TY - JOUR
AU - Watterson, Kevin, G.
AB - Abstract Objectives: The objective of this project was to quantify the effects of geometry on the distribution of hepatic blood to the lungs in patients with a total cavo-pulmonary connection. The basis for this work is the supposition that hepatic blood is necessary for proper lung function. Methods: Plastic models of these connections were made with varying degrees of offset between the inferior and superior vena cava and attached to an in vitro flow loop. Dye was injected into the inferior vena cava and its concentration quantified in each pulmonary artery. These data were converted to percentage concentration and distribution of hepatic blood to each lung. Results: With no offset between the vena cava, hepatic blood distribution and concentration to each lung was similar to normal. For an offset of one or more diameters, hepatic blood tended to flow preferentially towards the nearest pulmonary artery with the opposite pulmonary artery exhibiting a deficit (≪10% of normal). Conclusions: Distribution of hepatic blood to each lung was found to be a function of vena cava offset and pulmonary artery flow split. Under normal conditions, 60% of blood towards the right pulmonary artery, the hepatic blood distribution to both lungs could be maintained above 50% of normal if the inferior vena cava was offset towards the left pulmonary artery. Offsetting the inferior vena cava towards the right pulmonary artery jeopardized the delivery of hepatic blood to one lung. Fontan, Total cavo-pulmonary connection, Atrio-venous malformation 1 Introduction The total cavo-pulmonary connection (TCPC) is one of the many variations on Fontan-type operations used to correct for congenital heart defects such as pulmonary and tricuspid atresia, univentricular heart and hypoplastic left heart syndrome [1–4]. In the TCPC operation an intra-atrial or extra-cardiac tunnel is used to connect the inferior vena cava (IVC) directly to the right pulmonary artery (RPA) thereby preventing venous blood from entering the right heart. The superior vena cava (SVC) is anastomosed to the right pulmonary artery (RPA) and the main pulmonary artery closed. The venous blood flow pathway from the systemic to the pulmonary circulation under these conditions then appears as a ‘cross’, with the four limbs comprising the IVC, SVC, RPA and LPA (left pulmonary artery). In redirecting the venous blood in this manner, however, care must be taken to minimize the energy loss of the blood by ensuring that the connection has a low hemodynamic resistance. This requirement becomes important as the right ventricle no longer provides an energy input into the venous return, forcing the left ventricle to be responsible for driving the circulation through both the systemic and pulmonary vascular beds. A hemodynamically poor Fontan procedure would result in an increased resistance with a resultant drop in flow rate and/or venous hypertension. This resistance to blood flow is mainly due to the geometry of the connection with bends, expansions and junctions all creating energy losses through increased friction and flow disturbance or mixing. In general, the greater the disruption to the flow the greater the fluid energy loss. For this reason, there has been a growth in interest in the effect of Fontan geometry on fluid energy loss [2,5–13], with Sharma et al. [5] showing in vitro and Lardo et al. [12] in a sheep heart preparation that by offsetting the IVC in the TCPC connection, significant reductions in energy loss can be achieved. More studies are currently being performed on other geometric variations to further reduce the TCPC resistance [8–10]. Clinical results, however, have indicated that low flow resistance is not the only consideration in deciding the geometry of a Fontan-like procedure [14–20]. In some cases, where, for one reason or another, hepatic blood has been excluded from one or both lungs, complications have arisen involving the development of pulmonary arteriovenous malformations (PAVMs). Thus in deciding upon a TCPC connection geometry, care must be taken to allow adequate hepatic blood flow to both lungs. There is, therefore, a balance to be struck between using a TCPC geometry with little mixing in order to lower energy losses and one with mixing in order to disperse hepatic IVC blood to both lungs. The objective of this paper was to determine this balance by quantifying the distribution of IVC blood to each lung in an in vitro model of a TCPC connection. Previously published energy loss data have quantified energy loss as a function of IVC offset and RPA/LPA flow split [5]. The