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Ann Thorac Surg 1999;67:277-284
© 1999 The Society of Thoracic Surgeons

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Current Review

Arterial grafts for coronary artery bypass grafting: biological characteristics, functional classification, and clinical choice

^a Division of Cardiothoracic Surgery, Department of Surgery, University of Hong Kong, Grantham Hospital, Aberdeen, Hong Kong

Address reprint requests to Professor He, Division of Cardiothoracic Surgery, University of Hong Kong, Grantham Hospital, 125 Wong Chuk Hang Rd, Aberdeen, Hong Kong
e-mail: gwhe{at}hkucc.hku.hk

	Abstract

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 
Various arterial grafts have been used for coronary artery bypass grafting, but a unanimous opinion on how to best use these grafts has not been formed. Arterial grafts are not uniform in their biological characteristics. Differences between the perioperative behavior of the grafts and their long-term patency may be related to different characteristics. These characteristics should be taken into account in the use of arterial grafts, some of which are subject to more active pharmacologic intervention during and after operation to obtain satisfactory results. Clinical choice of grafts must be based on the general condition of the patient, the biological characteristics of the graft, the anatomy of the coronary artery, the match between the coronary artery and the graft, and technical considerations, including antispastic management.

	Introduction

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 
Compared with standard saphenous vein grafts, use of the internal mammary artery (IMA) as a coronary artery bypass graft has resulted in superior long-term results [1, 2]. Studies have demonstrated that there are differences between venous and arterial grafts: (1) Veins are more susceptable to vasoactive substances than arteries [3]; (2) the venous wall is supplied by the vaso vasorum, whereas the arterial wall may be supplied through the lumen in addition to the vaso vasorum [4]; (3) the endothelium of arteries may secrete more endothelium-derived relaxing factor (EDRF) [5]; and (4) the structure of the vein is subject to low pressure, whereas the artery is subjected to high pressure. Therefore, in a high-pressure system after coronary artery bypass grafting (CABG), venous grafts have to adapt to the high pressure, whereas arterial grafts do not. These differences may account for the difference in the long-term patency rate.

On the basis of superior long-term results of use of the IMA, other arteries have been used in CABG [6–14]. Such conduits include the radial artery (RA) [6], the gastroepiploic artery (GEA) [7], the inferior epigastric artery (IEA) [8, 9], the splenic artery [10], the subscapular artery [11], the inferior mesenteric artery [12], the descending branch of the lateral femoral circumflex artery [13], and the ulnar artery [14]. In addition, the intercostal artery [15] has also been suggested for use as a graft. However, although the long-term patency rates for the IMA are well established, there are only a few reports on other arterial conduits, and these involve a relatively small number of patients and shorter follow-up periods [16–18]. It has been expected that long-term results with other arterial conduits will be as good as those for the IMA. Such expectations are based on the hypothesis that all arterial conduits have similar biological features, such as contractility, relaxing characteristics, endothelial function, and anatomic structure. Histologic studies have revealed that there are major differences among various grafts in terms of the structure of smooth muscle such as elastic lamellae [4]. The differences observed in these studies suggest that arterial grafts, albeit arteries, are not uniform in either anatomy or function. In contrast, comparative functional studies [19–23] have demonstrated differences in arterial grafts with regard to contractility and endothelial function. These differences are the anatomic and physiologic bases of the divergent clinical manifestations of the grafts and may also account for the possible differences in postoperative graft function and long-term patency rates. One such clinically observed manifestation—the tendency to develop spasm during surgical dissection and the perioperative period—differs among arterial grafts. Many surgeons have observed that the tendency to spasm is higher in the GEA than in the IMA [24]. Similarly, spasm of the RA is a serious problem that, together with a low patency rate, which may be also related to this characteristic of the artery, led to the abandonment of RA grafts at an early stage in the 1970s [25]. Only after the development of a method to overcome spasm of this arterial graft has it recently been reused [26].

An important clinical question is how to properly choose arterial grafts. This choice has been largely based on personal preference and experience in various hospitals. This review examines this issue on the basis of the current scientific findings on arterial grafts, combined with clinical considerations.

