In the mid-1990s, cardiac surgeons became increasingly interested in the development of minimally invasive surgery for patients with ischemic and valvular heart disease. Some efforts centered on exposing the heart for coronary artery bypass graft and valve surgery through smaller incisions while others focused on eliminating the need for cardiopulmonary bypass when performing coronary artery bypass surgery. Specialized instruments and devices were developed that enhanced surgical exposure, cannulation for cardiopulmonary bypass, occlusion of the ascending aorta for antegrade cardioplegic arrest, bypassing the coronary arteries, and repairing or replacing heart valves.
The limiting factor in the development of a minimally invasive surgical procedure to treat patients with atrial fibrillation (AF) was the obvious risk of trying to perform all of the atrial lesions of the cut-and-sew Maze-III procedure through a small thoracotomy rather than via the traditional median sternotomy. For example, the left atrial appendage (LAA) cannot be amputated safely through a small right anterolateral thoracotomy. In the cut-and-sew Maze-III procedure, the LAA was inverted into the left atrium (LA) and amputated at its base with a knife (see Fig. 12.32 ). LAA amputation typically results in the transection of a small atrial branch of the circumflex coronary artery located at the extreme lateral aspect of the base of the LAA. Control of this small arterial bleeder is simple through a median sternotomy but extremely difficult through a small right thoracotomy. We addressed this problem in the development of a minimally invasive Maze-III procedure by leaving the LAA intact and closing it endocardially. Another problem was potential bleeding from the multiple atrial incisions that were foundational to the success of the cut-and-sew Maze-III procedure. This barrier was overcome by replacing the cut-and-sew Maze-III incisions with linear cryolesions . Unfortunately, in the mid-1990s, there were no commercially available linear cryoprobes, so to create one, we removed the insulation from the shaft of a 2-mm cryoprobe previously designed for us by Frigitronics, Inc. to treat patients with atrioventricular node reentry tachycardia (AVNRT). This provided us with an excellent linear cryoprobe capable of creating all of the lesions of the Maze-III procedure ( Fig. 14.1 ). We modified two such cryoprobes to freeze tissue from both sides simultaneously, which was made possible by the newly available (at the time) dual-channel Frigitronics console. The ability to freeze both sides of the tissue simultaneously simplified isolation of the pulmonary veins as well as creation of the atrial septal lesion. Fortunately, commercial disposable linear cryoprobes are now readily available and far superior to our homemade non-disposable probes, making it much easier to create the Maze-III cryolesions through a small chest incision (see Chapter 16 ).
This non-disposable cryoprobe was designed with a 2 mm active tip for the treatment of atrioventricular node reentry tachycardia (AVNRT). Because there were no commercially available linear cryoprobes at the time, we removed the insulation on the shaft of this cryoprobe to expose a 5-cm segment that could be used as a linear cryoprobe in the minimally invasive CryoMaze-III procedure. Two such “linear cryoprobes” were prepared in this manner so that they could be placed on both sides of the pulmonary veins for pulmonary vein isolation and on both sides of the atrial septum to create the atrial septal lesion. We called this technique a “floating cryoprobe clamp,” which we used routinely to perform minimally invasive CryoMaze-III procedures after 1996.
Principles of Creating a Permanent Myocardial Cryolesion
Heat-based energy sources such as radiofrequency, microwave, laser, and high-intensity focused ultrasound kill myocardial cells by heating them to a critical lethal temperature of 61°C. However, cryothermia creates lesions by withdrawing heat from the myocardium to freeze the cells to a critical lethal temperature. When performed properly, both heat-based lesions and cryosurgical lesions are as effective as surgical incisions in blocking electrical conduction in the atrium.
Cryobiology That Affects the Creation of a Cryolesion
Cryosurgery kills myocardial cells during both the freezing and thawing phases of the cryolesion. The slower the frozen tissue thaws, the greater the volume of cell death, , and repeating the freeze–thaw cycle increases the size of the ultimate cryolesion. Cell death during the freezing phase is caused by direct cellular injury from the formation of intracellular and extracellular ice crystals that destroy the cell membranes. During the thawing phase, cell death occurs because of microvascular stasis that develops around the edges of the cryolesion.
