Although many procedures have been described for surgical revascularization in moyamoya disease, the combined direct and indirect bypass procedure of superficial temporal artery (STA) to middle cerebral artery (MCA) bypass with encephalo-duro-arterio-synangiosis (EDAS) is a staple among these. The operation provides complementary benefits of immediate revascularization through direct bypass, as well as longer term collateral formation through indirect EDAS. The procedure is indicated for patients with symptomatic moyamoya with adequate donor and recipient vessels. The key elements and surgical steps of this operation are outlined in this chapter and include harvesting and preparation of the frontal and parietal branch of the STA, craniotomy with cruciate dural opening sparing major branches of the middle meningeal artery, selection and preparation of the recipient cortical MCA branch, performance of direct STA-MCA anastomosis, and technique for encephalo-duro and encephalo-arterio-synangiosis. The use of intraoperative blood flow measurements in performing direct bypass is also described: measurement of the STA cut flow prior to anastomosis and bypass flow following anastomosis allows determination of the bypass cut flow index (i.e., bypass flow/cut flow), which serves as a useful indicator of bypass function. Important elements of perioperative management are also reviewed including preoperative hydration, avoidance of hypotension and hypocarbia intraoperatively, and careful blood pressure control post- operatively.
Keywords: blood flow, bypass, middle cerebral artery, moyamoya, superficial temporal artery, surgery
The general approach of performing combined direct and indirect revascularization evolved from observations of moyamoya disease (MMD) cases in the 1980s where indirect procedures, especially encephalo-duro-arterio-synangiosis (EDAS) alone, failed to provide sufficient collaterals.1-3 Descriptions of combining direct superficial temporal artery (STA)-middle cerebral artery (MCA) bypass with various indirect procedures including EDAS, encephalo-myo-synangiosis (EMS), and encephalo-duro- arterio-myo-synangiosis (EDAMS) emerged in subsequent years, and demonstrated superior results in terms
of revascularization.4,5 The STA-MCA bypass with EDAS is one of the simple and elegant options for performing combined direct and indirect revascularization.
STA-MCA with EDAS can be considered the standard operation for treatment of MMD in adults. The procedure is indicated in these patients, if the following criteria are present:
1. Symptomatic patient, that is, patients presenting with stroke (hemorrhagic or ischemic), transient ischemic attack, or progressive cognitive decline.
2. Evidence of hemodynamic compromise with poor cerebrovascular reserve, which can be evaluated using a number of imaging modalities. Our institutional protocol relies on a combination of magnetic resonance (MR) imaging consisting of quantitative MR angiography with and without diamox challenge, global blood oxygen level dependent (BOLD) imaging with hypercapnic challenge and regional BOLD imaging using functional MR imaging paradigms. The aggregate information is used to determine if there is reduced or absent cerebrovascular reserve.
3. Adequate donor and recipient vessels to perform the STA-MCA direct anastomosis; this can be an issue in very young pediatric patients, in which case, indirect procedure alone can be pursued.
The combined STA-MCA with EDAS can also be considered the preferred option for pediatric patients if direct bypass is feasible; the greatest barrier to performing direct bypass is posed by the very young pediatric patients (< 5 years old), dependent on donor and recipient vessel size, in which case, indirect procedure alone can be pursued. For pediatric patients, even an asymptomatic hemisphere affected by moyamoya warrants consideration for surgery if there is presence of hemodynamic compromise on imaging, as progression to symptoms and stroke is prevalent in this population.
The advantage of the STA-MCA bypass in combination with EDAS, as opposed to in combination with other indirect procedures such as EMS or EDAMS, relate to the relative disadvantages of harvesting and using muscle on the brain surface. Although muscle can be a very effective source of collaterals, its use typically entails a larger craniotomy to expose more brain surface area for muscle contact, entails potential cosmetic issues related to transposition of the muscle underneath the bone flap, and has a higher risk of postoperative hematoma from oozing of muscle fibers over the brain surface, particularly when patients are on aspirin to optimize the patency of direct bypass. The EDAS procedure is more straightforward, combines naturally with the STA-MCA bypass requiring little alteration to the approach that would already be applied for the direct procedure, and provides effective collaterals without the potential disadvantage of muscle use.