authors therefore used these same geometries and flow splits to investigate the effect of IVC offset and RPA/LPA flow split on hepatic blood distribution to the lungs, so that a comparison to connection resistance could be made. 2 Methods 2.1 Flow model Rigid Plexiglas models of typical TCPC connections were constructed based on measurements given by Sharma [5]. The connections consisted of four straight, circular limbs representing the RPA, LPA, IVC and SVC, all with internal diameters of 13.5 mm. Three models were made, corresponding to IVC offsets of zero, one and two diameters. The models were connected to a steady flow system, using a static water tank to produce constant flow into the IVC and SVC. The outlets from the RPA and LPA were discharged to atmospheric pressure. Rotometers were located in the SVC, RPA and LPA in order to measure the overall flow rate as well as the inlet and outlet flow splits. Valves in each limb allowed flow control. An overall flow rate of 4 l/min with 60% of the flow through the IVC was used for all experiments. Flow through the RPA was varied from 30 to 70% of the total, in steps of 10%. 2.2 Hepatic blood distribution In order to determine the distribution of hepatic blood to the RPA and LPA, purple dye (5% potassium permanganate) was infused into the IVC limb well upstream of the connection so as to homogeneously colour the IVC flow purple. The SVC flow remained clear of dye. After stabilization of the flow, the RPA and LPA discharge fluids were simultaneously collected for a short time using plastic bowls. A laser pointer was then used to quantify the volume concentration of dye in the RPA and LPA fluid. This was achieved by passing the laser light through a fixed depth of the fluid onto a photo diode which produced a voltage proportional to the laser power. This voltage was converted to dye concentration using a calibration curve obtained by measuring the voltage obtained when known concentrations of dye were placed in the laser path. Video recordings of the connections were made as the dye inherently produced visualization of the flow mixing between the IVC and SVC flows. 2.3 Data analysis The laser measurements of dye concentration, CRPA and CLPA in the RPA and LPA, respectively, and the blood flow rates, Q, were used to calculate the following two parameters where VRPA is the percentage of IVC dye (hepatic blood) passing through the RPA. This quantity represents the percentage of hepatic blood being delivered to the RPA. i.e. a value of 100% means that all the hepatic blood is going to the RPA. With normal cardiac anatomy, 60% of the circulation passing through the IVC, and full mixing of IVC and SVC blood in the right heart, VRPA would have a value equal to the percentage of cardiac output passing through the RPA. For a normal individual this is approximately 60% [21]. Crel RPA is the concentration of dye in the RPA relative to that entering the system through the IVC and is therefore a measure of how much the hepatic blood is being diluted, i.e. a value of 100% means the RPA blood contains the same amount of hepatic blood as does the IVC blood and is therefore undiluted. From the normal anatomy case mentioned directly above, Crel RPA would have a value of 60% in both lungs, since 60% of the total blood passing through the IVC is fully diluted by the 40% passing through the SVC. Although closely related, these two parameters represent significantly different quantities. For instance, there may be a high concentration of hepatic blood in the RPA, but if the RPA flow rate is very low, then the rate of delivery of hepatic blood to the right lung will also be low. Similarly, there may be a low concentration of hepatic blood in the RPA, but if the flow rate is high, then a sufficient quantity of hepatic blood may still be delivered to the right lung over time. At present it is unknown whether it is rate of delivery of hepatic blood to the lungs or the concentration of hepatic blood in the lungs that is important. The same quantities were also calculated in a similar manner for the flow into the LPA. Although experiments were only conducted with IVC offsets towards the LPA, because of the symmetry of our model, these same data were used to represent the results if the IVC were offset towards the RPA. Results for both offset directions are therefore presented although they represent the same data measurements analysed in a different manner. 