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Eur J Cardiothorac Surg 2001;19:326-332
© 2001 Elsevier Science NL

Bronchial artery perfusion during cardiopulmonary bypass does not prevent ischemia of the lung in piglets: assessment of bronchial artery blood flow with fluorescent microspheres

Christian Schlensaka, Torsten Doensta, Stefan Preußera, Mark Wunderlicha, Manuela Kleinschmidtb, Friedhelm Beyersdorfa

a Department of Cardiovascular Surgery, University of Freiburg, Hugstetter Strasse 55, D-79106, Freiburg, Germany
b Department of Pathology, University of Freiburg, Hugstetter Strasse 55, D-79106, Freiburg, Germany

Received 15 December 1999; received in revised form 1 December 2000; accepted 30 December 2000.

Corresponding author. Tel.: +49-761-270-2818; fax: +49-761-270-2550
e-mail: schlensa{at}ch11.ukl.uni-freiburg.de


   Abstract
Top
 Abstract
1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Objective: Blood supply of the lungs during total cardiopulmonary bypass (CPB) is limited to flow through the bronchial arteries. This study was undertaken to assess the bronchial artery blood flow during CPB with fluorescent microspheres in a piglet model. Methods: We subjected ten piglets (mean weight 5.0±0.5 kg) to 120 min of normothermic, total CPB without aortic cross-clamping, followed by 60 min of post-bypass perfusion. Fluorescent microspheres were injected into the left atrium or the aortic cannula or distal to the cannula to assess bronchial artery blood flow before, during and after CPB. The reference samples were taken from the descending aorta. We compared the different sites of injection. Tissue samples of the lungs were taken before and 60 min after CPB. Results: Before CPB, total bronchial artery perfusion was 43.6±14.1 ml/min (4.8±1.3% of cardiac output) as by injection distal to the aortic cannula. These values were not different when microspheres were injected into the left atrium or the aortic cannula. There was no difference in scatter or in the amount of microspheres in the reference samples among the three injections sites. During CPB, bronchial artery perfusion was significantly decreased (4.4±2.4 ml/min vs. 40.0±5.0 ml/min before CPB) and returned to baseline values 60 min after CPB. Light microscopy of the tissue samples revealed alveolar septal thickening and a decrease in alveolar surface area after 60 min of reperfusion which was associated with a decreased capacity to oxygenate blood. Conclusions: (1) Bronchial artery blood flow can quantitatively be assessed during CPB when microspheres are injected into the ascending aorta and the reference samples are taken from the descending aorta. (2) Despite adequate perfusion pressure bronchial artery blood flow is decreased substantially during CPB. (3) The decrease in blood flow and the ultrastructural changes present at the end of CPB suggest the presence of low-flow ischemia of the lung during total CPB.

Key Words: Lactate • Histology • Perfusion pressure


   1. Introduction
Top
 Abstract
 1. Introduction
2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
During cardiopulmonary bypass (CPB), both heart and lung are excluded from the circulation. While the myocardium is generally protected by cardioplegia, no measures are taken to protect the lung. The blood supply of the lung consists of two circulatory systems; the pulmonary circulation, and the bronchial circulation. During total CPB, blood flow to the lung is limited to flow through the bronchial arteries. Under normal conditions the predominant function of the bronchial circulation is to nourish the non-alveolar lung tissues [1]. When pulmonary blood flow seizes (e.g. during CPB) bronchial blood flow may be expected to increase as a compensatory measure [2,3].

Bronchial artery blood flow has been measured previously using different techniques, e.g. by the Fick principle [4] or by using dye dilution techniques [5]. During CPB, direct measurement of bronchial blood flow is possible by estimating the blood volume returning to the vent-catheter [6]. However, this technique is highly inaccurate because bronchial blood flow can accumulate in the lungs. Fluorescent microspheres are routinely used for the assessment of regional myocardial blood flow by injection into the left atrium and collection of the reference sample in the aorta [7–9]. The left ventricle functions as a mixing chamber for the microspheres and the blood. However, the mixing chamber is not available under conditions of CPB and it is meaningless to inject the microspheres into the left atrium under these conditions. Thus, assessment of organ perfusion with microspheres under condition of CPB requires the injection of microspheres into or just distal to the aortic cannula, which may not be as precise as with the conventional technique. We aimed to assess bronchial artery blood flow with fluorescent microspheres before, during and after CPB. We set out the hypothesis that bronchial artery perfusion is increased during CPB in a piglet model. In order to test the hypothesis we had to verify the reliability of microsphere injection into the ascending aorta (distal to the aortic cannula) and collection of the reference sample in the descending aorta, the site of bronchial artery offspring. As expected, the site of microspheres injection did not affect the reliability of the microsphere-technique. Contrary to expectations, we found that bronchial flow was decreased rendering the lung ischemic.