The STA-MCA bypass with EDAS provides both immediate revascularization through direct bypass and longer term growth of additional collaterals through indirect EDAS. In fact, there is frequently a reciprocal relationship between direct STA bypass flow and indirect EDAS collaterals that provide durable temporally complementary revascularization.6 Key concepts that are critical in this procedure are as follows:
• Identification of the vascular territory in most need of flow augmentation, and choosing the skin incision, craniotomy, and donor vessel choice and configuration to optimize direct and indirect bypass.
• Preserving the middle meningeal artery (MMA) when performing the craniotomy and opening the dura, particularly if it is already providing extracranial- intracranial (EC-IC) collaterals (as evident from preoperative angiographic imaging).
• Use of flow-assisted surgical technique7,8 (as described further) to measure cut flow and cut flow index in order to assess direct STA-MCA bypass.
• Direct bypass allows for immediate flow augmentation and revascularization.
• Indirect bypass is simple/fast and can be integrated easily with direct bypass.
• Combined procedure provides complementary short- and long-term revascularization.
• Dual STA branch harvest can lead to wound healing problems.
• Longer procedure than indirect EDAS alone.
• Potential risk for hyperperfusion from direct STA-MCA bypass.
• Need for temporary vessel occlusion.
• Extension of combined revascularization concept to anterior and posterior cerebral artery territories.
• Lack Class I evidence for comparative efficacy to indirect or direct procedures alone.
The primary contraindication is recent stroke within the last 7 to 14 days, primarily due to higher risk of reperfusion hemorrhage with the direct STA-MCA portion of the procedure, and also in general due to heightened risk of anesthesia and surgery in the setting of a recent ischemic event. Additional contraindications for direct component of the procedure would be poor quality or caliber of the STA donor vessel, or existing spontaneous collaterals from the donor STA which would be disrupted by harvesting and cutting the vessel for direct anastomosis. In such a scenario indirect arterio-synangiosis, using the intact STA which is kept in continuity and apposed to the brain surface, would still be feasible, as long as harvesting the vessel in situ would not directly result in disruption of collaterals.
For the STA-MCA with EDAS operation the preoperative imaging is critical in planning. Catheter angiography allows the best assessment of the course and caliber of the donor STA vessels, and allows evaluation of spontaneous EC-IC collaterals from the MMA or other sources which must be preserved while performing the operation. The angiogram should provide dedicated internal and external carotid injections to allow the optimal evaluation of these features. The angiogram, in conjunction with blood flow imaging, is also important in determining the vascular territory that is most compromised and most in need of flow augmentation.
In the preoperative arrangements, admission of the patient prior to day of surgery to ensure overnight intravenous hydration while the patient is not allowed oral intake is an important safety measure to reduce the risk of hypovolemia and hypotensive episode during induction of anesthesia. Preoperative administration of aspirin, if the patient is not already routinely taking the medication, is advisable as a maneuver to enhance patency of direct STA-MCA anastomosis, and checking aspirin sensitivity assay to ensure that the medication is effective pre- operatively can be performed. For patients with comorbid diseases, it is essential to optimize the management of the condition prior to surgery, for example, in patients with sickle cell disease, use of exchange transfusions and reduction of hemoglobin S levels, or in patients with diabetes, strict glucose regulation, and controlled hemoglobin A1C levels. Otherwise, such conditions can affect either the success of the revascularization or healing and recovery from the surgery.
The primary risk associated with STA-MCA bypass with EDAS is similar to any revascularization surgery in patients with MMD, namely the risk of perioperative ischemic stroke. The addition of direct STA-MCA bypass to the EDAS operation ought not to increase this risk, given that temporary occlusion of the cortical MCA branch required for direct anastomosis is extremely well tolerated. However, it does add some additional operative time which could potentially elevate risk, as period of time under anesthesia may be a risk contributor. Direct bypass also can engender a risk for postoperative hyperperfusion or reperfusion hemorrhage which is not encountered with indirect EDAS alone, and requires postoperative vigilance and blood pressure management to avoid. Other general risks include postoperative seizures, and short-term prophylactic anticonvulsants are thus reasonable.
One feature of the STA-MCA with EDAS operation is the dual harvest of both STA branches, using one for direct anastomosis and the other for indirect arterio-synangiosis. The dual harvest however can lead to devascularization of the scalp tissue and incisional healing problems, which in turn can result in wound dehiscence or infection.
