Ann Thorac Surg 2004;77:1636-1641
© 2004 The Society of Thoracic Surgeons
Original article: cardiovascular
Evaluation of native valve-sparing aortic root reconstruction with direct imaging reimplantation or remodeling?
Kojiro Furukawa, MDa*,
Hitoshi Ohteki, MDb,
Zhi-Li Cao, MDa,
Yasushi Narita, CEb,
Yukio Okazaki, MDa,
Satoshi Ohtsubo, MDa,
Tsuyoshi Itoh, MDa
a Department of Thoracic and Cardiovascular Surgery, Saga Medical School, Saga, Japan
b Department of Cardiovascular Surgery, Saga Prefectural Hospital, Koseikan, Saga, Japan
Accepted for publication September 15, 2003.
* Address reprint requests to Dr Furukawa, Department of Thoracic and Cardiovascular Surgery, Saga Medical School, 5-1-1 Nabeshima, Saga City 840-8571, Japan.
e-mail: furukawa{at}bcm.tmc.edu
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Abstract
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BACKGROUND: Aortic root reimplantation and remodeling have been used to preserve the native aortic valve. However, direct observation of valve motions with these techniques has not been performed.
METHODS: Mongrel dogs were studied. The beating heart model was created using modified Tyrode's solution. Normal aortic valves and aortic valves preserved with the remodeling or reimplantation procedure were observed with an endoscope, and behavior was recorded on a high-speed video (200 frames/s). The aortic valve orifice area was measured at 11 data points per beat. A predictable maximum valve orifice area was defined as an area encircled by the three commissures. A ratio of each aortic valve orifice area to the predictable maximum valve orifice area was calculated. The control group, the reimplantation group, and the remodeling group were compared.
RESULTS: The preserved aortic valve with reimplantation showed bending and asymmetric motion. The ratio of aortic valve orifice area and predictable maximum valve orifice area in the reimplantation group was significantly smaller compared with the control and remodeling groups.
CONCLUSIONS: The opening and closing behavior of the aortic valve preserved with the reimplantation procedure was impaired. It was speculated that the remodeling procedure may preserve more physiologic root function compared with the reimplantation procedure.
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Introduction
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Until recently, the best surgical treatment for patients with aortic regurgitation, associated with annulo-aortic ectasia or an ascending aortic aneurysm, was replacement of the aortic root with a composite valved conduit [13]. However, aortic regurgitation with an ascending or aortic root aneurysm is mainly due to dilatation of the sinotubular junction [4], distortion of one or more of the sinuses of Valsalva, annulo-aortic ectasia, or a combination of these problems. Currently, aortic root reimplantation [5] and remodeling [6] are performed clinically to preserve the native aortic valve using this rationale. However, the aortic root is a dynamic unit that allows easy opening and closing and shares stress for the valve leaflets [710]. When the aortic root is replaced with artificial material the normal aortic root condition may be lost, with impaired preserved aortic valve opening and closing characteristics. These movements could have important implications for the durability of the repair and possibly left ventricular function, and thus long-term results. Although the short-term and long-term outcomes of these operations have been good, which operation yields results that are more physiologic and more durable has not been well established. Comparative studies, including clinical results [11, 12] and indirect observation of opening and closing of the aortic valve using echocardiography [13], were reported. However, direct observation of valve motions with the two techniques was not performed. Therefore, we observed the behavior of the aortic valve after the remodeling and reimplantation procedures with direct imaging using cardiac endoscopy, and investigated which procedure is more physiologic. In the current clinical situation, the original reimplantation procedure, called "David-I" [14], is rarely performed. However, we used the original reimplantation procedure in this study because we wanted to clearly analyze the basic conceptual differences between the remodeling and reimplantation procedures.
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Material and methods
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General preparation
All animals were treated in accordance with the Saga Medical School's guidelines for animal experimentation. A total of 18 adult mongrel dogs (body weight, 15 to 25 kg) were studied. The dogs were anesthetized with ketamine chloride (10 mg/kg, intramuscular injection), thiamylal sodium (50 mg, intravenous injection), and pancuronium bromide (3 mg, intravenous injection). The animals were intubated and placed on a Harvard ventilator (Shinano Manufacture, Tokyo, Japan). Ketamine chloride (5 to 10 mg/kg) was added every 20 to 30 minutes. The electrocardiogram was derived from limb leads. A transverse bilateral thoracotomy, entering through the fourth intercostal space, was performed. The heart, ascending aorta, aortic arch, descending aorta, and pulmonary veins were exposed. After systemic heparinization (3 mg/kg, intravenous injection), a cannula for cardioplegia (4 mm, inner diameter) was introduced into the innominate artery, and a perfusion cannula was introduced into the femoral artery. After occlusion of the superior vena cava, inferior vena cava, pulmonary veins, and descending aorta, 20 mL/kg of cardioplegic solution, cooled to a temperature of 0°C to 10°C (glucose 50 g/L, regular insulin 20 U/L, potassium 20 mEq/L, sodium bicarbonate 2.3 g/L, d-mannitol 4 g/L, and vitriolated magnesium 2 g/L), was injected into the coronary arteries through the cannula. Cardiac arrest was obtained. Topical cooling was achieved with iced saline solution. Subsequently, the heart and thoracic aorta were extracted en bloc.