3 Results 3.1 Hepatic blood flow distribution Figs. 1 and 2 show the percentage of hepatic blood being delivered to the RPA and LPA as a function of RPA flow rate and offset. For zero-diameter offset, i.e. a cross junction, the percentage of hepatic blood entering each pulmonary artery is linearly proportional to the percentage of blood entering that artery (Fig. 1). Therefore, as the RPA flow increases from 30 to 70%, the percentage of hepatic blood to that artery increases proportionally from 35 to 66%. Similarly, as the corresponding LPA flow decreases from 70 to 30%, the percentage of hepatic blood to the LPA decreases from 70 to 35%. Under ideal conditions (60% blood to the RPA) the hepatic delivery to each lung is very similar to that of a normal individual. Fig. 1 Open in new tabDownload slide Percentage of hepatic blood passing to the pulmonary arteries as a function of RPA flow rate. Zero offset between IVC and SVC. Solid symbols, RPA; open symbols, LPA; circles, measurements; squares, ideal normal values. Fig. 1 Open in new tabDownload slide Percentage of hepatic blood passing to the pulmonary arteries as a function of RPA flow rate. Zero offset between IVC and SVC. Solid symbols, RPA; open symbols, LPA; circles, measurements; squares, ideal normal values. Fig. 2 Open in new tabDownload slide Percentage of hepatic blood passing to the pulmonary arteries as a function of RPA flow rate. (a) IVC offset towards LPA. (b) IVC offset towards RPA. Solid symbols, RPA; open symbols, LPA; circles, one-diameter offset between IVC and SVC; triangles, two-diameter offset between IVC and SVC; squares, ideal normal values. Fig. 2 Open in new tabDownload slide Percentage of hepatic blood passing to the pulmonary arteries as a function of RPA flow rate. (a) IVC offset towards LPA. (b) IVC offset towards RPA. Solid symbols, RPA; open symbols, LPA; circles, one-diameter offset between IVC and SVC; triangles, two-diameter offset between IVC and SVC; squares, ideal normal values. If, however, the IVC is offset then a different mixing pattern emerges (Fig. 2). In these cases, the hepatic blood tends to be directed towards the nearest pulmonary artery. For example, if the IVC is offset towards the LPA, then the majority of hepatic blood is delivered to the LPA and the RPA suffers from a low hepatic blood delivery (Fig. 2). In extreme cases, where the flow split between the two pulmonary arteries is 70:30, less than 9% of hepatic blood is supplied to the lung with 30% of the flow. Comparing the results to a normal individual with a normal RPA flow rate of 60% of cardiac output, it can be seen that it is not possible to obtain normal hepatic blood distribution with an IVC offset of one diameter or more. There was no meaningful difference in the hepatic flow distribution between the one- and two-diameter offset models. 3.2 Hepatic blood concentration Figs. 3 and 4 show the relative concentration of hepatic blood in the RPA and LPA as a function of RPA flow rate and offset. For the zero offset case (Fig. 3), there was only a slight dependence of hepatic blood concentration on offset with the concentration in both pulmonary arteries closely approximating normal. The introduction of an IVC offset, however, produced a high concentration in the pulmonary artery closest to the IVC (Fig. 4). For example, when the IVC was offset towards the LPA, the concentration of hepatic blood in the LPA remained above 80% for all RPA flow rates and even reaches 100% if the flow in the LPA was small (Fig. 4). The corresponding concentration in the RPA on the other hand, never rose above 45% and dropped as low as 18% for low RPA flow. As above, there was no meaningful difference in the hepatic concentration distribution between the one and two diameter offset models. Fig. 3 Open in new tabDownload slide Concentration of hepatic blood passing to each pulmonary artery relative to that in the IVC as a function of RPA flow rate. Zero offset between IVC and SVC. Solid circles, RPA; open circles, LPA; square, ideal normal value. Fig. 3 Open in new tabDownload slide Concentration of hepatic blood passing to each pulmonary artery relative to that in the IVC as a function of RPA flow rate. Zero offset between IVC and SVC. Solid circles, RPA; open circles, LPA; square, ideal normal value. Fig. 4 Open in new tabDownload slide Concentration of hepatic blood passing to each pulmonary artery relative to that in the IVC as a function of RPA flow rate. One- (circles) and two-diameter (triangles) offset between IVC and SVC. (a) IVC offset towards LPA. (b) IVC offset towards RPA. Solid symbols, RPA; open symbols, LPA; square, ideal normal value. Fig. 4 Open in new tabDownload slide Concentration of hepatic blood passing to each pulmonary artery relative to that in the IVC as a function of RPA flow rate. One- (circles) and two-diameter (triangles) offset between IVC and SVC. (a) IVC offset towards LPA. (b) IVC offset towards RPA. Solid symbols, RPA; open symbols, LPA; square, ideal normal value. 