   2. Methods
Top
 Abstract
 1. Introduction
 2. Methods
3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
CPB was established in ten domestic piglets. The mean weight was 5.0±0.5 kg, which is equivalent to 4 weeks of age. Use of the animals was approved by the animal welfare committee of the University of Freiburg. All animals received humane care in compliance with the ‘Guide for the Care and Use of Laboratory Animals’ published by the National Institute of Health (NIH publication 85-23, revised 1985).

2.1. Monitoring and ventilation
After induction of anesthesia, the piglets were intubated with an endotracheal tube and placed on a respirator (Servo 900c, Siemens–Elema, Sweden). A positive end-expiratory pressure (PEEP) was set between 5 and 7 mmHg. During CPB, ventilation was discontinued but a PEEP was maintained. Rectal temperature was continuously monitored and kept at 36.0–37.5°C by warming blankets. The right and left jugular veins were cannulated for application of drugs and fluids (Ringer's solution at 50 ml/h) and monitoring of central venous pressure. After midline laparotomie, a 6 F arterial sheath was inserted into the abdominal aorta for monitoring of aortic pressure and withdrawal of blood samples and blood gas analyses. A catheter with fiberoptics and thermistor (Pulsion-Cold-System, Pulsion&Co. Medical System KG, München) was placed through the arterial sheath into the descending aorta for monitoring cardiac output. Urine output was measured hourly.

2.2. Establishment of CPB
Cardiopulmonary bypass (CPB) was established by cannulating the ascending aorta (2.0 mm, Cardiocorp., Friburg, Switzerland) and the right atrium (18 CH, Polystan AS, Denmark). The perfusion circuit was primed with fresh whole blood (approximately 400 ml) obtained from a donor piglet (same litter) prior to surgery. Heparin (400 IE/kg) and mannitol (50 ml) were added to the priming volume. After administration of heparin (400 IE/kg), the ductus arteriosus was closed and CPB was started. Total CPB was initiated by clamping the main pulmonary artery. No protamin was given at the end of CPB.

2.3. Experimental protocol
Fig. 1 shows a schematic of the experimental protocol. Total CPB time was 120 min, followed by 60 min of reperfusion. Microspheres were injected before CPB, immediately after establishment of CPB, at the end of CPB and at the end of reperfusion. Tissue samples of the lung were taken from he right lower lobe before CPB, at the end of CPB and at the end of reperfusion. Additionally, tissue samples from separate animals were taken before CPB and incubated for 2 h at 37°C under vacuum (total, global ischemia).



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  		Fig. 1. Schematic of the experimental protocol. Total cardiopulmonary bypass (CPB) was established for 120 min followed by 60 min of reperfusion. The arrows indicate the timepoints of injection of MS and the excision of tissue samples of the lung (tissue sample).

 
2.4. Assessment of bronchial artery blood flow
Bronchial artery blood flow was determined with fluorescent microspheres in a modification of the methods described by Sakka et al. [8]. Microspheres were injected as bolus (2 million over 5 s) at four different time points using four different color codes (orange, blue–green, red, yellow–green). All catheters were teflon coated to avoid adherence to the tubes. Microspheres were injected at three different sites: (1) left atrium, (2) arterial cannula of the CPB, (3) ascending aorta, distal to the aortic cannula. The reference samples were withdrawn from the descending aorta. Withdrawal of blood was started with a Harvard pump (Harvard Apparatus Inc., South Natick, MA) 5 s before the injection of microspheres and continued for 90 s at a constant flow rate of 7.5 ml/min. At the end of the experiments the whole lung was resected and divided into 14 pieces. All tissue samples and the reference samples were digested in KOH (10 mol/l, 50°C) for 8 h. Subsequently, microspheres were filtered out of the digest by a polyamid 7 µm filter membrane. After drying of the filters (2 h at 37°C), microspheres were dissolved with 3 ml ethoxyacetylacetate, and the light emission of the fluorescent dye was measured in a fluorescent spectrophotometer (Perkin–Elmer Spectrophotometer 650-10LC, Ueberlingen, Germany). The number of microspheres in the samples was calculated by comparing the degree of fluorescence to a previously obtained calibration curve. Regional blood flow was calculated using the following formula

where MS is microspheres, CO is cardiac output and reference is the reference sample.

