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Ann Thorac Surg 1995;60:1294-1298
© 1995 The Society of Thoracic Surgeons


Original Articles: Cardiovascular

Retrograde Cerebral Perfusion: Anatomic Study of the Distribution of Blood to the Brain

Jean-Louis de Brux, MD, Jean-Baptiste Subayi, MD, Jean-Dominique Pegis, MD, Jean Pillet, MD

Service de Chirurgie Cardio-Vasculaire et Thoracique, and Laboratoire d'Anatomie, Faculté de Médecine, Angers, France

Accepted for publication June 10, 1995.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Despite apparently good clinical results with retrograde cerebral perfusion during operation on the aortic arch, there is still concern about the real distribution of the blood injected in the superior vena cava to the brain, especially when the internal jugular vein is valvulated (88% of the cases). This anatomic study was carried out to determine how a liquid injected in the superior vena cava reaches the brain.

Methods. Three groups of adult cadavers (5, 5, and 3 cases, respectively) were injected with latex, colored blue, through a cannula in the superior vena cava. In group I, 600 mL of latex was injected. Group II was identical except that a catheter had been inserted, before the injection, into the internal jugular vein to collapse the internal jugular vein valve, when existing. In group III, the azygos vein was ligated.

Results. The internal jugular vein was not valvulated in 2 cases in group I. In those 2 cases, latex was found up to the jugular foramen. In the other cases in group I, and in all cases in group II, where the internal jugular vein was valvulated, the following veins were injected: internal jugular vein up to the valve (almost no latex beyond), azygos vein, inferior vena cava, renal veins, rachidian and perimedullar venous plexuses, and venous sinuses of the brain. In group III, no opacification was observed beyond ligated azygos vein or valvulated internal jugular vein.

Conclusions. Despite the fact that this study was carried out on cadavers, one can assume that, during retrograde cerebral perfusion, the azygos vein system is a major way to the central nervous system when the internal jugular vein is valvulated.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
See also page 1298.

Retrograde cerebral perfusion, as a method of cerebral protection during operation on the aortic arch, is gaining acceptance, even for long durations of cerebral perfusion [14]. As the number of reported clinical cases is growing, neurologic damage after operation on the aortic arch seems to be reduced. However, it has not yet been anatomically proved that the blood injected into the superior vena cava (SVC) reaches the brain in the presence of valvulated internal jugular veins (IJVs). The experiments carried out in dogs often use direct injection through the internal maxillary veins [5, 6]. In humans, only metabolic evidence of the real perfusion of the brain has been demonstrated [7]. Anatomic pathways from the SVC to the brain have only been assumed [8], especially in the presence of a valvulated IJV. We present here an anatomic study that shows evidence of the pathways of blood from SVC to the brain.


    Material and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
This study was carried out in 13 human adult, recently deceased cadavers. A median sternotomy and a bilateral cervicotomy were performed. Superior and inferior venae cavae were controlled, as well as both internal jugular veins and carotid arteries. A 28F cannula was inserted in the SVC through a pursestring suture in the right atrial appendage. Latex Neopren (Safic-Alcan Laboratories, Puteaux, France) was injected through this cannula by means of a pressure cuff set at 70 mm Hg. Pressure monitoring was not performed directly in the SVC. Superior vena caval tapes were applied to prevent backward injection to the right atrium (Fig 1Go).



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Fig 1. . Cannula (C) and mediastinal veins. (Arrow = right internal thoracic vein [reclined]; lbv = left brachiocephalic vein; rijv = right internal jugular vein; svc = superior vena cava.)

 
Cadavers were divided into three groups (Fig 2Go): In group I (5 cases), 600 mL of latex was injected into the SVC at a rate of approximately 100 mL/min. In group II (5 cases), a 10F catheter simulating the presence of a Swan-Ganz catheter was inserted in the right IJV down to the SVC to collapse the IJV valve, if it exists. The inferior vena cava was ligated. Subsequently, 600 mL of latex was injected as in group I. Group III (3 cases) was the same as group II, except that the azygos vein was ligated near its ending in the SVC. It was not possible to inject more than 200 mL of latex.



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Fig 2. . Anatomic study. (Asterisk = catheter in internal jugular vein [IJV]; Az. V. = azygos vein; black arrow = azygos vein ligated; RA = right atrium; white arrow = inferior vena cava ligated.)

 
The cadavers were then stored for 1 week in a mixture of formol, alcohol, glycerin, and water. This period was necessary for the latex to solidify. The experiment was then resumed to look for the presence of latex in the vessels: right and left brachiocephalic veins, IJV, internal thoracic and epigastric veins, and renal veins. Thorax and abdomen were subsequently eviscerated and the profound venous trunks were examined: azygos, intercostal, and lumbar veins and inferior vena cava. The spine was severed at the level of T10 and C1 and the perimedullar, intrarachidian and extrarachidian venous plexuses were studied. Finally, the posterior part of the skull was removed in 5 cases in groups I and II and 1 case in group III, and the venous sinuses of the brain were studied.