3.3 Flow visualization For all the flow rates and geometric conditions, the separation and mixing between the clear SVC and dyed IVC flows could clearly be seen Figs. 5–7 . Although the flows were steady, the mixing was characterized by unsteady interactions due to the geometry of the connections and the interaction between the two opposing inlet flows. The unsteadiness was seen to derive from eddy production and motion which visually suggested that the mixing of the flows was dominated by bulk fluid motion (convection) rather than by molecular motion (diffusion). Fig. 5 Open in new tabDownload slide Effect of RPA flow on the flow visualization of the mixing between the IVC and SVC in the TCPC. Zero offset between IVC and SVC. Left, RPA flow=30% of total; right, RPA flow=70% of cardiac output. Fig. 5 Open in new tabDownload slide Effect of RPA flow on the flow visualization of the mixing between the IVC and SVC in the TCPC. Zero offset between IVC and SVC. Left, RPA flow=30% of total; right, RPA flow=70% of cardiac output. Fig. 6 Open in new tabDownload slide Effect of RPA flow on the flow visualization of the mixing between the IVC and SVC in the TCPC. One-diameter offset between IVC and SVC. Left, RPA flow=30% of total; right, RPA flow=70% of cardiac output. Fig. 6 Open in new tabDownload slide Effect of RPA flow on the flow visualization of the mixing between the IVC and SVC in the TCPC. One-diameter offset between IVC and SVC. Left, RPA flow=30% of total; right, RPA flow=70% of cardiac output. Fig. 7 Open in new tabDownload slide Effect of offset direction on the flow visualization of the mixing between the IVC and SVC in the TCPC. One-diameter offset between IVC and SVC. RPA flow=60% of cardiac output. Left, IVC offset towards the RPA; right, IVC offset towards the LPA. Fig. 7 Open in new tabDownload slide Effect of offset direction on the flow visualization of the mixing between the IVC and SVC in the TCPC. One-diameter offset between IVC and SVC. RPA flow=60% of cardiac output. Left, IVC offset towards the RPA; right, IVC offset towards the LPA. For zero-diameter offset (Fig. 5), flow visualization showed the vena cava flows meeting ‘head on’ before bifurcating into the pulmonary arteries. The interface between the two flows was shifted superiorly towards the SVC due to the larger IVC flow and was clearly seen at the pulmonary artery–vena cava anastomosis. One or two diameters away from this anastomosis, however, this interface was eradicated, indicating a rapid mixing. Little variation in the dye distribution with RPA flow rate could be visually discerned. A marked change in the mixing pattern was seen, however, if the IVC was offset by one diameter or more towards the LPA (Figs. 6 and 7). In these cases, the effect of RPA flow rate had a marked effect on the distribution of IVC flow. For a low RPA flow rate, very little of the IVC flow was seen to travel towards the RPA with the fluid in that limb remaining virtually dye free. The impingement of the IVC flow on the cranial wall of the LPA, however, produced an anti-clockwise vortex which assured that at least some of the IVC flow was directed towards the RPA. For a high RPA flow, there was a significant flow of IVC blood towards the RPA producing a coloration in the RPA flow. SVC flow could be seen to be drawn towards the RPA in a relatively smooth manner producing a clear interface between the dyed and undyed flow for some considerable distance downstream (Fig. 6). Fig. 7 shows how the dispersion of the dye changes depending on whether the IVC is offset towards the RPA or LPA under normal RPA flow conditions (60% of cardiac output). The visualization showed that when the IVC was offset towards the LPA, there was significant transport of dye towards the opposite RPA (Fig. 7, right). However, for the reverse case when the IVC was offset towards the RPA, there was visually very little transport of dye towards the opposite LPA (Fig. 7, left). There was no significant difference in the flow visualization between the one and two diameter offset models. 