	Biological characteristics

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 
All arterial grafts for CABG are conductance arteries (as opposed to "resistance" arteries). A common feature of arterial grafts is that removal of these arteries would not usually affect the blood supply to the corresponding organ and is of concern only in extreme situations. The common physiologic role of these conductance arteries is to channel blood flow to perfuse corresponding organs, such as the heart (the coronary artery), the stomach or other visceral organs (the GEA, the splenic artery, and the inferior mesenteric artery), the hand (the RA), and the body wall (the IMA, the IEA, and the subscapular artery). However, these arteries may differ in function because the organs they perfuse have different physiologic roles, so that the flow required or the flow reserve of these organs may differ. To understand the differences among these arteries, anatomic, physiologic, pharmacologic, and embryologic studies at the organ, tissue, and cellular levels have been conducted.

Anatomic differences
Differences in gross anatomy among arterial grafts are obvious because arterial grafts are located at different parts of the body and supply different organs. Studies have shown evidence of the divergent anatomic structure of the arteries [4]. One of the most obvious differences with regard to structure can be seen in arteries such as the GEA, IEA, and RA, which contain more smooth muscle cells in their walls and are therefore less elastic. In contrast, other arteries such as the IMA may be more elastic because they contain more elastic laminae [4]. Such structure divergence may explain the differences in physiologic and pharmacologic reactivity.

Contractility, incidence of spasm, and comparison with coronary arteries
Contractility and incidence of spasm in arterial grafts
Knowledge of how vasospasm develops is still lacking. The correlation between vasospasm and the reactivity of a vessel to vasoconstrictors is also unclear. However, it is presumed that vasospasm is the extreme form of vasoconstriction, which may be the response of a vessel to many stimuli (spasmogens). These stimuli may be physical (eg, mechanical stimulation or temperature changes) or pharmacologic (eg, nerve stimulation or vasocontrictor substances).

Important vasoconstrictor substances, which may be spasmogens in the case of blood vessels, are [22] (1) endothelium-derived contracting factors such as endothelin (ET); 2) prostanoids such as TXA₂ thromboxane A₂ (TXA₂) and prostaglandin F₂; (3) circulating sympathomimetic substances (-adrenoceptor agonists) such as norepinephrine and synthetic ₁-adrenoceptor agonists (methoxamine or phenylephrine); (4) platelet-derived contracting substances such as 5-hydroxytryptamine and TXA₂; (5) substances released from mast cells and basophils such as histamine; (6) muscarinic receptor agonists such as acetylcholine; (7) renin–angiotensin system-related substances such as angiotensin II; and (8) the depolarizing agent potassium ions.

The contractility of arterial grafts in response to these vasconstrictors has been extensively studied [19–23, 27]. A previous study [22] revealed that there are basically two types of vasoconstrictors that are important spasmogens in arterial grafts. Type I vasoconstrictors (ET, prostanoids [TXA₂ and prostaglandin F₂], ₁-adrenoceptor agonists) are the most potent and they strongly contract arterial grafts even when endothelium is intact. Type II vasoconstrictors (eg, 5-hydroxytryptamine) induce only weak vasoconstriction when endothelium is intact. However, those vasoconstrictors probably play an important role in the spasm of arterial grafts in the event that endothelium is destroyed by surgical handling.

The difference among arterial grafts with regard to the response to these vasoconstrictors is in the magnitude of the response and sensitivity to the spasmogen. Although all arterial grafts react to the these vasoconstrictors, there is a general agreement that some arteries have a stronger reaction to vasoconstrictors than others. This difference is best reflected by the finding that the GEA reacts more strongly to vasoconstrictors such as K⁺, TXA₂, ET-1, and norepinephrine than other arteries [21]. In a comparison between the RA and the IMA, the response to norepinephrine and 5-hydroxytryptamine [20], angiotensin, and ET-1 [28] was higher in the RA than in the IMA. Clinically, although all arterial grafts may develop vasospasm, it develops more frequently in the GEA [24] and RA [26] than in the IMA and IEA. Postoperative vasospasm and occlusion accounted for the early abandonment of the RA [26] and may be the reason for the abandonment of the GEA in some cardiac surgical centers.