2.5. Histological investigations
The tissue samples for histological investigations were fixed in 4% formalin solution and stained with hematoxylin eosin (HE). Samples were inspected under light microscopy at a maximal magnification of 100x.

2.5.1. Determination of tissue lactate
We determined tissue lactate as a marker for anaerobic metabolism. Tissue samples were frozen immediately after resection in liquid nitrogen. These tissue samples were ground under liquid nitrogen and extracted with 6% perchloric acid (PCA). The neutralized extracts were assayed for lactate content enzymatically as described by Bergmeyer [10].

2.6. Statistical analysis
Statistical analysis was performed by ANOVA with repeated measures analysis of variance with post hoc Newman–Keuls test. A P<0.05 was considered significant. Values are given as mean±standard deviation (SD).


   3. Results
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
4. Discussion
 Appendix A. Conference...
 References
 
Fig. 2 shows CO or pump flow as well as perfusion pressure before CPB, at the beginning and at the end of CPB as well as at the end of 60 min of reperfusion. The mean arterial pressure measured in the abdominal aorta did not change with the onset of CPB. Neither blood flow nor aortic pressure changed during the experiment. During reperfusion flow rate and blood pressure were slightly but not significantly decreased.



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  		Fig. 2. Cardiac output (CO) or pump flow during CPB (A) and arterial perfusion pressure (B) before CPB, at the beginning and at the end of CPB, as well as at the end of 60 min of reperfusion (n=10). Note that there was no decrease in perfusion pressure or flow with the onset of CPB. Values are given as mean±SD.

 
Fig. 3 shows the number of microspheres in the reference sample in relation to the site of microsphere application. Microspheres were injected in conventional manner into the left atrium, into the aortic cannula during CPB or into the aorta just distal to the aortic cannula. The pump flow was adjusted to pre-bypass CO. Perfusion pressure did not change under these conditions (Fig. 2). There was no significant difference between the three injection sites with respect to scatter or amount of microspheres in the reference sample. Additionally, in six animals double measurements were determined at the application site ‘atrium’ and ‘aorta’. The results were identical.



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  		Fig. 3. Number of microspheres in the reference sample (individual values and mean±SD) when microspheres (2 millions) were injected into the left atrium (n=8), into the aortic cannula (n=8) or into the aorta distal to the aortic cannula (n=8). The reference samples were withdrawn from the descending aorta. Please see text for details.

 
Fig. 4 shows bronchial artery blood flow in absolute values before cardiopulmonary bypass, at the beginning and at the end of CPB as well as after 60 min of reperfusion. There was a significant decrease in bronchial artery blood flow with the beginning of total CPB (P=0.01), which was the same at the end of CPB. Bronchial blood flow returned to near normal values during reperfusion.



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  		Fig. 4. Bronchial artery blood flow in absolute values before CPB, at the beginning, at the end of 120 min of CPB and after 60 min of reperfusion (n=10). Note the dramatic decrease in bronchial blood flow during CPB. Values are given as mean±SD; *P=0.01 vs. before CPB.

 
Fig. 5 shows bronchial artery blood flow in percent of cardiac output. Under normal conditions, bronchial artery blood flow was 4.8±1.3% of cardiac output. Since perfusion pressure and flow during CPB did not change, bronchial artery blood flow as expressed as percent of CO showed the same pattern as the absolute values.



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  		Fig. 5. Bronchial artery blood flow in percent of cardiac output (CO) before CPB, at the beginning, at the end of 120 min of CPB and after 60 min of reperfusion (n=10). Values are given as mean±SD; *P=0.01 vs. before CPB.

 
Fig. 6 shows light microscopic images of tissue samples of the lung before CPB, at the end of 60 min of reperfusion and after 120 min of total, global ischemia. We used 120 min of total, global ischemia in order to be able to compare the effects of CPB to total ischemia. There was a significant increase in alveolar septal thickness and a decrease in alveolar surface area after CPB. After 120 min of total, global ischemia, the alveolar septi were about 30% thicker and the alveolar surface area was 60% smaller than after CPB suggesting the presence of low flow but not total ischemia. The increase in alveolar septal thickening and decrease in alveolar surface area was associated with a reduced capacity to oxygenate blood as indicated by PaO2/PaCO2 before CPB and 60 min after reperfusion (455±152/34±7 mmHg vs. 373±99/42±8 mmHg, n.s.).