4 Discussion In recent years the TCPC has grown in popularity over the atrio-pulmonary connection. However, with the growth in patient numbers, the importance of maintaining hepatic blood supply to both lungs has become evident [14–20]. The growth in popularity of the TCPC has also resulted in a number of studies investigating the optimal geometric configuration for the TCPC junction. These have mainly focused on determining a hemodynamically efficient connection in terms of minimum energy or pressure loss, but have not considered whether these geometries are optimal or even sufficient in terms of delivering hepatic blood to each lung. This study aims at addressing this imbalance by quantifying the distribution of hepatic venous blood to each lung in the TCPC. The connection geometry chosen for this study was that used by Sharma et al. [5], who offset the IVC from the SVC by up to two vena cava diameters towards the RPA. This variation was used because intra-operatively it is possible to include an IVC offset into the TCPC although this offset is usually limited to around one diameter. Sharma's work showed that zero IVC offset caused energy loss due to the mixing of the two vena cava flows. The flow visualization presented in this paper (Fig. 5) confirms the presence of this mixing, showing the two flows impinging at the TCPC intersection and rapid dye dispersion in the adjoining arteries. The quantification of this zero-offset mixing presented here has demonstrated its efficiency, with the distribution of hepatic blood to each pulmonary artery matching the percentage flow rate in that limb, and with the relative concentration of hepatic blood in each pulmonary artery being almost 60% (Figs. 1 and 3). This same distribution and concentration of hepatic blood would occur in the normal heart, where the vena cava flows are most likely mixed in passing through the right atrium and ventricle. One can conclude, therefore, that zero IVC offset produces the most thorough distribution of hepatic blood to the lungs. However, the energy loss involved is relatively high. Due to the energy loss of the zero offset TCPC, Sharma advised that an offset of at least one vena cava diameter be included, as this halved the energy loss. The flow visualization presented here shows that this increase in efficiency is due to the a reduction in the mixing between the IVC and SVC flows (Figs. 6 and 7). If the majority of flow is directed towards the IVC offset, then the IVC and SVC flows are almost totally separated (Fig. 6, left; Fig. 7, left). In the most extreme case, less than 10% of IVC flow (hepatic flow) is delivered towards the opposite pulmonary artery with a relative hepatic blood concentration of less than 20%. For the opposite case, where the majority of flow is directed away from the IVC offset, the distribution of hepatic blood to the lungs is more even, with around 50% of hepatic blood passing to each lung at a minimum relative concentration of around 40%. The flow visualization shows, what is more, that this good hepatic blood distribution in the latter case is achieved with a low degree of mixing, (Fig. 7, right), and hence presumably a low energy loss. Offsetting the IVC by one diameter or more, therefore, produces a low energy loss but, depending on whether the offset is towards the lung of greatest or least flow, produces either a relatively even or uneven hepatic blood distribution. Two questions therefore arise: firstly, what is an adequate supply of hepatic blood, and secondly, in which direction should the IVC be offset? The first question is extremely difficult to answer at present because the hepatic blood factor responsible for proper lung function has not been identified. What is more, the problem of hepatic blood supply has been highlighted by postoperative complications [14–16] and long-term developments [17–19], suggesting that both the gross absence and long-term reduction of hepatic blood supply are important. From the results presented here, the lowest relative concentration of hepatic blood passing to any one lung was 18%, compared to 60% for normals (see Section 2). This reduction, although impossible to say for sure, does not seem to be large and may be sufficient to prevent the formation of PAVMs. Of more consequence, perhaps, is the left–right curving of the vena cava suggested by others as a means of further reducing energy loss [7,8]. This streamlining may be problematic as it could further reduce IVC/SVC mixing and consequently reduce hepatic blood delivery to one lung below the minimum found in these results. This highlights the contradiction between designing a TCPC connection for low energy loss and good hepatic blood distribution, and raises the question as to what is the most important factor in determining the shape of the TCPC connection. Is it energy loss or hepatic blood distribution? Unfortunately this question cannot be answered yet as not enough is known about the relationship between hepatic blood supply and AVM formation. These results suggest, however, that