However, there are groups of arteries with similar contractility in response to vasoconstrictors. The IMA and IEA are in this group [21, 23]. The response of these two arteries to a number of vasoconstrictors, such as ET, U46619, or K⁺, is similar [21, 23].

Comparison with coronary arteries
In general, coronary arteries are highly reactive vessels, and coronary spasm is a well-known phenomenon. However, a direct comparison between the coronary artery and coronary bypass grafts is still lacking. Although previous studies have attempted to do so, such comparisons were devalued when the human coronary artery was taken from an explanted heart with coronary artery disease [21]. In a normal heart, the reactivity of coronary arteries may be equal to or higher than that of arterial grafts, as demonstrated in canine vessels [3]. However, when a large coronary artery has atherosclerotic disease, it may be less reactive to vasoconstrictors than arterial grafts, although the reactivity of a small coronary artery may remain high.

Receptors
Most vasoconstrictors except K⁺ contract arterial grafts by activating a specific receptor. Some receptors on the smooth muscle of the arterial grafts have been characterized. For example, the IMA is an ₁-adrenoceptor–dominant artery, with little ₂- or ß-function [29]. In contrast, the RA has both ₁- and ₂-function, although its ß-function is also weak [30].

Other receptors functionally demonstrated in arterial grafts are ET_A, ET_B [31], 5-hydroxytryptamine [32], angiotensin [33], thromboxane–prostanoid [34], vasopressin [35], and vasoactive intestinal peptide [36] receptors in the IMA. There are fewer reports on the receptors in other arterial grafts [28, 36].

Receptors are also located in the cellular membrane of the endothelial cell in the arterial grafts. Usually, these receptors mediate relaxation through the endothelium-dependent mechanism. However, more studies are warranted to understand the difference among arterial grafts regarding these receptors.

Endothelial function
Compared with the marked difference in EDRF release between the IMA and the saphenous vein [5], the difference among arteries is less significant. Although there is some degree of difference, as in the EDRF-related relaxation of the IMA and IEA [23], this difference is most likely related to the higher incidence of atherosclerosis in the IEA [23, 37]. Other differences found in various studies [38, 39] regarding endothelial function among arterial grafts have no clear clinical implications yet. More likely, under normal conditions, arteries used as coronary bypass grafts have no major differences in endothelial function [21, 28]. However, endothelial function may be affected by the development of atherosclerosis in a particular artery. Also possible is that there may be differences in the various components of EDRF because the so-called EDRF includes at least three major components (endothelium-derived nitric oxide, prostaglandin I₂, and endothelium-derived hyperpolarizing factor) [40].

Smooth muscle relaxation
No major differences have been observed among arterial grafts with regard to endothelium-independent relaxation (eg, in response to vasodilators such as nitroglycerin), which is often used as an index of function of the relaxation properties of the smooth muscle [19, 23], although there may be some differences in response to vasodilator substances with regard to sensitivity [36]. These findings imply that arterial grafts may have no major differences in relaxation properties.

Embryologic considerations
Commonly used arterial grafts belong to different groups of arteries in various locations of the body. Basically, they can be divided into somatic arteries and splanchnic arteries [41]. Somatic arteries are those that supply the body wall and include the IMA, IEA, the subscapular artery, and the intercostal artery. In comparison, splanchnic arteries are those that supply visceral organs and include the GEA and the splenic artery, among others. From embryologic development [41], somatic arteries arise from intersegmental branches to the body wall, whereas splanchnic arteries arise from segmental branches of the primitive dorsal aorta to supply the digestive tube.

The limb arteries are special arteries that supply the extremities. They arise either from somatic arteries (upper limb arteries) or from the dorsal root of the umbilical artery (lower limb arteries).

Physiologic considerations
All arterial grafts for CABG are conduit arteries, and their physiologic function is to carry blood flow to organs. Because the organs they supply have different physiologic functions, these arteries are entitled to adapt to the diverse demand for blood supply to individual organs. Therefore, the structure and reactivity of these arteries differ such that some are more spastic (more reactive to vasoconstrictors) than others.

