Coding cerebral bypasses: a proposed nomenclature to better describe bypass constructs and revascularization techniques

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  • 1 Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona; and
  • | 2 Department of Neurological Surgery, Rutgers New Jersey Medical School, Newark, New Jersey
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OBJECTIVE

Bypass surgery has evolved into a complex surgical art with a variety of donor arteries, recipient arteries, interpositional grafts, anastomoses, and suturing techniques. Although innovation in contemporary bypasses has increased, the literal descriptions of these new bypasses have not kept pace. The existing nomenclature that joins donor and recipient arteries with a hyphen is simplistic, underinformative, and in need of improvement. This article proposes a nomenclature that systematically incorporates anatomical and technical details with alphanumeric abbreviations and is a clear, concise, and practical “code” for bypass surgery.

METHODS

Detailed descriptions and illustrations of the proposed nomenclature, which consists of abbreviations for donor and recipient arteries, arterial segments, arteriotomies, and sides (left or right), with hyphens and parentheses to denote the arteriotomies joined in the anastomosis and brackets and other symbols for combination bypasses, are presented. The literature was searched for articles describing bypasses, and descriptive nomenclature was categorized as donor and recipient arteries (donor-recipient), donor-recipient with additional details, less detail than donor-recipient, and complete, ambiguous, or descriptive text.

RESULTS

In 483 publications, most bypass descriptions were categorized as donor-recipient (335, 69%), with superficial temporal artery–middle cerebral artery bypass described most frequently (299, 62%). Ninety-seven articles (20%) used donor-recipient descriptions with additional details, 45 (9%) were categorized as ambiguous, and none contained a complete bypass description. The authors found the proposed nomenclature to be easily applicable to the more complex bypasses reported in the literature.

CONCLUSIONS

The authors propose a comprehensive nomenclature based on segmental anatomy and additional anastomotic details that allows bypasses to be coded simply, succinctly, and accurately. This alphanumeric shorthand allows greater precision in describing bypasses and clarifying technical details, which may improve reporting in the literature and thus help to advance the field of bypass surgery.

ABBREVIATIONS

ACA = anterior cerebral artery; ACoA = anterior communicating artery; c = continuous suturing technique; CmaA = callosomarginal artery; D-R = donor-recipient; DT = descriptive text; ECA = external carotid artery; EC-IC = extracranial to intracranial; E-E = end-to-end; E-S = end-to-side; f = frontal; i = interrupted suturing technique; IC-IC = intracranial to intracranial; L = left; MCA = middle cerebral artery; MCoA = middle communicating artery; p = parietal; PcaA = pericallosal artery; PICA = posterior inferior cerebellar artery; R = right; RAG = radial artery graft; S-S = side-to-side; STA = superficial temporal artery; SVG = saphenous vein graft; t = temporal; YRAG = Y-shaped RAG; YSTA = Y-shaped STA graft; * = intraluminal suturing technique.

OBJECTIVE

Bypass surgery has evolved into a complex surgical art with a variety of donor arteries, recipient arteries, interpositional grafts, anastomoses, and suturing techniques. Although innovation in contemporary bypasses has increased, the literal descriptions of these new bypasses have not kept pace. The existing nomenclature that joins donor and recipient arteries with a hyphen is simplistic, underinformative, and in need of improvement. This article proposes a nomenclature that systematically incorporates anatomical and technical details with alphanumeric abbreviations and is a clear, concise, and practical “code” for bypass surgery.

METHODS

Detailed descriptions and illustrations of the proposed nomenclature, which consists of abbreviations for donor and recipient arteries, arterial segments, arteriotomies, and sides (left or right), with hyphens and parentheses to denote the arteriotomies joined in the anastomosis and brackets and other symbols for combination bypasses, are presented. The literature was searched for articles describing bypasses, and descriptive nomenclature was categorized as donor and recipient arteries (donor-recipient), donor-recipient with additional details, less detail than donor-recipient, and complete, ambiguous, or descriptive text.

RESULTS

In 483 publications, most bypass descriptions were categorized as donor-recipient (335, 69%), with superficial temporal artery–middle cerebral artery bypass described most frequently (299, 62%). Ninety-seven articles (20%) used donor-recipient descriptions with additional details, 45 (9%) were categorized as ambiguous, and none contained a complete bypass description. The authors found the proposed nomenclature to be easily applicable to the more complex bypasses reported in the literature.

CONCLUSIONS

The authors propose a comprehensive nomenclature based on segmental anatomy and additional anastomotic details that allows bypasses to be coded simply, succinctly, and accurately. This alphanumeric shorthand allows greater precision in describing bypasses and clarifying technical details, which may improve reporting in the literature and thus help to advance the field of bypass surgery.

In Brief

Bypass surgery has evolved into a complex art that incorporates a variety of donors, recipients, interpositional grafts, anastomoses, and suturing techniques. Given these contemporary advancements in bypass techniques, the existing nomenclature that joins abbreviations for donor and recipient arteries with a hyphen is simplistic and uninformative. The authors propose a new nomenclature system based on segmental anatomy and anastomotic details that uses alphanumeric shorthand to code bypasses simply, succinctly, and accurately and clarify technical details, thus encouraging greater descriptive precision.