As noted above, aspirin is administered preoperatively to patients, typically at full dose of 325 mg for adults and 81 mg for pediatric patients, and aspirin sensitivity is confirmed by platelet function assay prior to the surgery. During the surgery, low-dose heparin (10 units/mL) is used for flushing the donor STA and recipient MCA vessel for direct anastomosis, but no systemic anticoagulation is used.
General endotracheal anesthesia is utilized. The primary considerations are maintenance of blood pressure at or above the patient’s baseline blood pressure throughout, especially during the induction of anesthesia when there is most risk of lability and hypotension. Arterial line placement is mandatory for monitoring of the blood pressure during the surgery and for access to draw arterial blood gas samples. End-tidal carbon dioxide levels should be monitored and correlated with arterial levels, to avoid hyperventilation, which reduces cerebral blood flow. The anesthetic regimen is chosen to allow titration to achieve burst suppression during the temporary clipping time for direct anastomosis. Both electroencephalography (EEG) and somatosensory-evoked potential (SSEP) leads are placed prior to positioning for neuromonitoring. EEG allows determination of burst suppression when needed during the operation, and along with SSEP can also alert to hypoperfusion and brain ischemia as both reflect integrity of cortical activity. It is important to assess baselines in these modalities, as prior strokes may affect the symmetry, amplitude, or latency; the relevant concern would be changes noted relative to baseline. Since the EEG and SSEP monitoring utilize scalp electrodes, it is advisable to map the STA prior to placement of these needle or corkscrew electrodes to avoid inadvertent injury to the STA.
During the surgery, the anesthesiologist must also maintain euvolemia for the patient; use of the typical brain relaxation agents such as mannitol and furosemide must be avoided due to risk for hypovolemia, hypotension and subsequent hypoperfusion in the already tenuous and compromised vascular territory undergoing surgery, or even the contralateral side in patients with bilateral disease.
The patient is positioned with the surgeon at the head of the bed, anesthesiologist to the left of the patient and the operating nurse to the right of the patient so that instruments can be easily handed to the right hand of the surgeon during the operation. The patient’s head is turned to the right or left dependent on the side that needs to be operated.
The patient is positioned supine, with pin fixation to place the head into lateral position. Dependent on neck mobility and girth, a roll under the ipsilateral shoulder may be necessary to avoid overrotation of the neck and jugular vein compromise. The Sugita head holder is particularly suitable for the case as it accommodates a ring retractor system with hooks which can be used for both anterior and posterior retraction of the skin edges. Although this head holder allows placement of four pins for stability, in MMD patients where bilateral surgery may ultimately be needed, it is best to utilize only three pins for fixation to avoid the fourth pin which would otherwise be located in the contralateral scalp and risk injuring the contralateral STA (Fig. 18.1a).
18.9.2 Skin Incision and STA Harvest
The STA anterior (frontal) and posterior (parietal) branch are mapped with Doppler and marked on the skin. After sterile preparation and draping, a straight incision is then created over the parietal branch using needle tip bovie electrocautery on a low setting, and the STA branch is exposed using blunt dissection with a mosquito instrument. The exposed STA is then dissected free with a cuff of attached tissue for a length of approximately 8 to 10 cm. The STA bifurcation and anterior branch are also identified and followed. In pediatric patients, skin elasticity allows the anterior skin edge to be lifted allowing harvest of the frontal branch through the existing linear incision. In adults this is typically not feasible, and the linear incision is curved anteriorly into a skin flap; the frontal branch is then harvested from the undersurface of the flap (Fig. 18.1b). The frontal branch will typically be utilized for direct anastomosis and the parietal branch for the in situ indirect arterio-synangiosis. Thus, the former is cut distally, and occluded with a temporary clip proximally, while the latter is left in continuity. The cut frontal branch is flushed with heparin solution (10 units/mL, ensuring to release the clip momentarily to flush proximal to it in order to reduce risk of thrombus formation from stagnant flow). Both frontal and parietal branch ae then wrapped in a papaverine soaked cottonoid to keep them hydrated and relieve any vasospasm created from manipulation during the harvest.