Segmental differences
All arterial grafts for CABG are conduit arteries. The reactivity of the grafts varies along their length. As demonstrated in the IMA, the main portion (the midportion, comprising more than 60% of the total length of the graft) of the IMA is less reactive than the distal portion and possibly the proximal portion [42, 43]. This variation may also occur in other arterial grafts, such as the GEA, IEA, and RA. Although the full length of arterial grafts is reactive [43], the major muscular components are located at the two ends of the artery (muscular regulator) [44]. In particular, the distal end is a more efficient physiologic regulator of flow because this part contains relatively more smooth muscle cells and is smaller in diameter than the proximal end. Such characteristics are physiologically important in regulating blood flow distribution. However, when such arteries are used as bypass grafts, these characteristics may be detrimental. In terms of preventing vasospasm of arterial grafts, trimming off the small and highly reactive distal end of the grafts (IMA, GEA, IEA, or other grafts) may be important and clinically feasible.

Incidence of atherosclerosis
There are two aspects with regard to the incidence of atherosclerosis in arterial grafts: (1) the incidence of atherosclerosis in the in situ native position, and (2) the incidence of atherosclerosis after coronary grafting.

Incidence of atherosclerosis in native arteries
The exact incidence of atherosclerosis in midsized conduit arteries is unknown. In general, the incidence of atherosclerosis in the four major arterial grafts is low compared with that in the left anterior descending coronary artery [4]. In fact, atherosclerosis is absent or only mildly present in all four arterial grafts. Early studies had demonstrated that the incidence of atherosclerosis in the IMA was low [45]. It is frequently seen on the angiogram that a patent IMA exists with a stenotic vertebral artery. In contrast, the incidence of atherosclerosis at the proximal end of the IEA may be high, as seen in a small group of patients [23, 37]. Although the reason accounting for this observation is unknown, it may be related to the finding that the incidence of atherosclerosis is higher in the lower limb arteries than the upper limb arteries, and the IEA is the first branch of the external iliac artery [23]. The incidence of atherosclerosis in the GEA is low, as recently reported by us [37] and others [46].

Incidence of atherosclerosis in bypass grafts
The incidence of atherosclerosis is low in IMA grafts [1, 2], even as late as 15 to 21 years after CABG [47]. The long-term incidence in other arterial grafts has yet to be studied, although there is evidence showing that it could be low in the GEA [46].

	Functional classification

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 
On the basis of experimental studies on vasoreactivity, together with physiologic and embryologic considerations, a functional classification for arterial grafts was proposed by He and Yang [21]. This classification suggests that there are three types of arterial grafts: Type I, somatic arteries; type II, splanchnic arteries; and type III, limb arteries. Type II and III arteries are prone to spasm because of their higher contractility and therefore require more active pharmacologic intervention [21, 28, 48, 49] (Fig 1). The correlation between this functional classification and long-term patency, however, needs to be studied.

View larger version (17K): [in this window] [in a new window]   Fig 1. Functional classification of clinically used arterial grafts according to physiological and pharmacological contractility, anatomical, and embryological characteristics.

	Considerations in choosing grafts

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 
In choosing an adequate graft, many factors need to be considered.

General condition of the patient
Nontechnical factors related to graft failure
Cholesterol levels, particularly high levels of low-density lipoprotein and triglycerides, may affect the patency of the graft. In addition, other factors, such as high levels of lipoprotein(a), a thrombogenic molecule that is related to the hypercoagulable state, may also influence long-term patency [50]. Other risk factors for coronary artery disease, such as smoking, hypertension, and in particular, diabetes, may also affect the fate of the graft. In addition, diabetes has been thought to be a contraindication for bilateral IMA grafting because of a possible increase in sternal wound infection [51], although this has not been shown in other studies [52]. However, these factors do not account for the differences between venous and arterial grafts.

Age
It is obvious that the age of the patient is an important factor. The main advantage of arterial grafts is their superior patency compared with venous grafts. Young patients are benefited more by this advantage. For a single IMA graft, there is almost no contraindication [53]. However, although there are no uniform criteria with regard to age for complex arterial grafting, such as bilateral IMA grafting, 65 years has been suggested as the upper limit [53]. However, this limitation may largely depend on surgeon experience and preference. Essentially, there is no age limit for use of the RA, although in general the RA is used in patients younger than 70 years [54]. In general, arterial grafts are indicated more in patients who are expected to live for more than 10 years, which is beyond the benefit of vein grafts.