care should be taken in adding more streamlining to the TCPC connection as it may reduce hepatic blood supply to one lung below a healthy level. More work is required before a definite answer can be found. Studies on increasing flow efficiency through curving of the vena cava [7,8] raise important considerations with regard to the second question, namely, in which direction should the IVC be offset? Sharma et al. curved the IVC towards the RPA to match the greater IVC flow to the lung of greatest demand. This matching of flows and the resultant streamlining, however, may not be desirable in terms of hepatic blood distribution. In fact, the results presented here show that increased mixing is obtained if the IVC is offset towards the lung of lowest demand because this forces some of the IVC flow to bend into the high flow lung. These results indicate that a compromise solution between mixing and energy efficiency may be possibly if an IVC offset of around one IVC diameter without left–right curvature is incorporated into the TCPC connection. To be certain of these findings, however, more in vivo research needs to be performed relating TCPC geometry to lung function and energy efficiency. 4.1 Effect of offset size From these flow visualization and concentration measurements it is evident that there is a large change in flow dynamics if the IVC offset is changed from zero to one diameter. For larger offsets, however, i.e. from one to two diameters, there is very little change. The results suggest that further increases in offset would have little effect although at these offsets the in vitro model may differ significantly from in vivo pulmonary artery anatomy. These results are consistent with energy loss measurements which demonstrated an initial large reduction in energy loss if a one-diameter offset is used, but little further loss if the offset is increased [5]. These results demonstrate that the surgeon does not need to struggle to incorporate a large offset into the TCPC anastomosis and therefore make the geometric alterations suggested by in vitro work feasible in vivo. 4.2 Study limitations The conclusions drawn above are based on results from an idealized in vitro model which did not include geometric effects such as vessel taper, in-plane and out-of-plane curvature and branching. These geometric variations may be important because they may have an influence on the direction taken by the IVC and SVC blood streams as they pass through the anastomosis site. To estimate the effect of each of these variables we can note that the direction taken by the blood after entering the anastomosis will be highly dependent upon the direction of the blood as it enters. As the outlets to the TCPC are primarily orientated left to right, it follows that factors which influence the left to right motion of the blood on entering will be important. Therefore, from the list of geometric variables above, it is probable that only left to right curvature in the IVC and SVC will have an effect on our results. All other geometric variations, taper, out-of-plane curvature and branching will have only minor effects on IVC and SVC blood flow direction. These effects of left to right curvature have been discussed above. One other assumption used in our in vitro procedure was that of steady flow. This assumption was made because in vivo, the pumping action of the right ventricle is removed from the venous circulation and hence cannot generate right sided pulsatility. Variations to blood flow due to breathing are of a low frequency which we believe will have little effect on IVC/SVC mixing. 5 Conclusions This study has shown the importance of the TCPC geometry on the distribution of hepatic blood to the lungs. The dye method used in this study provided accurate results and has been shown to be a useful tool for this application in vitro. These results have confirmed through flow visualization the reduction in IVC/SVC mixing achieved by offsetting the IVC and SVC one diameter or more and as such reinforces the energy gains associated with this type of offset found by others. 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TI - Distribution of hepatic venous blood in the total cavo-pulmonary connection: an in vitro study
JF - European Journal of Cardio-Thoracic Surgery
DO - 10.1016/S1010-7940(00)00425-5
DA - 2000-06-01
UR - https://www.deepdyve.com/lp/oxford-university-press/distribution-of-hepatic-venous-blood-in-the-total-cavo-pulmonary-Ilt6FTA7aN
SP - 658
EP - 665
VL - 17
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DP - DeepDyve
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