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  		Fig. 6. Light microscopic images of lung tissue before CPB (A), after 60 min of reperfusion (B) and 120 min of in vitro ischemia (C). Note the increase in alveolar septal thickness and decrease in alveolar surface area after CPB compared to the native lung (A).

 
Table 1 shows lactate content of lung tissue before CPB, after 120 min of CPB and after 120 min of total, global ischemia. There was a significant increase in tissue lactate content during 120 min of CPB. After 120 min of total, global ischemia tissue lactate content was three times higher than at the end of CPB. The increased content of lactate at the end of CPB compared to before CPB supports the notion of low flow, but not total ischemia during CPB.


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  		Table 1. Lactate content of lung tissue before CPB, after 120 min of CPB and after 120 min of total, global ischemiaa

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
Appendix A. Conference...
 References
 
We demonstrate, that despite adequate perfusion pressure, bronchial artery blood flow is decreased substantially during CPB. The decrease in blood flow is associated with ultrastructural changes present at the end of CPB suggesting the presence of low flow ischemia of the lung during total CPB. We also demonstrate, that bronchial artery blood flow can reliably be assessed during CPB when microspheres are injected into the ascending aorta and the reference samples are taken from the descending aorta.

The assessment of bronchial blood flow under normal conditions obeys the same principles as the determination of myocardial blood flow or regional blood flow in other organ systems. However, when the left ventricle as mixing chamber is excluded and the systemic circulation is delivered by a roller pump, the distribution of the microspheres when injected into the blood stream through the aortic cannula or distal to the cannula may become inhomogeneous. Inhomogeneity of the microspheres in the blood may result in artifacts in regional blood flow since blood with high amounts of particles may reach the bronchial circulation while blood with low amounts of microspheres may be aspirated into the reference sample or vice versa. We reasoned that if such inhomogeneity would be present when microspheres are injected into the cannula or the aorta, the total number of microspheres would be expected to be significantly higher or lower, or both, resulting in different mean values and a significantly greater amount of scatter. We injected microspheres in the left ventricle and compared the results with those when microspheres were injected into the aorta or the aortic cannula. Neither the amount of microspheres in the reference samples nor the total blood flow to the lung as assessed by the microsphere technique differed among the three injection sites. We therefore conclude that the injection of microspheres into the ascending aorta, distal to the aortic cannula and collection of the reference sample from the descending aorta is a reliable method to determine bronchial blood flow in our animal model ‘on’ or ‘off’ pump.

Using this technique, we found that bronchial blood flow decreases dramatically with the onset of reperfusion. This observation was unexpected since the reduction in pulmonary flow may have resulted in a compensatory increase in bronchial blood flow. Indeed, under chronic conditions (e.g. restricted pulmonary blood flow due to congenital heart defects) the bronchial circulation increases. [11,12]. Little is known about the response to acute obstructions of the pulmonary artery and the results are inconclusive [2,3,12,13]. Recently, Kowalski et al. [14] demonstrated a linear decrease of bronchial artery blood flow over 24 h in rabbit lungs after occlusion of the main pulmonary artery without an increase of flow after reperfusion. Bronchial artery blood flow was determined by a modification of the reference flow technique with radiolabeled microspheres [15]. We demonstrate, that the bronchial artery blood flow decreases immediately with the onset of CPB and returns to near normal values after reperfusion. The reason for this sudden decrease is unclear. During routine cardiopulmonary bypass procedures in humans, there is usually a profound decrease in arterial blood pressure with the beginning of CPB, which is caused by decrease in peripheral vascular resistance. Such a decrease in arterial pressure may be suspected to be the reason for the reduction in bronchial artery blood flow. However, both perfusion pressure and systemic blood flow did not change, arguing against this possible explanation. Other possible explanations include a differential increase in pulmonary vascular resistance after starting CPB. Since the measurement of pressure in the aorta may not reflect pressure or resistance in the bronchial arteries, we are only able to speculate on this matter. Whatever the mechanism might be, it appears reasonable to conclude, that if the clinical scenario of a substantial decrease in resistance and perfusion pressure were to occur in this model, the effects on bronchial artery blood flow would have been even greater. If the histological and metabolic data translate into decreased pulmonary function this phenomenon may be responsible for a great part of the pulmonary dysfunction observed after CPB under clinical conditions.