Control group
The control group consisted of five dogs. After the heart and thoracic aorta were extracted, the opening to the left atrium was closed. Then the heart and thoracic aorta were returned to the thoracic cavity and the ascending aortas were anastomosed. A cannula (3 mm, inner diameter) was introduced into the left atrium through the left atrial appendage. Warmed (37°C) cadioplegic solution was injected into the coronary arteries through the cannula in the innominate artery. The beating heart model was then created. Oxygenated and warmed (37°C) modified Tyrode's solution (NaCl 6.0 mg/L, KCl 0.35 mg/L, MgCl26H2O 0.1 mg/L, CaCl22H2O 0.3 mg/L, NaH2PO42H2O 0.05 mg/L, NaHCO3 3.0 mg/L, glucose 2.0 mg/L) was infused via the femoral artery at a perfusion pressure of 40 mm Hg and via the left atrium at a pressure of 15 to 20 cm H2O. The electrocardiogram and aortic pressure were monitored simultaneously. Aortic pressure was monitored with a fiberoptic pressure manometer (Camino model 110-4, Camino Laboratories, San Diego, CA, USA). A 6-mm diameter fiberscope (Olympus BF type 10, Olympus Corp, Tokyo, Japan) was inserted into the aorta through the left subclavian artery. The aortic valve was observed endoscopically. The observations were recorded with a high-speed (200 frames/s) video system (NAC, model MHS-200, NAC Inc, Tokyo, Japan). The dopamine added to the Tyrode's solution was to enhance contractility.
Remodeling and reimplantation groups
The remodeling and reimplantation groups consisted of seven and six dogs, respectively. Autologous blood (1 L) was extracted through the right atrium before arresting the heart. The autologous blood was used for reperfusion. After the heart was arrested, continuous retrograde cardioplegia (150 mL/min at 60 cm H2O) was started through a cannula (Research Medical Inc, Midvale, Utah, USA) placed in the coronary sinus. Every 30 minutes, selective antegrade cardioplegia was induced in the left coronary artery (100 mL) and the right coronary artery (50 mL) using a selective coronary perfusion catheter (Research Medical Inc). The techniques for remodeling and reimplantation of the aortic root have been described in detail previously [5, 6]. The extracted heart and aorta were placed in normal saline on ice. First, the ascending aorta was incised, and the aortic tissue including the sinuses of Valsalva were excised to within 2 mm of the aortic annulus. Both coronary arteries were trimmed with buttons of tissue. The diameter of the left ventricular outflow tracts (LVOT) for all animals was in the range of 18 to 20 mm. Collagen-impregnated Dacron grafts (diameter, same size for the remodeling group, 2-mm larger for the reimplantation group) were used for root reconstruction. In the remodeling group, the commissures were attached to the Dacron graft. Three separate extensions for replacement of the three sinuses were fashioned in the proximal end of the graft. The extensions were fixed to the aortic annulus with continuous 5-0 polypropylene sutures (remodeling group). In the reimplantation group, six interrupted horizontal mattress sutures of 3-0 braided polyester, reinforced with a spaghetti, were passed from inside to outside the left ventricular outflow tract, immediately below the aortic valve, and these sutures were ligated. Next, the remnant of the arterial wall was sutured to the graft with a continuous 5-0 polypropylene suture (reimplantation group). The coronary arteries were reconstructed using the Carrel patch technique with continuous 5-0 polypropylene sutures. The opened left atrium was closed. Finally, the heart and thoracic aorta were returned to the thoracic cavity, and the graft and ascending aorta were anastomosed. After warm cardioplegia (20 mL/kg, 37°C), warm and oxygenated autologous blood (1 L, 37°C) was injected into the coronary arteries for reperfusion. The beating heart model was created in the same manner for the control group. The observations and recordings of the aortic valve were also performed in the same manner.
