hours after transplantation. Group A = PvO2 > 300 mm Hg; PaO2 < 300 mm Hg. Group B = PvO2; PaO2 > 300 mm Hg.

View larger version (11K): [in this window] [in a new window]   Fig 2. PO2/FiO2 ratio for both groups at 1, 12, 24, and 48 hours after operation. Group A = PvO2; PaO2 > 300 mm Hg. Group B = PvO2 > 300 mm Hg, PaO2 < 300 mm Hg.

Postoperative stay and survival
Median duration of intubation was also similar in both groups (2.3 days in group A compared with 2.1 days in group B; p = 0.6) (Fig 3).

View larger version (12K): [in this window] [in a new window]   Fig 3. Average intubation time in both groups. Group A = PvO2; PaO2 > 300 mm Hg. Group B = PvO2 > 300 mm Hg, PaO2 < 300 mm Hg.

The 30-day mortality rate was 3 of 25 (12%) in group A patients and 5 of 44 (11.3%) in group B patients. This difference did not reach statistical significance (p = 0.80). Survival at 1 year was nearly identical in the two groups: 80% and 82% in group A and B, respectively (p = 0.8). Causes of death are summarized in Table 3.

View larger version (33K): [in this window] [in a new window]   Fig 4. Procurement rate (efficiency percent) of donor lungs from total number of lungs offered for donation before and after adoption of pulmonary vein gas sampling technique. UK before 1995 = percent in the UK before 1995 (study beginning); Wyn before 1995 = percent at Wythenshawe Hospital before 1995 (study beginning); UK after 1995 = percent in the UK after 1995 (study period); Wyn after 1995 = percent at Wythenshawe Hospital after 1995 (study period). (UK = United Kingdom; Wyn = Wythenshawe Hospital.)

	Comment

Top Abstract Introduction Material and methods Results Comment References

Gas exchange remained one of the most important "gold standards" in assessing lung function for possible donation [1–4]. Given that graft and patient 1-year survival rates for recipients of lung transplants are still lower than those for any other transplanted solid organ, it is not surprising that lung transplant surgeons are often reluctant to implant lungs with less than favorable gas exchange characteristics. The standard criteria in most lung transplantation programs for considering potential lungs to be suitable for donation are adequate arterial oxygenation with peripheral arterial blood oxygenation of PaO₂ more than 300 mm Hg on inspired oxygen fraction (FiO₂) of 100% [1–4].

Our experience from this study suggests that peripheral arterial blood gas may not reflect the accurate status of each lung oxygenation. Various pathophysiologic mechanisms affect the PaO₂ of peripheral arterial blood gases independent of individual lung function [11–14]. Brain stem death is associated with raised intracranial pressure leading to impaired brain stem perfusion. Medullary ischemia results in intense sympathetic nervous system activation. This, in turn, results in transient, mostly pre-capillary pulmonary artery pressure elevation and lung edema formation due to increased capillary permeability. A various degree of ventilation perfusion is mismatched with predominance of shunt flow. The degree of shunt flow affects the individual lung oxygenation and the peripheral arterial oxygen level in different ways [11–14].

Peripheral arterial gas analysis does not also consider the possibility of isolated single lungs that may be suitable for donation. Puskas and associates [15] from Toronto described their technique of limited experience in unilateral donor lung assessment. This included exclusion of each lung separately from ventilation by the double-lumen endotracheal tube and vascular clamp occluding the pulmonary artery. In an attempt to assess the individual lung gas exchange, other centers have adopted unilateral pulmonary artery clamping and radial artery sampling techniques. Although such techniques allow adequate assessment of each lung separately, it may be difficult to apply in routine clinical practice of lung procurement because it requires adequate experience in double lumen intubation and ventilation, which may not be available in every donor hospital. Unilateral pulmonary artery clamping may compromise the hemodynamic stability of borderline donors. Pulmonary vein gas sampling would be technically easier to perform in such donors and would provide more accurate assessment for each lung lobe during pulmonary procurement.

Unfortunately, less than 20% of other solid organ donors are deemed suitable for lung donation [16]. The overall lung procurement efficiency rate is still less than 20% for most of the United States lung transplant centers [9] and between 30% to 43% for most of the United Kingdom lung transplant centers [10, 17]. During the period of this study we have increased the procurement rate for lung retrieval to an average of 63% to 65% of our multiple organ donors whose lungs have been retrieved and successfully used for transplantation. This basically reflects the impact of adopting the pulmonary vein gas sampling technique for identifying additional suitable donor lungs for transplantation.

In view of our initial results of this study, other general measures have also been introduced to our lung retrieval policy. Gradually, our surgical team has built its confidence in dealing with borderline lung offers, and we strongly recommend the pulmonary vein gas sampling technique at both the local and national levels. Lung donors have been considered for retrieval provided there was no history of aspiration or asthma and both operative assessment and pulmonary vein gas analyses were satisfactory. Assessment of donor roentgenogram appearances was only performed by our retrieval team and reviewed in line of the operative assessment and pulmonary vein gas sampling. Our operative and 1-year survival results were not affected by the introduction of the pulmonary vein gas sampling technique or other measurement to improve our procurement rate.

Limitations
The first limitation of this study is there was no clear correlation between the level of donor oxygenation and subsequent lung allograft function. From a clinical point, such correlation would be very difficult to investigate because the early graft function is affected by various factors related to both donor and recipient criteria and procedures. Previous studies have demonstrated that the level of donor oxygenation remained a clinically reliable tool in the decision-making of lung suitability for donation [1–4].

Second, comparing the oxygenation results of recipients in groups A and B, we did not analyze the level of recipients oxygenation according to the procedure they have had (single vs bilateral lung transplantation). In single lung transplant recipients for emphysema, the native lung did not contribute to the oxygenation because they all underwent selective transplanted lung ventilation through a double lumen intubation [18]. However, we have previously reported in cryptogenic fibrosing alveolitis recipients that the major right cardiac output is diverted to the more compliant transplanted lung minimizing the contribution of the native lungs to the recipient level of oxygenation [19]. In both groups of single lung transplant recipients, the level of oxygenation was a reflection of the transplanted lung performance.

In conclusion, despite these limitations, our study demonstrated that measurement of pulmonary vein gas in each individual pulmonary vein may therefore increase the rate of donor acceptance in comparison with the standard peripheral arterial gas sampling technique. Pulmonary vein gas sampling is easy to perform and it does provide an accurate assessment of each lung lobe gas during pulmonary procurement. Pulmonary vein gas also identifies suitable isolated lung donation, which normally may be considered unsuitable.

In the presence of an ever-increasing demand for lung transplantation and a limited donor pool, it will become increasingly important to identify the scrutiny and review criteria in which donor lungs are considered acceptable for donation. This will allow us to identify factors that preclude the use of some donor lungs, or ideally identify adverse factors that can be remedied to increase the potential for a satisfactory clinical outcome.

	References

Top Abstract Introduction Material and methods Results Comment References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Tarek M. Aziz Rasheed A.G. Saad Marcello Migliore Colin S. Campbell Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Aziz, T. M. Articles by Yonan, N. A. Search for Related Content PubMed PubMed Citation Articles by Aziz, T. M. Articles by Yonan, N. A. Related Collections Lung - transplantation Related Article