We took histological specimens to relate the changes in blood flow to ultrastructure and presumably function. Septal thickness indicates the distance for alveolar gas exchange and alveolar surface area indicates the total amount of area with gas exchanging function. Thus, the increase in alveolar septal thickness would reflect hampered gas exchange and the reduction in alveolar surface area indicates a reduction in the available area for gas exchange. These structural changes of the lung parenchyma was associated with a decreased capacity to oxygenate blood. After 60 min of reperfusion PaO2/PaCO2 levels were clearly reduced compared to pre-bypass levels. Our findings may support the observations of a recent study of Suzuki et al. [10], who showed gradually decreased PaO2-levels in infants after CPB with a peak reduction after 12 h of reperfusion. However, since we were not able to quantify our observations, it is impossible to assess the severity of these findings and relate them to function.

The presence of an increased lactate content at the end of CPB suggests the presence of anaerobic metabolism, i.e. ischemia. Since the amount of lactate in the ischemic tissue in vitro was substantially higher than after CPB, it is reasonable to conclude that during CPB the lung is subjected to low flow but not total ischemia.

We conclude, that bronchial artery blood flow can quantitatively be assessed during CPB when microspheres are injected into the ascending aorta and the reference samples are taken from the descending aorta. We also conclude that despite adequate perfusion pressure bronchial artery blood flow is decreased substantially during CPB. We finally conclude that the decrease in blood flow and the ultrastructural changes present at the end of CPB suggest the presence of low flow ischemia of the lung during total CPB.


   Acknowledgments
 
The study was supported by funds from the Zentrum für Klinische Forschung II from the University of Freiburg. We thank Drs Jose Bitu-Moreno and Irene Wenzel-Elias for technical assistance and Dr Koppany Sarai for advice.


   Footnotes
 
Present at the 13th Annual Meeting of the European Association of Cardio-thoracic Surgery, Glasgow, Scotland, UK, September 5–8, 1999.


   Appendix A. Conference discussion
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
References
 
Dr M. Turina (Zurich, Switzerland): Whenever you take an animal on cardiopulmonary bypass there is a profound drop of blood pressure. Did you correlate the drop in bronchial artery perfusion to the level of the arterial pressure?

Dr Schlensak: You are correct that under clinical conditions and in large animals, there is a decrease in blood pressure with the onset of cardiopulmonary bypass. However, in our piglet model we did not observe this phenomenon although the CPB conditions were comparable to the clinical condition. As a consequence, there is always close correlation between flow and pressure in our system. However, bronchial artery blood flow decreased during bypass despite the maintenance of flow and pressure. That was the striking observation, and we have not been able to pinpoint the mechanism to this point.

Dr Turina: Because there is a major drop in peripheral vascular resistance which will reduce the perfusion pressure head for the bronchial arteries.

Dr Schlensak: As touched on in the last answer, we did not see a decrease in aortic perfusion pressure during CPB. This observation may be a unique feature to this animal model. The measurement of pressure in the aorta may not reflect pressure or resistance in the bronchial arteries, which was not measured. However, if the clinical scenario of a substantial decrease in resistance and perfusion pressure were to occur in this model, the effects on bronchial artery blood flow would have been even greater.

Dr A. Diegeler (Leipzig, Germany): Did you change temperature during your investigation and does it cause differences in lung performance?

Dr Schlensak: We didn't change temperature during the experiments. The lowest rectal temperature reached during the experiments was 35.2°C. Our assessment of pulmonary function was limited metabolite and histological studies and we are unable to make any statements regarding clinically relevant functional parameters.

Dr T. Mesana (Marseille, France): Do you believe that this reduction in flow is related to the non-pulsatile flow? In other words, do you think that if you had used the pulsatile assisted circulation, you should have the same reduction in flow?

Dr Schlensak: This is indeed our favorite working hypotheses since this is the only obvious difference between the ‘off pump’ and ‘on pump’ circulation. Other explanations may include differential changes in vascular resistance or changes in the ventilation pattern.

Dr M. Kamler (Essen, Germany): Did you ventilate the lungs during cardiopulmonary bypass?

Dr Schlensak: While dynamic ventilation of the lungs was discontinued a positive (PEEP) was maintained at 7 cm H2O during CPB. We aimed to imitate the clinical situation where either a PEEP or a high frequency ventilation was very small tidal volumes is maintained. This technique ascertains inflation of the lung tissue during CPB.