Data analysis
Under stable hemodynamic conditions, the aortic valve orifice area (AVOA) was measured using computer tracings (Mac SCOPE, Mitani Corporation, Chiba, Japan) at 11 data points during the systolic phase of the cardiac cycle. The 11 points were divided equally in time. The initial data point was recorded as point 0 at the beginning of valve opening. The final data point was recorded as point 10 at valve closure. In this study, predictable maximum valve orifice area (p-MVOA) was defined as an area encircled by three commissures (Fig 1).
The ratio of each AVOA to the p-MVOA was calculated, and the ratios were averaged over three heartbeats.

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Fig 1. p-MVOA, defined as an area encircled by three commissures, A, B, and C. (p-MVOA = predictable maximum valve orifice area.)
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Statistics
All values were expressed as the mean ± the standard deviation. The unpaired t test was performed for comparison among the control group, the remodeling group, and the reimplantation group. A value of p less than 0.05 was considered statistically significant.
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Results
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Hemodynamics
In the control group, the heart rate, aortic systolic pressure, and aortic diastolic pressure were 126 ± 9.9 beats/min, 68.8 ± 13.2 mm Hg, and 45.6 ± 13.8 mm Hg, respectively. In the remodeling group, they were 114.3 ± 24.4 beats/min, 61.2 ± 8.4 mm Hg, and 34.5 ± 10.0 mm Hg, respectively. In the reimplantation group, they were 114.8 ± 33.9 beats/min, 62.3 ± 16.5 mm Hg, and 39.3 ± 17.9 mm Hg, respectively. There were no significant differences among the three groups.
Direct imaging
The aortic valve opened and closed flexibly and symmetrically and showed adequate opening in the control group (Fig 2).
In the remodeling group, the preserved aortic valve also opened and closed flexibly and symmetrically and preserved an AVOA (Fig 3).
Folding or distortion of the leaflets in the open position was not observed, and the appearance of free margins of the leaflets was kept straightened during the opening phase. In the reimplantation group, the preserved aortic valve showed bending and asymmetric motion. Also, in that group, wrinkling leaflets approached the prosthetic grafts (Fig 4).
Ratios of each AVOA to the p-MVOA (%) in the control group at points 1 through 9 were as follows: 5.7 ± 2.8, 29.9 ± 18.2, 56.5 ± 5.5, 53.0 ± 8.3, 46.1 ± 6.9, 40.9 ± 4.5, 32.9 ± 3.2, 21.2 ± 7.0, and 7.8 ± 6.0, respectively. Also, ratios in the remodeling group at the same points were as follows: 3.7 ± 1.7, 16.4 ± 5.4, 38.1 ± 6.5, 47.1 ± 7.9, 47.7 ± 6.6, 42.7 ± 7.3, 34.0 ± 7.2, 26.5 ± 4.4, and 13.0 ± 4.3, respectively. Also, ratios in the reimplantation group at the same points were as follows: 5.8 ± 4.9, 22.6 ± 8.6, 30.0 ± 6.8, 30.1 ± 7.7, 27.4 ± 8.3, 25.0 ± 7.7, 21.7 ± 6.0, 16.2 ± 4.7, and 6.2 ± 2.0, respectively. The ratios of the control group and the remodeling group from points 4 to 9 were significantly larger than the rartios of the reimplantation group (p < 0.05) (Fig 5).

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Fig 5. Change in the ratios of each valve orifice area to the p-MVOA in the control, remodeling, and reimplantation groups. (p-MVOA = predictable maximum valve orifice area.)
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Comment
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The surgical approach to aortic root aneurysm and(or) dissection is still controversial. Because aortic disease leaves the aortic valve cusps largely unaffected, valve-preserving operations, using a reimplantation [6] or a remodeling [5] procedure, have been developed and used. Studies of clinical results comparing these two procedures have been reported [11, 12]. However, which procedure is better in the clinical setting is still not well established. Concerning preserved valve motions after these procedures, few studies exist. In our investigations, only one clinical study using echocardiography was reported [13]. Therefore, we investigated valve motions after two procedures directly using endoscopy after these two procedures.
The valve configurations of the remodeling and reimplantation groups were quite different in this study. In the remodeling group, the preserved aortic valve opened and closed flexibly and symmetrically, similar to what was seen in the control group. Also, the free margins of the preserved valve straightened through one cardiac cycle. In contrast, in the reimplantation group, the preserved aortic valve showed buckling and asymmetric motion. In theory (Fig 6),
the radius of the aortic root at the closure of the aortic valve is defined as r, and the length of the free margin of each valvular leaflet at the opening is 2r. Therefore, if each free margin of a valvular leaflet straightens at the opening, the diameter of the aortic root is 2.3r. If the aortic root loses its distensibility, each free margin is redundant [9]. In this study, we did not measure the change in size of the aortic root. However, the free margins of the leaflets of the preserved valves straightened upon opening after the remodeling procedure, and this suggests that the distensibility of the aortic root was preserved. The resulting aortic root that crowds the base of the leaflets, and commissures after the reimplantation procedure, may not possess distensibility.