Plant cells and pancreatic cells have a critical lethal temperature of −20°C at which they literally “explode” with complete disruption of the cell wall and the escape of cellular contents into the surrounding intercellular tissues ( Fig. 14.2 ). However, the seminal studies of John G. Baust, John M. Baust, and Kristi K. Snyder documented that the critical lethal temperature of myocardial cells is–30°C. Sudden myocardial cell death that occurs at–30°C does not depend on the time the myocardial cell is kept at that temperature, only that the cell reaches that temperature. In the sequential images of a pancreatic islet cell being frozen that are shown in Fig. 14.2 (from a video by John G. Baust), sudden death occurred 4.2 seconds after the cell temperature reached–19.94°C. Likewise, our independent experimental studies confirmed that myocardial cells die within 5 seconds of reaching–30°C ( Fig. 14.3 ).
Sequential photomicrographs from a video of a single pancreatic cell while being exposed to cryothermia. In each frame, the temperature of the cell and surrounding interstitial tissue is continuously displayed in the left upper portion of the frame, and the duration of the cryothermia application (freeze duration in seconds) is continuously displayed in the right upper portion of the frame. (A) After 10.5 seconds of cryothermia application, the tissue temperature is–1.51°C, and there is no evidence of either cellular or extracellular ice formation. (B) Extracellular and intracellular ice form almost simultaneously, though ice appears slightly earlier in the extracellular tissue. After 15.9 seconds of freezing, the tissue temperature is–5.4°C and intracellular and extracellular ice is apparent. (C). After 38.7 seconds of freezing, the tissue temperature is–19.94°C. Ice is prominent in both the cellular and extracellular tissues, and the cell wall is still intact. (D) 4.2 seconds later (42.9 seconds) at the same temperature of–19.94°C, the cell wall suddenly disrupts, and cellular contents are exposed to the extracellular tissues. The small round circles in this frame are fragments of the cell wall that have rolled into a ball much like a window shade suddenly wrapping up on itself. This is the histological hallmark of irreversible cellular injury. Whereas the lethal cryothermic temperature for this pancreatic cell and several other animal and plant cells is–20°C, the lethal cryothermic temperature for myocardial cells is–30°C.
(Courtesy Dr. JG Baust).
Correlation of myocardial cell damage with tissue temperature and duration of cryothermia exposure (axis in seconds). These are five examples of continuous temperature curves recorded from five separate tissue sites where the myocardium was monitored continuously by thermocouples. Note that myocardial cells survived at sites that were exposed to tissue temperatures below–10°C for 10 seconds and below–20°C for 22 seconds (blue shading). However, if the myocardial temperature reached–30°C (red shading), even for only 5 seconds, the myocardial cells did not survive.
(Reproduced from Cox JL, Malaisrie C, Churyla A, et al. Cryosurgery for atrial fibrillation: physiologic basis for creating optimal cryolesions. Ann Thorac Surg. 2021;112:354–362.)
Although the freezing portion of the freeze–thaw cycle alone can kill myocardial cells if they reach the critical lethal temperature of −30°C during the freeze, it is often impossible to reach that temperature in all of the targeted tissue because of the “heat sink” effect of the surrounding tissues (see Chapter 20 ). This limitation results in a non-transmural cryolesion and procedural failure. The primary effect of prolonging the application of a cryoprobe is to increase the number of cells that reach–30°C, thereby resulting in a larger permanent cryolesion. Thus, the myocardial temperature scale pertinent to creating permanent lesions of conduction in the heart ranges from the critical lethal temperature of 61°C for heat-based ablative energies to the critical lethal termperature of–30°C for cryothermia-based ablative energy ( Fig. 14.4 ).
Temperature scale for the critical lethal temperature of myocardial cells using heat-based ablation devices such as radiofrequency catheters and surgical devices (61°C) to the critical lethal temperature of myocardial cells using cryothermia-based ablation devices such as cryoballoon catheters and surgical cryoprobes (–30°C).
How to Create a Permanent Contiguous, Uniformly Transmural Cryolesion
Perhaps the most misunderstood aspect of cryosurgery for cardiac arrhythmias is the so-called “2-minute rule.” The traditional application of cryothermia for “2 minutes” has been variously interpreted as being:
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Total cryoprobe application time of 2 minutes ( Fig. 14.5 , left panel )
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Applying a cryoprobe for a predetermined 2-minute period of time ignores the effects of varying clinical circumstances and is likely to fail as often as it succeeds. The temperature of the cryoprobe, the temperature of the targeted myocardium, the thickness of the atrial wall, and the heat-sink effect of cavitary blood all impact the size, depth, and integrity of the ultimate cryolesion. These factors can combine to make a simple 2-minute application of cryothermia completely ineffective.