    Results
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Valvulated IJVs were found in 11 of the 13 cases (84.6%). In the 2 cases of group I where the IJV was not valvulated, latex was found in the IJV up to the jugular foramen. In all other cases, IJV valves were competent on the right and left sides, and almost no latex was found beyond them (Fig 3Go), even in group II with the catheter introduced in the IJV.



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Fig 3. . Opacification of the right internal jugular vein. (ca = right carotid artery; 1 = internal jugular vein below the valve; 2 = internal jugular vein beyond the valve.)

 
In groups I and II, a massive injection of latex was found in the internal thoracic, intercostal, lumbar, renal, and azygos veins, and also in the inferior vena cava (Figs 4, 5GoGo). In group I, the right atrium was also filled with latex.



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Fig 4. . Azygos and intercostal veins (az).

 


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Fig 5. . Inferior vena cava (ivc) and left renal vein (arrow). The right kidney has been removed.

 
As for the central nervous system, massive injection of latex was observed in the intrarachidian and extrarachidian venous plexuses in all cases of groups I and II (Fig 6Go), and also in the perimedullar venous plexuses (Figs 7, 8GoGo). As for the brain, opacification of the superior sagittal sinus as well as the lateral venous sinuses was observed (Fig 9Go) in the 5 cases where the skulls were removed. Also, superficial veins of the cerebral hemispheres and of the cerebellum were opacified.



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Fig 6. . Thoracic vertebra: intrarachidian (large arrows) and extrarachidian venous plexuses (small arrows). (S = spinal cord.)

 


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Fig 7. . Cervical spinal cord, posterior aspect. (Arrow = posterior vein of the spinal cord.)

 


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Fig 8. . Cervical spinal cord, anterior aspect. (Arrow = anterior vein of the spinal cord.)

 


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Fig 9. . Venous sinuses of the brain. (Curved arrow = longitudinal sinus; straight arrow = transverse sinus [left].)

 
In group III, with ligation of the azygos vein, no opacification was observed except that of the SVC, right and left brachiocephalic veins, and IJV up to the valves.


    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
This anatomic study showed that, even in the presence of valves in the IJV, a liquid injected in the SVC reaches the central nervous system. It also showed evidence for the major role of the azygos vein system between the SVC and the central nervous system, because when the azygos vein is ligated, no latex is found beyond the valves or the ligated vessels. Previous anatomic studies have shown that the IJV is valvulated in a majority of cases: 7 of 7 cases in the study by Dresser and McKinney [9], and 88% of the cases in the study by Midy and associates [10]. The valve is competent in most cases: 6 of 7 cases in the study by Dresser and McKinney [9] and 88% of the cases on the right side and 44% on the left side in the study by Murase and associates [8].

In the present study, all the valves seemed to be competent, although a very small amount of latex was found beyond the valve in the IJV; it was not possible to state if it came through the valve from the SVC, or from a back-flow of the venous sinuses of the brain.

However, in clinical use, it is possible that the IJV valves do not close completely and may flutter, allowing blood to go through the valves and directly perfuse the brain. There is Doppler evidence that this may occur [11], but one cannot rely on this possibility to perfuse the brain directly in 100% of the cases.

In the present study, massive injection of the inferior vena cava and renal veins (and also the injection of the right atrium when the inferior vena cava is not ligated) is consistent with clinical and metabolic observations that only 1% to 20% of the blood injected in the SVC returns through the innominate and left carotid arteries; the rest is drained through the inferior vena cava [12, 13].

From an anatomic point of view, the azygos vein system represents the major anastomosis between the SVC and the inferior vena cava. Furthermore, the vertebral venous system is largely anastomosed with the caval azygo-lumbar systems, and the veins of various viscera (kidney), as shown by Couinaud [14]. The vertebral venous system contributes to the composition of the venous plexus of the foramen magnum, which is largely anastomosed with the intracranial sinuses.

From a physiologic point of view, Batson [15] showed that the vertebral venous system is avalvulated and that the venous pressure remains lower in the vertebral than in the caval venous system when there is a pressure increase in the caval venous system. He stated that ``the direction of flow in these vessels [the vertebral veins] is largely a matter of chance.'' Numerous anatomic studies reported by Couinaud [14] and Batson [15] have shown the importance of the vertebral venous system in the venous drainage of the brain in the presence of a mechanical or functional obstacle in the SVC. Gonzales-Fajardo and associates [16] recently showed, in an experimental model in dogs, a sharp increase in central venous pressure and in intracranial pressure when the SVC and the azygos vein were clamped. This pressure increase was significantly lower when the azygos vein was left unclamped.