The superficial temporal artery–middle cerebral artery (STA-MCA) bypass was introduced more than 50 years ago, and the craft involved in bypass surgery remains simple, with surgeons relying on suturing and basic instruments, three different types of anastomoses, minimal technology, and manual dexterity. Nonetheless, creative neurosurgeons have advanced bypass surgery into a complex surgical art by developing an array of bypasses that include standard extracranial-to-intracranial (EC-IC) bypass using scalp arteries, EC-IC with interpositional grafts, and intracranial-to-intracranial (IC-IC) bypass to reimplant, reanastomose, and communicate with cerebral arteries without the use of EC donors and sometimes with the use of IC jump grafts.1–8 Bypass surgery has also evolved through the use of a variety of donor arteries, recipient arteries, interpositional grafts, anastomoses, and suturing techniques. Despite inherent anatomical and technical limitations, bypass surgery is one of only a few constructive rather than deconstructive procedures in neurosurgery, and it fosters innovation. The literature is full of bypass inventions that adapt a patient’s unique arterial anatomy to revascularize brain tissue after trapping, occluding, or obliterating vascular pathology.9–23

Although the levels of innovation, technical skill, and complexity evident in contemporary bypasses have increased, the literal descriptions of these new bypasses have not kept pace. A system of symbols has been developed to sketch bypasses,3 and although this system is valuable in the context of a textbook,24 its broader application to communications and publications is difficult to achieve. Most bypasses are written as the names of the donor and recipient arteries joined with a hyphen, as in the prototypical STA-MCA bypass. These descriptions are simplistic, underinformative, and inadequate. For example, the STA-MCA bypass is usually constructed with an end-to-side anastomosis to a cortical M4 branch through a small frontotemporal craniotomy. However, it might also be constructed with an end-to-end anastomosis to an insular M2 branch deep in the sylvian fissure through a pterional craniotomy. Proper bypass nomenclature should capture these differences in construction and technique.

The existing nomenclature is often ambiguous and may even be inaccurate. Therefore, an updated, improved system is needed. In descriptions of cerebral bypasses, donor and recipient arteries are essential and form the basis of the current nomenclature, but fundamental elements are missing, such as segmental anatomy, or the “address” of the bypass; the type of anastomosis (end-to-side, end-to-end, or side-to-side); and any special techniques, like extraluminal versus intraluminal suturing. Other descriptors, like left- and right-sidedness and the type of interpositional graft, should also be included. A better bypass nomenclature would include all of these missing elements to enable a complete description of bypass construction. In contrast to that of previous systems, we propose a method that uses an alphanumeric code that can describe specific bypasses more quickly and without drawings because the descriptive elements are systematically incorporated with alphanumeric abbreviations. We have sought to make this code for bypass surgery terminology clear, concise, and unambiguous to offer an easy shorthand for complex operations. We have found the proposed nomenclature to be simple, practical, and easy to learn, and its use may enhance understanding of bypass procedures, clarify important technical nuances, and improve communications and publications.

Methods

Proposed Nomenclature for Cerebral Bypasses

In its simplest form, a bypass consists of a donor artery and a recipient artery, the anastomosis that joins them, and left- or right-sidedness. Therefore, in the proposed system, the basic code consists of side (right or left), arterial segment, and arteriotomy in the anastomosis for both the donor and recipient arteries (Fig. 1). The most important details are the specific anatomical locations of the bypass donor and recipient sites, which require abbreviations for the parent artery (e.g., external carotid artery [ECA] or pericallosal artery [PcaA]) (Table 1) and one of the main cerebral or cerebellar arteries for the segmental address (e.g., M2, A3, s1) (Table 2, Fig. 2). Alphanumeric descriptions of segmental anatomy were established by Rhoton and colleagues for cerebral arteries in uppercase25 and by Lawton and colleagues for cerebellar arteries in lowercase.26 In the proposed nomenclature, parent artery abbreviations with a segmental address are redundant and are therefore excluded to simplify the code. For example, an M4 MCA recipient artery would be described only as M4 in the standard bypass nomenclature for moyamoya disease. Branch arteries, or those without a segmental address, are described with the parent artery abbreviations. The donor artery precedes the recipient artery in the nomenclature, reflecting the direction of anterograde blood flow in the bypass.

FIG. 1.
FIG. 1.

Formula for cerebral bypass coding. Each artery involved in a bypass is codified by four primary elements: the side, an arterial segment, an arterial abbreviation, and an arteriotomy. Donor and recipient sites with a segmental address need not include the corresponding arterial abbreviation. Donor and recipient sites without a segmental address require an arterial abbreviation. The parentheses and a hyphen group the arteriotomies that are sutured together in the anastomosis. A fifth element denotes the suturing technique; for example, the asterisk (*) indicates an intraluminal suturing technique. Please refer to Tables 1 and 2 for the lists of artery and segment abbreviations, respectively, used in all of the figures.

TABLE 1.

Abbreviations for cranial arteries used in bypass procedures for the proposed nomenclature

AbbreviationArtery Name
ACAAnterior cerebral artery
AChAAnterior choroidal artery
ACoAAnterior communicating artery
AICAAnterior inferior cerebellar artery
AIFAAnterior internal frontal artery
AngAAngular artery
APAAnterior parietal artery
ATAAnterior temporal artery
BABasilar artery
CalcACalcarine artery
CenACentral artery
CmaACallosomarginal artery
ECAExternal carotid artery
FPAFrontopolar artery
fSTAFrontal branch of STA
ICAInternal carotid artery
IMAInternal maxillary artery
InfTrInferior trunk of MCA
IPAInferior parietal artery
MCAMiddle cerebral artery
MidTrMiddle trunk of MCA
MMAMiddle meningeal artery
MTAMiddle temporal artery
OFAOrbitofrontal artery
OphAOphthlamic artery
PAAPosterior auricular artery
PCAPosterior cerebral artery
PcaAPericallosal artery
PCenAParacentral artery
PCoAPosterior communicating artery
PFAPrefrontal artery
PICAPosterior inferior cerebellar artery
PIFAPosterior internal frontal artery
POAParieto-occipital artery
PoCenAPostcentral artery
PPAPosterior parietal artery
PrCenAPrecentral artery
pSTAParietal branch of STA
PTAPosterior temporal artery
RAHRecurrent artery of Heubner
SCASuperior cerebellar artery
SPASuperior parietal artery
STASuperficial temporal artery
SupTrSuperior trunk of MCA
TOATemporo-occipital artery
TPATemporopolar artery
VAVertebral artery
TABLE 2.