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Fig 6. Theory about the aortic root distensibility and length of aortic valve free margins. (r = radius.)
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The configuration of the aortic valve in the ejection phase of the left ventricle is important for minimizing the stress on the leaflet surfaces, flexion stress at the center of the leaflet, and fatigue strain on the leaflet [10]. In the remodeling group, folding of the leaflets in the open position was not recognized. With respect to the durability of the preserved aortic valve, the valve configuration in the open position after remodeling was excellent. In the preserved valves after the reimplantation procedure, the leaflet free edges looked blurry, and there were many wrinkles in the leaflet. Therefore, the valves in the reimplantation group might receive more fatigue and flexion stress than in the remodeling group.
The sinus adapts, in diastole, to the new stress condition in the leaflet by reducing its radius of circumferential curvature. This stress sharing is also important for the longevity of the preserved aortic valve [7]. As a result, the stress on the valve in the diastolic phase should be shared between the artificial sinus and the leaflets. This occurs with stress transmission to the interleaflet triangles [7]. This stress sharing between the sinuses and leaflets could be possible under a flexible aortic root. From this study, loss of the aortic root compliance after reimplantation might cause valve dysfunction and stress overload, and thus may unfavorably influence preserved leaflet longevity [15].
Leyh and colleagues reported nearly normal opening and closing behavior of the preserved aortic valve after a remodeling procedure with echocardiography [13]. Our observations confirmed their results with direct observation.
The aortic valve orifice area in the reimplantation group was limited, significantly, compared with that in the control and remodeling groups. The limit of valve opening may not induce significant hemodynamic deterioration. Also, the maximum systolic gradients measured in preserved valves using both techniques were essentially physiologic in clinical situations [11]. However, it remains to be investigated whether the hemodynamic performance of these valves will also be physiologic under conditions of exercise.
Recently, early failures of preserved aortic valve were reported [1619]. However, we think that long-term failure has more to do with the quality of the cusps, initial accuracy of the geometric reconstruction concerning cusp coaptation [16], and contact of the cusp on the Dacron tube [19] than the method of reconstruction. Indeed, successful short-term and long-term outcomes using various reconstructive methods have been reported [11, 12, 16, 20]. Some surgeons might prefer the reimplantation procedure to remodeling because of predictability, bleeding, and the possibility of annular dilatation, especially in Marfan syndrome patients [14, 21]. The original reimplantation procedure, David-I [14], has been modified with neosinuses, a neosinotubular junction [14, 21, 22], and using a new "sinus graft" [23]. From our study, these modifications may enhance the function and durability of the aortic valve. de Oliveira and David [21] reported superior durability with reimplantation rather than remodeling. Aortic valve-sparing operations are complex procedures, and numerous variables likely play a role in their outcomes. We think the remodeling procedure has theoretical advantages, except for possible annular dilatation. Therefore, longer term and sophisticated clinical comparison studies will be necessary to prove our hypothesis.
This study has several limitations. One was the use of the isolated heart model, which did not provide a physiologic preload and afterload. In this study, no cardiac outputs were measured. The degree of opening of the aortic valve is dependent on the stroke volume and systolic ejection time. However, the three groups were compared under the same hemodynamic conditions. Another limitation was that the circulation was performed with transparent Tyrode's solution without hemoglobin. This was essential for direct observation by endoscopy. However, this may have resulted in changes in the contractility of the left ventricle and weakened its ejection force. These unnatural situations likely caused a low aortic pressure. This study was performed on dogs with a normal aortic root, not ill patients. In the clinical setting, aortic valve-sparing operations are performed on patients with aortic root aneurysm, and the relationships between the cusps, annulus, aortic sinuses, and sinotubular junction are quite different from those of the normal aortic root. However, these operations should be performed on the basis of a normal or nearly normal leaflet, and our experimental remodeling or reimplantation procedures are comparable to the clinical situation after root reconstruction using a prosthetic vascular graft. Therefore, we think our experimental model is proper for comparing these operations.
In conclusion, the opening and closing behavior of the aortic valve preserved by the reimplantation procedure was impaired. In addition, it was speculated that the remodeling procedure may preserve more physiologic aortic root function compared to the reimplantation procedure.
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Acknowledgments
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The authors wish to thank Shinichi Yasutake for his technical assistance.
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