Fig. 14.5 This sequence of intraoperative photographs demonstrates how to apply the traditional “2-minute rule” of cryothermia exposure correctly to ensure that a permanent contiguous, transmural cryolesion will invariably be created. These operative photos were chosen for illustration because they allow the surgeon to visualize the creation of a transmural iceball on the opposite surface of the atrium (epicardium) from the surface of cryothermia application (endocardium). (A) Initiation of cryothermia. A stab wound was made inside a pursestring suture (secured by a Rumel tourniquet) so that a linear cryoprobe could be introduced into the right atrium and placed against the endocardial surface in the location of the desired linear cryolesion. The desired cryolesion extends from the pursestring suture to the tip of the cryoprobe. If cryothermia is initiated immediately after positioning the cryoprobe and continued for 2 minutes, much of the frozen myocardium in the desired linear lesion site will never reach the critical lethal temperature of–30°C, and the cryolesion will fail in a high percentage of patients. (B) First appearance of iceball. After the initiation of cryothermia, an epicardial iceball will appear shortly, almost always at the tip of the cryoprobe. This indicates that the epicardial surface at the site of the iceball has reached a temperature of 0°C, which is a sublethal temperature (see text). Moreover, note that the majority of the atrial muscle in the desired lesion site between the pursestring suture and the iceball has not yet reached even this sublethal temperature of 0°C as evidenced by the absence of an iceball in this segment of atrial wall. Therefore, if cryothermia is applied for an additional 2 minutes beginning at this stage, much of the frozen myocardium in the desired linear lesion site will recover, and the cryolesion will fail in a high percentage of patients. (C) Iceball throughout the length of the desired lesion. To ensure that a permanent linear cryolesion will be created in the desired location, it is essential that the 2-minute “counting period” for application of cryothermia begin only after the epicardial iceball has formed completely throughout the length of the desired lesion . This is the proper way to use the traditional “2-minute rule” for creating atrial cryolesions, and it has proven to be extremely successful over the past 4 decades.
(Reproduced from Cox JL, Malaisrie C, Churyla A, et al. Cryosurgery for atrial fibrillation: physiologic basis for creating optimal cryolesions. Ann Thorac Surg. 2021;112:354–362.)
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Two minutes from the first appearance of an iceball on the myocardial surface opposite the site of cryoprobe application ( Fig. 14.5 , middle panel )
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Likewise, applying a cryoprobe for 2 minutes after the first appearance of an iceball on the surface opposite the cryoprobe will not reliably result in an adequate permanent cryolesion because the myocardial fibers not included in the iceball remain above 0°, a non-lethal temperature.
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Two minutes from the time an “iceball” is created throughout the length of the desired lesion ( Fig. 14.5 , right panel )
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The iceball must first be allowed to form throughout the length of the desired lesion . The surface iceball forms when the tissue temperature reaches 0°C as water vapor from the immediately adjacent air turns into ice crystals. However as noted earlier, 0°C is not a lethal temperature for myocardial cells, so despite the tissue being visibly frozen transmurally, it will recover if the lowest tissue temperature attained is 0°C ( Fig. 14.6 ).
Fig. 14.6 Left upper panel, This diagram illustrates why the appearance of an iceball on the epicardial surface opposite an endocardial cryoprobe is not the time to stop freezing the myocardium. An iceball forms when the epicardial surface temperature reaches 0°C because it is the temperature at which water vapor in the adjacent air forms ice crystals. Even when the iceball has formed along the entire length of the desired lesion, the subepicardial temperature will still be well above the critical lethal temperature of–30°C because there is always a temperature gradient from the site nearest the cryoprobe to the site farthest away from the cryoprobe. Therefore, if freezing is stopped at this point, the subepicardial myocardium will recover, the permanent cryolesion will be nontransmural, and the ablation procedure will fail. The same principles and limitations are operative when freezing from the epicardial surface and when using cryoprobes that cool to lower temperatures. After an iceball has formed throughout the length of the desired lesion , an additional 2 minutes of freezing should be applied. Right lower panel, During the additional critical 2 minutes of freezing, the temperature of the tissue located farther away from the cryoprobe will continue to decrease until eventually, the tissue at the opposite surface of the cryoprobe will reach the critical lethal temperature of–30°C, although there will still be a temperature gradient within the frozen tissue. However, when the subepicardium (in this case) reaches–30°C, the eventual permanent lesion will be permanently transmural.