Abbreviations for arterial segments of intracranial arteries for the proposed nomenclature (segmental addresses)

Segment NumberArterySegment Name
C1ICACervical
C2ICAPetrous
C3ICALacerum
C4ICACavernous
C5ICAClinoidal
C6ICAOphthalmic
C7ICACommunicating
A1ACAPrecommunicating or horizontal
A2ACAPostcommunicating or infracallosal
A3ACAPrecallosal
A4ACASupracallosal
A5ACAPostcallosal
M1MCASphenoidal
M2MCAInsular
M3MCAOpercular
M4MCACortical
P1PCAPrecommunicating
P2PCAPostcommunicating
P2APCACrural
P2PPCAAmbient
P3PCAQuadrigeminal
P4PCACalcarine
s1SCAAnterior pontomesencephalic
s2SCALateral pontomesencephalic
s3SCACerebellomesencephalic
s4SCACortical
a1AICAAnterior pontine
a2AICALateral pontine
a3AICAFlocculopeduncular
a4AICACortical
p1PICAAnterior medullary
p2PICALateral medullary
p3PICATonsillomedullary
p4PICATelovelotonsillar
p5PICACortical
FIG. 2.
FIG. 2.

Schematic representation of MCA (left side) and ACA (right side) bypasses. CCA = common carotid artery; ICA = internal carotid artery; OA = occipital artery. Modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

In the proposed system, the hyphen continues to be used to depict the anastomosis connecting donor and recipient arteries. However, three different types of anastomoses join donor and recipient arteries, and this anastomotic detail is incorporated in the nomenclature by adding an abbreviation for the position of the arteriotomy (end [E], side [S]) on each side of the hyphen for the different anastomoses: end-to-side (E-S), end-to-end (E-E), or side-to-side (S-S). Sidedness (right [R] or left [L]) is included as a prefix to avoid having the anastomotic detail in the middle of the code. For example, the superficial STA-MCA bypass becomes the L STA (E-S) M4 bypass. Bypasses that are unilateral use one descriptor for the entire bypass, whereas bypasses that are bilateral need descriptors for both donor and recipient. For the posterior inferior cerebellar artery (PICA), for example, the PICA-PICA bypass between the caudal loops of the tonsillomedullary segments would be L p3 (S-S) R p3 bypass, with the flow in the completed construct coursing from left to right.

More complex bypasses have additional details and conventions. Interpositional bypasses require the description of the graft, which is typically a radial artery graft (RAG) or saphenous vein graft (SVG) but may also include other elements, such as the posterior tibial artery or lateral circumflex femoral artery. Interpositional grafts are inserted between donor and recipient abbreviations and are joined by the applicable anastomotic abbreviation, for example, R ECA (S-E) RAG (E-S) M2 bypass.

Combination bypasses are constructs with multiple anastomoses indicated by the use of the + sign. For example, a double-barrel STA-MCA bypass from the frontal branch of the STA (fSTA) and parietal branch of the STA (pSTA) to the superior and inferior trunks of an MCA bifurcation aneurysm would be described as R fSTA (E-S) M2 + pSTA (E-S) M2´, with a prime symbol used to denote a second and different M2 MCA recipient.

More complex combination bypasses require brackets positioned according to the mathematical distributive property, by which multiplying the sum of two or more addends by a number equals adding the products of each addend multiplied by the number individually: a × [b + c] = [a × b] + [a × c]. Similarly, with bypass code, a donor artery that supplies two recipients can be described with brackets and addition. For example, a double reimplantation bypass that revascularizes the superior and inferior trunks of an MCA bifurcation aneurysm with one high-flow graft from the left cervical carotid artery would be L ECA (S-E) RAG [(S-E) M2 + (E-S) M2´].

An additional detail is the type of suturing technique used. Bypasses are sewn with either interrupted or continuous sutures. In addition, most suture lines are sewn extraluminally but occasionally must be sewn intraluminally due to immobility of the arteries or other reasons. For example, the deep suture line of an S-S bypass ("in situ bypass") is sewn with running intraluminal suturing, and occasionally this technique is applied to the E-E and E-S anastomoses.27 These suturing technique details can be added to the nomenclature with superscripts within the anastomotic parentheses: “i” for interrupted, “c” for continuous, and “*” for intraluminal suturing technique. In the previous example, L ECA (S-E) RAG [(S-E) M2 + (E-S) M2´], this detail would be incorporated as follows: L ECA (S-Ec) RAG [(S-Ec*) M2 + (E-Sc*) M2´].

Literature Review

The English-language medical literature was reviewed using the PubMed database to search for combinations of the following keywords: “cerebral revascularization,” “cerebral bypass,” “intracranial,” “extracranial,” “aneurysm,” “vascular insufficiency,” and “complex,” which yielded 3643 articles. Articles using descriptions of bypasses were included and reviewed for incompleteness or ambiguity in the authors’ descriptive abbreviations. Cross-referencing was then performed to find any missing articles.