The optimal retrograde cerebral perfusion conditions remain to be determined in humans, but it seems reasonable to follow the recommendations given by Usui and associates [5], keeping in mind that the recommended pressure of 25 mm Hg can be obtained with either a low flow through the SVC when the IJV is avalvulated or a higher flow when the IJV is valvulated. Nevertheless, one can assume that, even when the IJV is avalvulated, a great amount of the blood injected in the SVC is drained by the azygos vein and perfuses abdominal organs. Some authors have used total body retrograde perfusion [11, 17] with good clinical results, and state that this technique allows perfusion of abdominal organs (eg, kidneys, liver).

One of the drawbacks of this study is that it is a postmortem experiment, performed with latex; the rate of injection and the pressure monitoring do not reflect exactly the observations made in vivo with blood. Therefore, the results cannot be entirely extrapolated to the clinical use of retrograde cerebral perfusion. However, we showed anatomic evidence for the real perfusion of the brain during retrograde cerebral perfusion through the SVC, even in the presence of a valvulated IJV. Furthermore, the large distribution of the blood injected retrogradely in the SVC might extend the duration of safe circulatory arrest, with better protection, not only of the brain (even and durable cooling, prevention of air and particulate emboli, even in the absence of active metabolism at low temperatures) but also of other organs, such as spinal cord, kidneys, and other abdominal organs.


    Acknowledgments
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
We acknowledge the technical assistance of Mr Stéphane Sourice and Mr Bernard Vivien.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr de Brux, Service de Chirurgie Cardiovasculaire et Thoracique, CHU d'Angers, 4 rue Larrey 49033, Angers Cedex, France.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Takamoto S, Matsuda T, Harada M, Miyata S, Shimamura Y. Simple hypothermic retrograde cerebral perfusion during aortic arch replacement. A preliminary report on two successful cases. J Thorac Cardiovasc Surg 1992;104:1106–9.[Abstract]
  2. Safi HJ, Heather HW, Winter JN, et al. Brain protection via cerebral retrograde perfusion during aortic arch aneurysm repair. Ann Thorac Surg 1993;56:270–6.
  3. Coselli J. Retrograde cerebral perfusion via a superior vena caval cannula for aortic arch aneurysm operations. Ann Thorac Surg 1994;57:1668–9.
  4. De Brux J-L, Subayi J-B, Bukowski JG, et al. Perfusion cérébrale de longue durée dans la chirurgie de la crosse aortique. A propos de deux cas. Ann Chir 1994;48:845–9.[Medline]
  5. Usui A, Oohara K, Liu T, et al. Determination of optimum retrograde cerebral perfusion conditions. J Thorac Cardiovasc Surg 1994;107:301–8.
  6. Usui A, Oohara K, Liu T, et al. Comparative experimental study between retrograde cerebral perfusion and circulatory arrest. J Thorac Cardiovasc Surg 1994;107:1228–36.[Abstract/Free Full Text]
  7. Lin P, Chang C, Tan P, et al. Protection of the brain by retrograde cerebral perfusion during circulatory arrest. J Thorac Cardiovasc Surg 1994;108:969–74.[Abstract/Free Full Text]
  8. Murase M, Maeda M, Koyama T, et al. Continuous retrograde cerebral perfusion for protection of the brain during aortic arch surgery. Eur J Cardiothorac Surg 1993;7:597–600.[Abstract]
  9. Dresser LP, McKinney WM. Anatomic and pathophysiologic studies of the human internal jugular valve. Am J Surg 1987;154:220–4.[Medline]
  10. Midy D, Le Huec JC, Dumont D, et al. Etude anatomique et histologique des valves des veines jugulaires internes. Bull Assoc Anat 1988;72:21–9.
  11. Alexander JC. Retrograde cerebral protection for complex aortic surgery. Presented at the 15th Annual Cardiothoracic Surgery Symposium, San Diego, CA, Feb 23–26, 1995.
  12. Usui A, Hotta T, Hiroura M, et al. Retrograde cerebral perfusion through a superior vena caval cannula protects the brain. Ann Thorac Surg 1992;53:47–53.[Abstract]
  13. Boeckxstaens CJ, Flameng WJ. Retrograde cerebral perfusion does not perfuse the brain in nonhuman primates. Ann Thorac Surg 1995;60:319–28.[Abstract/Free Full Text]
  14. Couinaud C. Une méconnaissance en physiopathologie viscérale: le système veineux vertébral. J Chir 1973;105:125–42.
  15. Batson OV. The vertebral veins system. Am J Roentgenol 1957;78:195–212.
  16. Gonzales-Fajardo J, Garcia-Yuste M, Florez S, Ramos G, Alvarez T, Coca J. Hemodynamic and cerebral repercussions arising from surgical interruption of the superior vena cava. Experimental model. J Thorac Cardiovasc Surg 1994;107:1044–9.[Abstract/Free Full Text]
  17. Yasuura K, Ogawa Y, Okamoto H, et al. Clinical application of total body retrograde perfusion to operation for aortic dissection. Ann Thorac Surg 1992;53:655–8.[Abstract]

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