The temporalis muscle and fascia are opened in a T-shaped fashion below the intact STA branch (Fig. 18.2), and the muscle edges retracted both anteriorly and posteriorly to expose the underlying cranium. While protecting the STA branches, burr holes are placed inferiorly and superiorly beneath the proximal and distal aspects of the parietal STA branch, and a craniotomy is elevated with a power drill straight bit attached to a foot plate. The craniotomy placement spans both anterior and posterior to the parietal branch, to allow the vessel to have good exposure to the underlying brain for indirect bypass. Care is taken in the anterior aspect of the planned craniotomy to strip the dura in order to avoid injury to the MMA; if necessary this aspect of the boney opening is performed by sequential biting of the bone under direct vision rather than removing it with the remainder of the bone flap. The dura is tacked to the edges of the bone with sutures for epidural hemostasis, again with care to avoid dural vessel branches. The dura is then opened in a cruciate fashion but avoiding the MMA and any major dural branches, which are instead preserved as bridges of dura across the craniotomy field as needed (Fig. 18.2).
18.9.4 Recipient Vessel Preparation
At this point of the surgery, the intraoperative microscope is utilized. In preparing both for STA-MCA bypass and EDAS, the arachnoid over the cortical vessels is opened with an arachnoid knife. Different potential recipients for direct anastomosis are evaluated based on size, vascular territory (e.g., superior vs. inferior division of MCA) and orientation/location in the operative field. The ideal orientation for a right handed surgeon is a vessel laying from 10:30 to 4:30 on a clock face, with ideal location being central within the boney opening rather than close to a bone or dural edge. The chosen vessel is dissected more extensively and very small perforating branches are sacrificed if needed to prevent back-bleeding into the vessel during anastomosis. The recipient is then separated from the surrounding brain, by placing a small rubber dam beneath the vessel, and Gelfoam beneath this to elevate the artery out of its sulcus (Fig. 18.4a). Papaverine cottonoids are applied to the recipient briefly as needed to relieve any vasospasm created by the dissection.
18.9.5 Donor Vessel Preparation
The frontal branch which is being prepared for direct anastomosis is first prepared distally by dissecting away the surrounding cuff of tissue using microscissors; any small branch vessels encountered are coagulated gently to prevent bleeding after flow is restored. Once the vessel has been adequately prepared, the cut flow is measured.9'10 This entails releasing the proximal temporary clip and measuring the flow within the free-flowing artery using an ultrasonic transit-time flow probe (the Transonic Char- bel micro-flow probe) in cc/min (Fig. 18.3). Following the measurement, the vessel is again flushed with heparinized saline and a clip is reapplied proximally. The donor vessel end is then cut in a beveled fashion and fish mouthed in preparation for anastomosis. A marker is used to mark the vessel circumferentially prior to cutting the vessel for improved visualization of vessel edges during the anastomosis.
18.9.6 STA-MCA Bypass
A marking pen is utilized to mark the surface of the recipient cortical vessel where the arteriotomy will be placed in order to improve visualization of the vessel edges during anastomosis (Fig. 18.4a). After confirming that the patient is in burst suppression, temporary vessel clips are placed on the recipient vessel and a fine microblade is utilized to create the arteriotomy which is then extended with fine microscissors until it matches the length of the opening of the beveled and fish-mouthed donor vessel. The internal lumen of the recipient is flushed with heparinized saline and a small silastic stent can be placed inside the recipient vessel lumen to hold the vessel walls apart, as needed.
To perform the anastomosis, a 10-0 nylon suture is placed between the heel of the donor vessel and one end of the arteriotomy (Fig. 18.4b); the suture is tied to create the first apical stitch. At the other side of the arteriotomy, the suture is placed from the toe of the donor vessel to the other apex of the arteriotomy. Having placed the apical stitches, the remaining suture from the apical stich can be used to close the arteriotomy on each side in a running to or interrupted fashion. If performed in a running fashion, the suture loops are kept loose until all the stitches have been places and then tightened sequentially while keeping the pulled suture taut, in order to create even tension along the entire suture line (Fig. 18.4c). If closed in an interrupted fashion, stitches can be placed from each end towards the center and the subsequent stitch placed before tying the prior suture (Fig. 18.4e); both maneuvers allow maximal visualization of needle placement in the donor and recipient vessel edges during suturing. After one side of the arteriotomy is complete, the lumen should be checked form the other side to ensure none of the stitches have caught the “back” wall (Fig. 18.4d). Once confirmed, the remaining side of the anastomosis is completed (Fig. 18.4f), making sure to remove the stent, if one has been used, prior to placement of the final stitches. Once the anastomosis is complete, the distal and then proximal temporary clips are removed from the recipient vessel and the anastomosis line is observed for hemostasis, prior to then removing the temporary clip from the proximal donor STA.