Bypass nomenclature found in the literature was categorized into four distinct groups as follows. A bypass was categorized as complete (C) if the nomenclature described the donor artery, recipient artery, segmental arterial anatomy, sidedness, interpositional graft (if any), and the type of anastomoses. A bypass described only by the donor and recipient arteries without any additional detail was categorized as donor-recipient (D-R; e.g., STA-MCA). A bypass described by the donor and recipient arteries with some additional details, such as the sidedness, the graft, or the segmental anatomy of the involved arteries, but without complete detail, was categorized as “donor-recipient plus” (D-R+; e.g., STA-M4 MCA bypass). A bypass described by less information than the donor and recipient arteries was categorized as donor-recipient minus (D-R−; e.g., STA bypass). A bypass described by a unique adjective or coined term was categorized as ambiguous (A; e.g., azygos bypass, bonnet bypass, or arborization bypass).21,28–34 Finally, a bypass described with detailed text for steps from beginning to end of the procedure was categorized as descriptive text (DT).

Results

Of the 3643 publications identified in the PubMed search, 483 were found that included at least one description of a cerebral bypass. STA-MCA bypass was the bypass described most frequently (62%). Most bypass descriptions were categorized into the D-R group (335 D-R, 69%). D-R+ descriptions with additional details were reported in 97 papers (20%), and D-R− descriptions with fewer details were reported in 56 papers (12%). No publication contained a complete description of a bypass. The bypasses in 45 articles (9.3%) were categorized as A (ambiguous), and in 135 articles (21.5%), bypasses were described with DT.

We were able to apply the proposed nomenclature to some of the most colorful and complex bypasses in the literature (Fig. 3A). Russin also described an “arborization” bypass to revascularize a fusiform M2 MCA aneurysm incorporating the origin of two temporal M3 (tM3) branches.9 The arborization used two consecutive S-S anastomoses, the first between an fM3 and one of the temporal branches, and the second between the two temporal branches at a point distal to the first anastomosis. The proposed nomenclature describes this bypass as L fM3 (S-S) tM3 + tM3 (S-S) tM3´. This combination bypass is indicated by the plus (+) sign. The M3´ indicates an M3 branch different from the branch involved in the S-S anastomosis between the temporal and frontal branches, and the prime symbol is used because these opercular segments lack distinct names.

FIG. 3.
FIG. 3.

Descriptions of complex bypasses with illustrations, symbol schematics (see Fig. 2 for the key), and proposed alphanumeric coding. A: Arborization bypass in the ACA territory: L CmaA (S-S*) R CmaA + L PcaA (S-S*) R PcaA. B: YSTA interpositional bypass in the ACA territory: L A2 (S-E) YSTA [(E-S) L A3 + (E-S) R A3]. C: Bonnet bypass: L STA (S-E) SVG (E-S*) R M2. Panels A left and C left published with permission from Barrow Neurological Institute, Phoenix, AZ. Panel B left from Endo H, Sugiyama SI, Endo T, et al. Revascularization of the anterior cerebral artery by Y-shaped superficial temporal artery interposition graft for the treatment of a de novo aneurysm arising at the site of A3-A3 bypass: technical case report. J Neurosurg. 2018;129(5):1120–1124. © 2018 Hidenori Endo; published with permission. Panels A right, B right, and C right modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

The double-limbed bypass uses a Y-shaped interpositional graft from a harvested STA trunk and its frontal and parietal branches (Fig. 3B). Endo et al. used a Y-shaped STA graft (YSTA) to revascularize a complex anterior communicating artery (ACoA) aneurysm, connecting a single proximal A2 anterior cerebral artery (ACA) donor and two bilateral A3 ACA recipients: L A2 (S-E) YSTA [(E-S) L A3 + (E-S) R A3].35 The brackets denote a combination bypass with two distal anastomoses supplied by a single graft. An RAG may also be refashioned into a Y-shaped graft (YRAG) to create a similar bypass.36 The “bonnet bypass” reported by Spetzler et al. is a construct that connects a contralateral STA donor to an ipsilateral MCA via a long graft over the convexity of the brain (Fig. 3C).37 The proposed nomenclature can readily capture different bonnet bypasses, for example, R STA (S-E) SVG (E-S) L M4.

Lawton and Quiñones-Hinojosa introduced double reimplantation bypass for reconstructing bifurcations after aneurysm trapping using a single nonbranched graft to supply two recipient arteries.38 The graft is connected proximally to the donor artery, and efferent branches are then reimplanted onto the graft with each subsequent anastomosis. This technique was first introduced as an EC-IC interpositional bypass: L ECA (E-E) SVG [(S-E) M2 + (E-S) M2´] (Fig. 4A). The double bypass technique then evolved to include an IC-IC interpositional bypass with the use of the A1 ACA as an intracranial donor site: L A1 (S-E) RAG [(S-S) M2 + (E-S) M2´] (Fig. 4B). This technique evolved further to include a “fourth-generation” IC-IC interpositional bypass with the use of intraluminal suturing for the reimplanted MCA trunks: R A1 (S-Ec) SVG [(S-Sc*) M2 + (E-Sc*) M2´]; the bypass may also be constructed with an RAG. The first reimplantation is an S-S anastomosis, and the second reimplantation uses intraluminal suturing to sew the deep suture line, both denoted with asterisks in the code (Fig. 4B). The double bypass technique may be similarly used for a triple bypass: L ECA (S-E) SVG [(S-E) M2 + (S-E) M2´ + (Ε-S) M2´´] (Fig. 4C).