Dr J. Hasse (Freiburg, Germany): Have you, by chance, been looking in a control where you block the bronchial arteries completely and have you looked to the tissue for changes?

Dr Schlensak: This is an excellent idea and theoretically providing the proof of principle. However, in practice, it is extremely difficult to identify the origin of all bronchial arteries, which prevented us from performing these experiments.

Dr D. Dougenis (Patras, Greece): Based on your results, would you consider the bronchial circulation very important for the lung recovery and therefore recommend reimplanting the bronchial arteries, for instance; in surgery for descending thoracic aneurysms?

Dr Schlensak: It is difficult for me to give you a satisfactory answer because did not investigate the effects of a lack of bronchial blood flow on the recovery of function after CPB. The thought of implantation of the bronchial arteries during replacement of the descending aorta is intriguing but may be limited by the well known time constraints of the operation. In any case, we know from lung transplantation, that bronchial blood flow recovers to a certain extent although bronchial arteries are not reimplanted. More importantly, despite the absence of bronchial anastomoses, the transplanted lungs are well able to fully recover from the transplantation ischemia.


   References
Top
 Abstract
 1. Introduction
 2. Methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 

  1. Baretti R., Bitu-Moreno J., Beyersdorf F., Matheis G., Francischetti I., Kreitmayr B. Distribution of lung preservation solutions in parenchyma and airways: influence of atelectasis and route of delivery. J Heart Lung Transplant 1995;14:80-91.[Medline]
  2. Jindal S.K., Lakshminarayan S., Kirk W., Butler J. Acute increase in anastomotic bronchial blood flow after pulmonary arterial obstruction. J Appl Physiol 1984;57:424-428.[Abstract/Free Full Text]
  3. Malik A.B., Tracy S.E. Bronchovascular adjustments after pulmonary embolism. J Appl Physiol 1980;49:476-481.[Abstract/Free Full Text]
  4. Deal C.W., Louis E., Kerth W.J., Osborn J.J., Gerbode F. Bronchopulmonary precapillary blood flow during cardiopulmonary bypass. Am Heart J 1968;75:43-48.[Medline]
  5. Fritts H.W., Harris P., Chidsey C.A., Clauss R.H., Cournand A. Estimation of flow through bronchial-pulmonary vascular anastomoses with the use of T-1824 dye. Circulation 1961;23:390-398.[Abstract/Free Full Text]
  6. Baile E.M., Ling H., Heyworth J.R., Hogg J.C., Pare P.D. Bronchopulmonary anastomotic and noncoronary collateral blood flow in humans during cardiopulmonary bypass. Chest 1985;87:749-754.[Abstract/Free Full Text]
  7. Glenny R.W., Bernard S., Brinkley M. Validation of fluorescent-labeled microspheres for measurement of regional organ perfusion. J Appl Physiol 1993;74:2585-2597.[Abstract/Free Full Text]
  8. Sakka S.G., Wallbridge D.R., Heusch G. Glossary: methods for the measurement of coronary blood flow and myocardial perfusion. Basic Res Cardiol 1996;91:155-178.[Medline]
  9. Van Oosterhout M.F., Willigers H.M., Reneman R.S., Prinzen F.W. Fluorescent microspheres to measure organ perfusion: validation of a simplified sample processing technique. Am J Physiol 1995;269:H725-H733.[Abstract/Free Full Text]
  10. Bergmeyer H.U. . Methods of enzymatic analysis, 2nd ed. Deerfield Beach, FL: Verlag-Chemie, 1974:1464-1565.
  11. Weibel E.R. Early stages in the development of collateral circulation to the lung in the rat. Circ Res 1960;8:353-376.[Abstract/Free Full Text]
  12. Agostoni P.G., Deffebach M.E., Kirk W., Mendenhall J.M., Albert R.K., Butler J. Temperature alters bronchial blood flow response to pulmonary arterial obstruction. J Appl Physiol 1987;62:1907-1911.[Abstract/Free Full Text]
  13. Malik A.B., Tracy S.E. Bronchovascular adjustments after pulmonary embolism. J Appl Physiol 1980;49:476-481.
  14. Kowalski T.F., Guidotti S., Deffebach M., Kubilis P., Bishop M. Bronchial circulation in pulmonary artery occlusion and reperfusion. J Appl Physiol 1990;68:125-129.[Abstract/Free Full Text]
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ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
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