The final maneuver is then to measure the bypass flow using the ultrasonic microflow probe. The cut flow index (CFI), that is, the bypass flow/cut flow, can then be determined, with a CFI of less than 0.5 indicating a well-functioning bypass. The flow measurements should be made under similar anesthetic conditions related to blood pressure, burst suppression and end-tidal carbon dioxide, as these factors alone can impact blood flow. High bypass flows, such as greater than 80 cc per minute, should prompt judicious blood pressure control to avoid hyperperfusion.
18.9.7 Encephalo-arterio- synangiosis
To perform the arterio-synangiosis, the parietal branch of the STA, which is still intact, is laid over the brain surface (Fig. 18.5), ensuring that the arachnoid has been opened particularly in areas where the vessel apposes the brain surface. Then, 10-0 nylon sutures are used to suture the cuff of tissue along the STA to the arachnoid to maintain good apposition between the artery and the brain. Three to four such sutures are placed along the length of the STA as it travels over the brain surface. Care is taken to avoid stitches near the edge of the craniotomy in order to avoid kinking of the vessel as it travels in and out of the surgical field.
The final step in the revascularization procedure is the dural synangiosis. This can be performed simply be inverting the cut dural leaflets onto the brain surface, such that the outer more vascular dural surface is in direct contact with the brain surface. Alternatively, the dura can be split into two layers with forceps, exposing the vasculature within the dura, and then inverting the inner layer over the pia while laying the outer layer onto the pia (Fig. 18.5). This has the advantage of providing a greater surface area of contact between the dura and the brain.
The dural opening and remaining exposed brain surface can be covered with dural substitute or hemostatic layer such as Gelfoam. The bone flap is thinned and trimmed to avoid pressure or kinking of the STA branches. The flap is replaced such that the parietal branch serving as indirect bypass enters and exists through the inferior and superior burr hole sites.
The temporal fascia and muscle is stitched but the proximal portion is not closed to avoid kinking or pressure on the STA stump and branches. After bone flap replacement and muscle closure, the bypass flow is remeasured to ensure patency has been maintained. A nonadherent Gelfilm layer is placed over the STA stump to prevent adhesion and scarring in this location in case of any future need to reopen the incision. The skin is then closed with galeal stitches after placement of a short closed-system subgaleal drain. A nylon suture is placed in the skin; in pediatric patients, absorbable suture instead of nylon can be used to avoid the need for subsequent suture removal. In adults, healing of the incision is generally slower, compounded by the devascularization of the scalp by the dual STA harvest and the longer curved incision in adults; these factors favor the use of permanent suture material which can be removed when the surgeon chooses based on inspection and verification of healing, rather than absorbable sutures which lose integrity at a pre-determined interval.
If the frontal STA branch which is typically used for the STA-MCA bypass is discovered to be inadequate during surgery or has poor cut flow, the parietal branch can be used as an alternative. In such a scenario the parietal branch alone will serve as both direct bypass and the source for arterio-synangiosis along the course of the vessel, where it is apposed to the brain surface, proximal to the anastomosis.
Pitfalls and mistakes to remain vigilant for and avoid include the following:
18.10.1 Donor Vessel
• Injuring STA during harvest or craniotomy.
• Failing to coagulate side branches leads to leakage after bypass.
• Failing to flush and irrigate vessel leads to desiccation.
• Creating a dissection in the vessel wall during harvest or flushing.
• Inadequate craniotomy size, location.
• Sacrifice of the MMA during craniotomy or dura opening.
• Poor hemostasis prior to starting bypass—continuous oozing disrupts visualization.
18.10.3 Recipient Vessel
• Injuring or coagulating recipient which is friable.
• Failure to coagualate perforating branches which will cause back bleeding during anastomosis.
• Catching back wall during suturing of the anastomosis.
• Inadequate number of sutures leads to leakage of anastomosis.
• Failure to remove stent.
• Revascularizing wrong territory (superior vs. inferior
• Strangulating STA during bone flap replacement or muscle reapproximation.