FIG. 4.
FIG. 4.

Descriptions of complex bypasses with illustrations, symbol schematics (see Fig. 2 for the key), and proposed alphanumeric coding. A: Double reimplantation technique, EC-IC: L ECA (E-E) SVG [(S-E) M2 + (E-S) M2´]. B: Double reimplantation technique, IC-IC: L A1 (S-E) RAG [(S-S*) M2 + (E-S*) M2´]. C: Triple reimplantation technique, EC-IC: L ECA (S-E) SVG [(S-E) M2 + (S-E) M2´ + (E-S) M2´´]. Panel A left published with permission from Lawton MT, Quiñones-Hinojosa A. Double reimplantation technique to reconstruct arterial bifurcations with giant aneurysms. Neurosurgery. 2006;58(4)(suppl 2):ONS-347–ONS-354. By permission of the Congress of Neurological Surgeons. Panel B left published with permission from Barrow Neurological Institute, Phoenix, AZ. Panel C left reprinted by permission from Springer Nature: Acta Neurochir. Wessels L, Fekonja LS, Vajkoczy P. Bypass surgery of complex middle cerebral artery aneurysms—technical aspects and outcomes. © Springer-Verlag GmbH Austria 2019;161:1981–1991. Panels A right, B right, and C right modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

The azygos bypass is a double reimplantation bypass in the ACA territory with construction similar to that used in the treatment of a giant, thrombotic ACoA aneurysm.11 The name is ambiguous, but its code provides the complete details for azygos bypass construction, including the callosomarginal artery (CmaA): R PcaA (S-Ec) RAG [(S-Sc*) L PcaA + (E-Sc) L CmaA]. A different example of an azygos bypass is shown in Fig. 5A, and its details are captured completely by the code: L CmaA (S-E) RAG [(S-E*) R CmaA + (E-S) R PcaA].

FIG. 5.
FIG. 5.

Descriptions of complex bypasses with illustrations, symbol schematics (see Fig. 2 for the key), and proposed alphanumeric coding. A: Azygos bypass: L CmaA (S-E) RAG [(S-E*) R CmaA + (E-S) R PcaA]. B: MCoA, EC-IC: L fSTA (E-S) M2 + pSTA (E-S) M2´ + M2 (E-E*) M2´. C: MCoA, IC-IC: L A1 (S-E) RAG (E-S) M2 + M2 (E-E*) M2´. Panels A left, B left, and C left published with permission from Barrow Neurological Institute, Phoenix, AZ. Panels A right, B right, and C right modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

The middle communicating artery (MCoA) was recently introduced as a novel bypass construct between MCA trunks to redistribute flow in the MCA territory in response to changing supply and demand, analogous to the anterior and posterior communicating arteries. The MCoA has been created in three forms with three unique donors: 1) with a double-barrel STA (Fig. 5B), 2) with an interpositional graft from the cervical ECA, and 3) with an interpositional graft from the A1 ACA (Fig. 5C). The codes for these bypasses may appear cumbersome, but the nomenclature conveys details of these sophisticated bypasses that would be lost without it, like the use of the asterisk to denote intraluminal suturing (Fig. 6).

FIG. 6.
FIG. 6.

Case example of cerebral bypass coding of the MCoA, which exists only as a bypass construct and does not occur naturally and is constructed using the IC-IC interpositional bypass technique shown in Figure 5C. The intraoperative photographs show the creation of the bypass in a stepwise manner. A: Preoperative angiogram (left ICA angiogram, anteroposterior view) showing the aneurysm located at the MCA bifurcation with the frontal and temporal trunks originating from the base of the aneurysm. B: Intraoperative photograph of the MCA aneurysm in the sylvian fissure. C: Photograph of preparation for the proximal anastomosis in the construction of the MCoA, an A1 (S-E) RAG. D: Intraluminal inspection of the completed first suture line of the distal RAG anastomosis to M2. E: Photograph of the final anastomosis showing end-to-end reimplantation of the frontal and temporal trunks with intraluminal suturing of these two M2 segments. F: Photograph of the completed MCoA bypass with distal clip occlusion of the aneurysm. G: Postoperative angiogram (left ICA angiogram, anterior oblique view) showing the patency of the bypass and the filling of the distal MCA territory. Panels B–F published with permission from Barrow Neurological Institute, Phoenix, AZ.

A three-vessel anastomosis recently proposed by Ravina et al. used a single-donor graft to revascularize two parallel A3 ACAs joined with a half-completed S-S anastomosis.13 Two ACAs were sewn together along the deep suture line, and the donor graft was sewn to these half-joined ACAs.13 This innovative bypass could be coded as R STA (E-E) RAG (E-S) [L A3 (1/2S-1/2S) R A3].

Discussion

The literature review performed in this study demonstrates the significant ambiguity and imprecision of the existing nomenclature for the reporting of cerebral bypasses in the literature. The current nomenclature is simplistic, prevents a thorough understanding of bypass construction, and omits critical technical details. We propose a new systematic nomenclature that is clear and concise and addresses the current deficiencies of naming bypasses found in the literature. The proposed nomenclature encourages greater precision in describing bypasses, includes technical details that can advance the field, and may improve bypass reporting in the literature. Bypass surgery is remarkably innovative, with novel bypasses appearing regularly in the literature. The adoption of improved and descriptive nomenclature would help capture this dynamic evolution.