Urgency of operation
In catastrophic emergencies it may be wise not to perform relatively time-consuming arterial grafting.

Other situations
Extreme chest deformities and significant disease of the subclavian or internal thoracic arteries are probably contraindications to the use of the IMA [53].

Biological characteristics
Adequate size
The size of a vessel depends on the transluminal pressure. In the collapsed state, the size of the vessel is obviously not the size in vivo under the physiologic pressure. In general, all major arterial grafts are of adequate size for coronary grafting, as measured at a pressure of 100 mm Hg, which is between 2.0 and 2.5 mm [21]. However, there are some specific concerns. The adequacy of the size of the IMA has been discussed, although there is general agreement that the size of the left IMA (LIMA) is usually adequate for the left anterior descending coronary artery. The RA is larger than other arterial conduits and is larger than the coronary arteries and is therefore not of concern [54]. In contrast, the IEA is normally small, and the distal end of the IEA is often very small (1 to 1.2 mm), so that adequacy of size is questionable, unless it is used as a composite graft to the LIMA [55]. Fewer questions on the size of the GEA have been raised, although the GEA may appear small during harvesting because of the frequent spasm of this spastic artery. The size of the intercostal artery may be small under most situations, and it has not been developed as a graft. Recent studies have addressed adequate perfusion of arterial grafts and found that the myocardium may be hypoperfused by arterial grafts [56]. During exercise, the flow reserve of the arterial graft may not be adequate. Therefore, it is probably necessary to consider the size of the graft in relation to a particular coronary branch.

Thickness of the wall and intimal hyperplasia
The combined width of the intima and media is as follows: [4]. The correlation between the thickness of the vascular wall and the development of atherosclerosis or graft occlusion is still unknown. Intimal hyperplasia has been suggested to be an adverse effect of long-term patency [4], but this is still speculative, and there are no clinical data to support this hypothesis.

Anatomic structure of the graft
The IMA is an elastic artery with well-formed internal elastic laminae, whereas the IEA, the GEA, and particularly the RA are muscular [4]. It has been speculated that more elastic structure is favorable for higher long-term patency [4], but this hypothesis needs to be supported by more clinical data.

Adequate length
Insofar as usable length is concerned, the LIMA has an adequate length for the left anterior descending coronary artery system. The RA has an adequate length for grafting to any coronary artery branch, with an average length of 20.5 cm (range, 15.2 to 23.5 cm) [57]. In contrast, the maximal length of the IEA is 17 cm (range, 15 to 22 cm), measured at autopsy [37]. Because of its very small diameter at the distal end, the available length is sometimes limited [55, 58]. In a study by Buche [58], the average length of the right IEA was 13.1 ± 1.3 cm, although by extensive dissection the IEA could be as long as 19 cm [58]. Buche [58] also suggests that the IEA be harvested only when the length and size are adequate on routine preoperative angiography. Together with other considerations, the IEA has been used as a part of a composite graft with the LIMA [55]. The pedicle GEA has adequate length for grafting to the posterior descending coronary artery, the most common target vessel for the GEA [17, 50], and to the obtuse marginal arteries [50].

Pedicle versus free graft
In a recent report, free grafts of the IMA reached patency rates similar to those for the pedicle IMA [59]; however, other studies [53] have disagreed with this finding. Dion [53] reported an 80% patency rate for free IMA grafts versus 96% for in situ grafts. A pedicle graft may be more physiologic than the free graft, as would be true for the GEA. Furthermore, a pedicle graft would have an intact vaso vasorum supply to the wall of the graft, whereas the free graft can only be nourished from the intraluminal blood supply, which may not be adequate. Finally, although the role of nerve supply to the arterial graft is not well established, physiologically it may play a role in the integrity of the graft as an organ and may therefore play a role in superior long-term patency. For these reasons, if a pedicle graft can be used, then it is always the choice.