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One should continue to freeze the tissue for an additional 2 minutes after the iceball has formed throughout the length of the desired lesion to be certain that all of the myocardial cells of the desired lesion have been destroyed. This probably represents a bit of “overkill” but is based on studies that were performed specifically to determine how long it takes for cryoablated tissue to decrease from 0°C (iceball formation) to–30°C (cell death) ( Fig. 14.7 ). As mentioned earlier, this time varies depending on a variety of factors, but under experimental conditions, it was usually around 30 seconds. To be certain that every cryolesion is created perfectly under all conditions, we recommend that cryoablation be continued for 2 minutes after the formation of an iceball along the entire length of the desired lesion site. When the opposite side of the atrial wall cannot be seen, we routinely perform 3-minute cryloesions, the 3 minutes being from the time the cryothermia is initiated. If the atrial wall is thicker than normal, we occasionally freeze along the same lesion line on both sides of the atrial wall to be certain of permanent transmurality.
Temporal relationship between iceball formation and myocardial cell death. These are continuous myocardial temperature curves recorded from the tissue surface opposite the cryoprobe in tissue slabs that were of varying thickness. Because iceballs form at 0°C and the critical lethal temperature for myocardial cells is-30°C, the additional freeze time needed for permanent transmurality after the appearance of a complete iceball can be determined. In normothermic tissue, the time from iceball formation to cell death is approximately 30 seconds (red line). Thus, freezing for an additional 2 minutes after the formation of a complete iceball opposite the cryoprobe is more than adequate to create a permanent transmural cryolesion.
Surgical Technique of the Minimally Invasive CryoMaze-III Procedure
The cannulation and exposure techniques for performing on-pump minimally invasive procedures vary widely and have evolved substantially since the mid-1990s because of cumulative surgical experience and the evolution of specifically designed minimally invasive tools and devices. Therefore, this aspect of the surgical technique of the minimally invasive CryoMaze-III procedure is not discussed here. My personal preference is to expose the heart through an anterolateral mini-thoracotomy in the right fourth intercostal space ( Fig. 14.8 ), but others prefer a more lateral mini-thoracotomy. We originally used the Heartport system to occlude the ascending aorta to deliver antegrade cardioplegia but later switched to the Chitwood clamp because of its ease of application and lower cost. The specific technique of the minimally invasive CryoMaze-III procedure that is currently used is discussed in more detail in Chapter 28 by Dr. Niv Ad. In addition, in Chapters 15 and 27 , Dr. Patrick McCarthy describes his technique for performing all of the lesions of the CryoMaze-III procedure when ablating concomitant AF associated with other cardiac surgery by applying only three freezes in the LA and three freezes in the right atrium (RA). His recent modification of the CryoMaze-III procedure decreases the aortic cross-clamp time for AF ablation in patients undergoing coronary artery and/or valve surgery.
Minimally invasive CryoMaze-III procedure: patient position and exposure. In the initial minimally invasive CryoMaze-III procedure, the heart is exposed through an anterolateral mini-thoracotomy in the right fourth intercostal space (ICS). Some surgeons prefer a more lateral mini-thoracotomy. The right femoral artery is cannulated for arterial inflow, though other arterial cannulation sites can be used. The right femoral vein is cannulated for venous return from the inferior vena cava. The superior vena cava can be cannulated directly with a right-angle cannula through a separate small stab wound below the mini-thoracotomy or via the right jugular vein.
Right Atrial Lesions
Creation of Right Atrial Lesions Off-Pump
The right atrial lesions of the minimally invasive CryoMaze-III procedure can be created entirely through two pursestring sutures in the RA without cardiopulmonary bypass if so desired. The first step is to place a pursestring suture approximately two-thirds of the way down from the superior vena cava SVC to the inferior vena cava (IVC) immediately anterior to the crista terminalis and secure it with a Rumel tourniquet. A linear cryoprobe is then inserted through the pursestring suture and passed well into the SVC, keeping it as lateral as possible to avoid directly freezing the anatomic sinoatrial (SA) node ( Fig. 14.9 ). The cryoprobe is placed inside the RA and lifted upward to assure good contact with the endocardial surface. In addition, lifting the probe against the endocardium assures that there is no blood between the probe and the endocardium. Another advantage of this technique is that it allows visual confirmation of the epicardial iceball developing along the desired lesion. After the SVC lesion is completed as described, the probe is positioned into the IVC to complete the SVC–IVC intercaval lesion ( Fig. 14.10 ). After this lesion is completed, the cryoprobe is removed, and the first pursestring suture is tied down.