There is no substitute for carefully curated intraoperative photographs, videos, and illustrations depicting the stepwise construction of a complex bypass.1,39–42 However, these media are not often available, take time to produce, and can be costly. Previously, we introduced a system of symbols (Fig. 2) to diagram bypasses with the intent to improve communication.3,24 These symbols are also meant to help bypass surgeons design novel bypasses and hone new bypass concepts. The symbols allow the creation of bypass blueprints before surgery and graphic communication afterward. Although this system of symbols is a valuable teaching tool for compiling cases in a textbook, it has proven to be less applicable as a communication tool or a reporting standard. It is difficult to produce these bypass blueprints for publications or the medical record because there are no commercially available graphic tools for bypasses like those available in architecture, for example. Therefore, written shorthand for bypasses is more likely to have the desired communication impact than symbolic shorthand.

Our proposed nomenclature is simple, succinct, and clear. It is modeled after mathematical formulas, and simple principles like the distributive property can be applied. Critical information is contained within the abbreviated code that can be deciphered and understood by neurosurgeons. Unusual bypass constructs in the literature were easily captured, with high interobserver reliability. In addition, neurosurgeons reading the code have deciphered the constructs with high interobserver reliability. The bypass code includes the essential components of the construct and provides an accurate and precise shorthand description of the bypass for the operative team of assistant surgeons, residents, and nurses. This shorthand can reduce errors, facilitate safe surgery, and improve documentation in the medical record.

The proposed nomenclature enhances the description of the bypass but does not explicitly describe the surgical approach. The nomenclature captures the segmental anatomy, which is suggestive of the approach. For example, an R STA (E-S) s1 bypass would be approached through an orbitozygomatic transsylvian approach to the oculomotor-tentorial triangle, whereas an R STA (E-S) s2 bypass would be approached through a subtemporal approach to the ambient cistern. Statistics on interobserver reliability were not performed because of the limited number of authors. We believe the proposed nomenclature is intuitive, easy to learn, and widely applicable. We introduce it with the hope that other bypass surgeons find value in it, adopt it in their publications and presentations, and ultimately elevate the discourse on bypass surgery.

Conclusions

Bypasses are becoming increasingly complex with the expansion of IC-IC techniques. Descriptions of these constructs with existing nomenclature may be imprecise or confusing, and illustrations and symbolic schematics may not be available. We propose a comprehensive nomenclature based on the segmental anatomy and additional anastomotic details that enables bypasses to be coded simply, succinctly, and accurately. The alphanumeric shorthand encourages greater precision in describing bypasses, improves our reporting in the literature, and includes technical details that could advance the field of bypass surgery.

Acknowledgments

We thank the staff of Neuroscience Publications at Barrow Neurological Institute for assistance with manuscript preparation, illustrations, and graphical application development.

Addendum

Consistent and accurate representation of increasingly complex bypass techniques is a challenge. Ambiguity and lack of a standard nomenclature that captures the nuances of contemporary bypass techniques confound the medical literature and impede the neurosurgical advancement of bypass techniques. We have developed an innovative, standardized bypass coding nomenclature that can code basic to elegantly complex bypasses simply and accurately.

To introduce the nomenclature and make it easy to understand and adopt, we have developed a web-based graphical application that translates visual, onscreen bypass input into the written code (Video 1).

VIDEO 1. Barrow Bypass Coder. This web-based interactive tool allows users to indicate pathologies, build bypasses, and generate the detailed bypass code. Copyright Barrow Neurological Institute, Phoenix, AZ. Published with permission. Click here to view.

The desktop computer app is designed for neurosurgeons and neurosurgery residents. It features drag-and-drop symbols for pathologies and treatments and editable blood vessels and grafts to generate the written code. You can find it on the Barrow Neurological Institute website by searching “Barrow Bypass Coder.”

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Lawton, Tayebi Meybodi. Acquisition of data: Tayebi Meybodi, Gadhiya, Borba Moreira. Analysis and interpretation of data: Lawton, Tayebi Meybodi. Drafting the article: Lawton, Tayebi Meybodi. Critically revising the article: Lawton, Tayebi Meybodi. Reviewed submitted version of manuscript: Lawton, Tayebi Meybodi. Statistical analysis: Lawton, Tayebi Meybodi. Administrative/technical/material support: Lawton, Tayebi Meybodi. Study supervision: Lawton.