Incidence of spasm
As mentioned previously, a less spastic graft would have fewer postoperative ischemic problems and better long-term patency [21, 25, 26]. Type I arteries (the IMA and IEA) fall into this category. However, as long as the spastic characteristics are taken into account, as for the GEA and RA, adequate pharmacologic therapy may achieve results similar to those of the type I arteries [17, 26, 49]. The revival of the RA is a typical example. The incidence of spasm during harvesting may be also related to technique. Gentle manipulation may reduce the incidence of spasm, but there is no evidence to show that spasm can be totally avoided by gentle harvesting without pharmacologic intervention.

Incidence of atherosclerosis and occlusion rate
Arteries with a low incidence of atherosclerosis are favorable grafts. The IMA is a typical example. The GEA also has a low incidence of atherosclerosis [4, 37, 46], and it is a favorable graft from this point of view. In contrast, the IEA, at least at the proximal portion, has a high incidence of atherosclerosis [23, 37] and is therefore not as satisfactory as the IMA [58], unless used as part of a Y graft, as suggested by Calafiore [55], in which case the required length of the IEA is short, so the atherosclerotic proximal part can be resected. Medial calcifications (Monckeberg’s disease) are also seen in the IEA [60].

The incidence of atherosclerosis in the RA is unknown, but it has been observed that the RA has a higher degree of atherosclerosis than the IMA [61]. Furthermore, RA atherosclerosis is correlated to the presence of diabetes, aortofemoral disease, femoral–popliteal disease, age, and male gender [61]. The biological characteristics of the major arterial grafts are summarized as Table 1.

Status of the native coronary artery
The severity of native coronary artery disease is also a factor in determining the target vessel for arterial grafts. For example, It has been suggested that the target vessel for the IEA must be one that is completely occluded or severely stenotic, with low coronary resistance, and in territories not totally infarcted to avoid "string sign" [55].

Vessel match between graft and coronary artery
The match between the arterial graft and the native coronary artery includes matching the size and length, as previously discussed.

Technical considerations
Personal experience
The use of arterial grafts in large part depends on surgeon preferance, except for the use of the LIMA, which has been unanimously accepted as the choice for the left anterior descending coronary artery, unless there is a contraindication. The technique of arterial grafting is more difficult and time-consuming than that for venous grafts, particularly when multiple arterial grafts are used.

Antispastic protocol
As previously mentioned, antispastic therapy plays an important role in some circumstances, such as RA grafting, because antispastic therapy is the key to the revival of use of the RA. Various antispastic agents have been suggested. Papaverine, despite its acidic nature is still widely used. Nitrovasodilators are also recommended [49, 62–64]. Use of the calcium antagonist diltiazem is key to the revival of the RA [26], and other calcium antagonists, such as verapamil, have also recently been used [49]. The combination of vasodilators may achieve even better antispastic effects. For example, nitroglycerin and verapamil can be effectively used together [49], and this mixture of pharmacologic agents, but not papaverine, has been demonstrated to maximally preserve the endothelium in the RA [65]. Challenge of new vasodilators in arterial grafts, such as the use of the PDE inhibitor milrinone [66], potassium channel openers [67], and TXA₂ antagonists [34] opens a new era in the antispastic therapy of arterial grafts.

	Conclusions

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 
Arterial grafts are biologically divergent conductance arteries. Although it has been shown that use of arterial grafts may achieve superior long-term patency, unanimous opinion as to how best to use these grafts has not been formed. Clinical choice of grafts must be based on the general condition of the patient, the biological characteristics of the graft, the anatomy of the coronary artery, the match between the coronary artery and the graft, and technical considerations, including antispastic management.

	Acknowledgments

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 
This work was supported by Hong Kong Research Grants Council grant 338/048/0004, Committee of Research and Conference grants 337/048/0018 and 335/048/0079, and University grant 014/048/9602 and 344/048/0001 from the University of Hong Kong.

Professor He is a member of the Institute of Cardiovascular Science and Medicine, The University of Hong Kong.

	References

Top Abstract Introduction Biological characteristics Functional classification Considerations in choosing... Conclusions Acknowledgments References

 

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