• Catch STA stump in suture line during skin closure.
For the STA-MCA bypass, if a poor bypass flow or cut flow index (e.g., <0.5) is encountered, several factor can be contributing:
• Poor patient selection (no hemodynamic compromise): this problem is best averted by careful attention to preoperative hemodynamic imaging and careful patient selection.
• Donor problem: avoid by not injuring or coagulating vessel during harvest, keeping the branch moist and wrapped in a papaverine soaked cottonoid, flushing with heparinized saline, cleaning the adventitial cuff well, and making sure the vessel wall is not dissected prior to anastomosis.
• Anastomosis problem: avoid by checking back wall during suturing (and using a silastic stent), flushing with heparinized saline prior to completion, and making sure no sutures are protruding into the lumen.
• Recipient or distal bed problem: avoid by choosing adequate size recipient, flushing with heparinized saline, and recognizing that the vascular territory may require double STA bypass if recipient beds are isolated by proximal occlusive disease.
It is best to avoid the potential pitfalls by careful attention to detail, rather than manage them after occurrence, but in some cases, salvage strategies are necessary.
If the donor STA becomes injured, for example, the parietal branch, which is kept intact is caught in the drill during craniotomy, that branch can still potentially be salvaged and used as a direct bypass if it can be cut proximal to the area of injury.
If direct STA-MCA anastomosis thromboses, it is important to check the suture line and massage the vessels and anastomosis site gently as a small clot may dislodge and regain patency. Otherwise, if a problem with the suture line is suspected, the anastomosis can be reopened and revised using heparin and small flushes of tissue plasminogen activator (tPA) to fully dissolve any thrombus prior to resuturing. Unfortunately if thrombus has formed in the anastomosis for any reason, this is frequently white platelet rich clot which is less responsive to heparin and tPA and is prone to reaccumulation. Even if patency cannot be restored, direct bypass should be kept in place as the bypass occasionally recanalizes over time to deliver flow.
If the anastomosis suture line has leakage after release of temporary clips, the first maneuver is to apply gentle pressure with a cotton ball which frequently abates the issue. If unsuccessful, an additional stitch may be required, although there is risk of suboptimal placement as visualization is impaired compared to during the anastomosis. Another strategy if interrupted sutures have been used is to leave one suture end long for each stitch during the anastomosis; if a leak is subsequently evident between sutures after the temporary clips are removed, the long ends of each can then be tied together to cinch the leakage area avoiding the need for placement of a new stich.
Tips and key elements can be categorized as relevant to different phases of the operation as outlined below.
18.12.1 Preoperative Management
• Good preoperative patient selection.
• Study angiographic imaging and plan case (assess the best donor/recipient territory, assess for spontaneous MMA collaterals).
18.12.2 Intraoperative Anesthetic Management
• No mannitol, lasix, hyperventilation during surgery.
• Burst suppression during temporary clipping.
• Anticonvulsant prophylaxis.
• SSEP/EEG monitoring to detect, and thus avoid, intraoperative ischemia.
• Strict blood pressure maintenance during induction and anesthesia.
• Attention to details throughout—from skin incision to closure.
• Avoid all thrombogenic material—flush vessels, create perfect field hemostasis, avoid Floseal.
• Keep STA moist and wrapped in papaverine soaked cottonoid until used.
• If there’s leakage at anastomosis site, irrigate copiously and apply gentle pressure (rare to require additional stich); for interrupted sutures, tie long end of adjacent stitches together.
Additionally, close postoperative monitoring and management is critical. Blood pressure should be controlled to patient’s baseline range and the patient should be observed in the intensive care unit for the first 24 to 48 hours postoperatively. Postoperative head CT to rule out any hemorrhage, and assessment of bypass function and patency with quantitative magnetic resonance angiography (Fig. 18.6), and angiogram during the hospital stay as a baseline is useful. Reassessment of hemodynamics with imaging at 6 weeks, 6 months, and 12 months is our standard protocol and annually thereafter, along with neuropsychological testing. If bilateral surgery is needed these are generally separated by 4 to 6 weeks to allow interim recovery.
The author would like to acknowledge Christa Wellman and Ziad Hage, MD, for assistance in preparation of the figures, and Fady T Charbel, MD, for the development of the flow-based approach to STA-MCA bypass.
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