Supplemental Information

Videos

References

  • 1

    Wessels L, Fekonja LS, Vajkoczy P. Bypass surgery of complex middle cerebral artery aneurysms—technical aspects and outcomes. Acta Neurochir (Wien). 2019;161(10):19811991.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Natarajan SK, Zeeshan Q, Ghodke BV, Sekhar LN. Brain bypass surgery for complex middle cerebral artery aneurysms: evolving techniques, results, and lessons learned. World Neurosurg. 2019;130:e272e293.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Tayebi Meybodi A, Huang W, Benet A, et al. Bypass surgery for complex middle cerebral artery aneurysms: an algorithmic approach to revascularization. J Neurosurg. 2017;127(3):463479.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Sanai N, Zador Z, Lawton MT. Bypass surgery for complex brain aneurysms: an assessment of intracranial-intracranial bypass. Neurosurgery. 2009;65(4):670683.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Baranoski JF, Przybylowski CJ, Mascitelli JR, et al. Anterior inferior cerebellar artery bypasses: the 7-bypass framework applied to ischemia and aneurysms in the cerebellopontine angle. Oper Neurosurg (Hagerstown). 2020;19(2):165174.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Tayebi Meybodi A, Benet A, Lawton MT. The V3 segment of the vertebral artery as a robust donor for intracranial-to-intracranial interpositional bypasses: technique and application in 5 patients. J Neurosurg. 2018;129(3):691701.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Rubio RR, Gandhi S, Vigo V, et al. an anatomic feasibility study for revascularization of the ophthalmic artery, part I: intracanalicular segment. World Neurosurg. 2020;133:e893e901.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Tayebi Meybodi A, Lawton MT, Griswold D, et al. Revascularization of the upper posterior circulation with the anterior temporal artery: an anatomical feasibility study. J Neurosurg. 2018;129(1):121127.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Russin JJ. The arborization bypass: sequential intracranial-intracranial bypasses for an unruptured fusiform MCA aneurysm. J Clin Neurosci. 2017;39:209211.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kato N, Prinz V, Finger T, et al. Multiple reimplantation technique for treatment of complex giant aneurysms of the middle cerebral artery: technical note. Acta Neurochir (Wien). 2013;155(2):261269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Mirzadeh Z, Sanai N, Lawton MT. The azygos anterior cerebral artery bypass: double reimplantation technique for giant anterior communicating artery aneurysms. J Neurosurg. 2011;114(4):11541158.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Lee SH, Choi SK. In situ intersegmental anastomosis within a single artery for treatment of an aneurysm at the posterior inferior cerebellar artery: closing omega bypass. J Korean Neurosurg Soc. 2015;58(5):467470.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Ravina K, Yim B, Lam J, et al. Three-vessel anastomosis for direct bihemispheric cerebral revascularization. Oper Neurosurg (Hagerstown). 2020;19(3):313318.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Benet A, Montemurro N, Lawton MT. Management of a ruptured posterior inferior cerebellar artery (PICA) aneurysm with PICA-PICA in situ bypass and trapping: 3-dimensional operative video. Oper Neurosurg (Hagerstown). 2017;13(3):400.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Meybodi AT, Lawton MT, Benet A. Sequential extradural release of the V3 vertebral artery to facilitate intradural V4 vertebral artery reanastomosis: feasibility of a novel revascularization technique. Oper Neurosurg (Hagerstown). 2017;13(3):345351.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Lawton MT, Abla AA, Rutledge WC, et al. Bypass surgery for the treatment of dolichoectatic basilar trunk aneurysms: a work in progress. Neurosurgery. 2016;79(1):8399.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Abla AA, Lawton MT. Revascularization for unclippable posterior inferior cerebellar artery aneurysms: extracranial-intracranial or intracranial-intracranial bypass? World Neurosurg. 2014;82(5):586588.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Tayebi Meybodi A, Lawton MT, Griswold D, et al. The anterior temporal artery: an underutilized but robust donor for revascularization of the distal middle cerebral artery. J Neurosurg. 2017;127(4):740747.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Kalani MY, Ramey W, Albuquerque FC, et al. Revascularization and aneurysm surgery: techniques, indications, and outcomes in the endovascular era. Neurosurgery. 2014;74(5):482498.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Abla AA, Lawton MT. The superficial temporal artery trunk-to-M2 middle cerebral artery bypass with short radial artery interposition graft: the forgotten bypass. World Neurosurg. 2015;83(2):145146.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Abla AA, Lawton MT. Anterior cerebral artery bypass for complex aneurysms: an experience with intracranial-intracranial reconstruction and review of bypass options. J Neurosurg. 2014;120(6):13641377.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Tayebi Meybodi A, Lawton MT, Griswold D, et al. Assessment of the temporopolar artery as a donor artery for intracranial-intracranial bypass to the middle cerebral artery: anatomic feasibility study. World Neurosurg. 2017;104:171179.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Mura J, Riquelme F, Cuevas JL, et al. Simplified azygos anterior cerebral bypass: y-shaped superficial temporal artery interposition graft from A2 with double reimplantation of pericallosal arteries: technical case report. Neurosurgery. 2013;72(2 Suppl Operative):onsE235ons240.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. Thieme; 2018.

  • 25

    Rhoton AL Jr. The supratentorial arteries. Neurosurgery. 2002;51 (4)(suppl):S53S120.

  • 26

    Rodríguez-Hernández A, Rhoton AL Jr, Lawton MT. Segmental anatomy of cerebellar arteries: a proposed nomenclature. Laboratory investigation. J Neurosurg. 2011;115(2):387397.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Lawton MT, Lang MJ. The future of open vascular neurosurgery: perspectives on cavernous malformations, AVMs, and bypasses for complex aneurysms. J Neurosurg. 2019;130(5):14091425.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Duckworth EA, Rao VY, Patel AJ. Double-barrel bypass for cerebral ischemia: technique, rationale, and preliminary experience with 10 consecutive cases. Neurosurgery. 2013;73(1 Suppl Operative):ons30-8ons37-8.

    • Search Google Scholar
    • Export Citation
  • 29

    Nakajima H, Kamiyama H, Nakamura T, et al. Direct surgical treatment of giant intracranial aneurysms on the anterior communicating artery or anterior cerebral artery. Neurol Med Chir (Tokyo). 2013;53(3):153156.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Cantore G, Santoro A, Guidetti G, et al. Surgical treatment of giant intracranial aneurysms: current viewpoint. Neurosurgery. 2008;63(4)(suppl 2):279290.

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    Hongo K, Horiuchi T, Nitta J, et al. Double-insurance bypass for internal carotid artery aneurysm surgery. Neurosurgery. 2003;52(3):597602.

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    Otani N, Wada K, Sakakibara F, et al. “Reverse” bypass using a naturally formed “bonnet” superficial temporal artery in symptomatic common carotid artery occlusion: a case report. Neurol Med Chir (Tokyo). 2014;54(10):851853.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Bulsara KR, Patel T, Fukushima T. Cerebral bypass surgery for skull base lesions: technical notes incorporating lessons learned over two decades. Neurosurg Focus. 2008;24(2):E11.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Wada K, Otani N, Toyooka T, et al. Superficial temporal artery to anterior cerebral artery hemi-bonnet bypass using radial artery graft for prevention of complications after surgical treatment of partially thrombosed large/giant anterior cerebral artery aneurysm. J Stroke Cerebrovasc Dis. 2018;27(12):35053510.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Endo H, Sugiyama SI, Endo T, et al. Revascularization of the anterior cerebral artery by Y-shaped superficial temporal artery interposition graft for the treatment of a de novo aneurysm arising at the site of A3-A3 bypass: technical case report. J Neurosurg. 2018;129(5):11201124.

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Illustration from Schneider et al. (pp 205–214). Copyright Elyssa Siegel. Published with permission.

  • View in gallery

    Formula for cerebral bypass coding. Each artery involved in a bypass is codified by four primary elements: the side, an arterial segment, an arterial abbreviation, and an arteriotomy. Donor and recipient sites with a segmental address need not include the corresponding arterial abbreviation. Donor and recipient sites without a segmental address require an arterial abbreviation. The parentheses and a hyphen group the arteriotomies that are sutured together in the anastomosis. A fifth element denotes the suturing technique; for example, the asterisk (*) indicates an intraluminal suturing technique. Please refer to Tables 1 and 2 for the lists of artery and segment abbreviations, respectively, used in all of the figures.

  • View in gallery

    Schematic representation of MCA (left side) and ACA (right side) bypasses. CCA = common carotid artery; ICA = internal carotid artery; OA = occipital artery. Modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

  • View in gallery

    Descriptions of complex bypasses with illustrations, symbol schematics (see Fig. 2 for the key), and proposed alphanumeric coding. A: Arborization bypass in the ACA territory: L CmaA (S-S*) R CmaA + L PcaA (S-S*) R PcaA. B: YSTA interpositional bypass in the ACA territory: L A2 (S-E) YSTA [(E-S) L A3 + (E-S) R A3]. C: Bonnet bypass: L STA (S-E) SVG (E-S*) R M2. Panels A left and C left published with permission from Barrow Neurological Institute, Phoenix, AZ. Panel B left from Endo H, Sugiyama SI, Endo T, et al. Revascularization of the anterior cerebral artery by Y-shaped superficial temporal artery interposition graft for the treatment of a de novo aneurysm arising at the site of A3-A3 bypass: technical case report. J Neurosurg. 2018;129(5):1120–1124. © 2018 Hidenori Endo; published with permission. Panels A right, B right, and C right modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

  • View in gallery

    Descriptions of complex bypasses with illustrations, symbol schematics (see Fig. 2 for the key), and proposed alphanumeric coding. A: Double reimplantation technique, EC-IC: L ECA (E-E) SVG [(S-E) M2 + (E-S) M2´]. B: Double reimplantation technique, IC-IC: L A1 (S-E) RAG [(S-S*) M2 + (E-S*) M2´]. C: Triple reimplantation technique, EC-IC: L ECA (S-E) SVG [(S-E) M2 + (S-E) M2´ + (E-S) M2´´]. Panel A left published with permission from Lawton MT, Quiñones-Hinojosa A. Double reimplantation technique to reconstruct arterial bifurcations with giant aneurysms. Neurosurgery. 2006;58(4)(suppl 2):ONS-347–ONS-354. By permission of the Congress of Neurological Surgeons. Panel B left published with permission from Barrow Neurological Institute, Phoenix, AZ. Panel C left reprinted by permission from Springer Nature: Acta Neurochir. Wessels L, Fekonja LS, Vajkoczy P. Bypass surgery of complex middle cerebral artery aneurysms—technical aspects and outcomes. © Springer-Verlag GmbH Austria 2019;161:1981–1991. Panels A right, B right, and C right modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

  • View in gallery

    Descriptions of complex bypasses with illustrations, symbol schematics (see Fig. 2 for the key), and proposed alphanumeric coding. A: Azygos bypass: L CmaA (S-E) RAG [(S-E*) R CmaA + (E-S) R PcaA]. B: MCoA, EC-IC: L fSTA (E-S) M2 + pSTA (E-S) M2´ + M2 (E-E*) M2´. C: MCoA, IC-IC: L A1 (S-E) RAG (E-S) M2 + M2 (E-E*) M2´. Panels A left, B left, and C left published with permission from Barrow Neurological Institute, Phoenix, AZ. Panels A right, B right, and C right modified with permission from Thieme Medical Publishers from Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. New York: Thieme; 2018.

  • View in gallery

    Case example of cerebral bypass coding of the MCoA, which exists only as a bypass construct and does not occur naturally and is constructed using the IC-IC interpositional bypass technique shown in Figure 5C. The intraoperative photographs show the creation of the bypass in a stepwise manner. A: Preoperative angiogram (left ICA angiogram, anteroposterior view) showing the aneurysm located at the MCA bifurcation with the frontal and temporal trunks originating from the base of the aneurysm. B: Intraoperative photograph of the MCA aneurysm in the sylvian fissure. C: Photograph of preparation for the proximal anastomosis in the construction of the MCoA, an A1 (S-E) RAG. D: Intraluminal inspection of the completed first suture line of the distal RAG anastomosis to M2. E: Photograph of the final anastomosis showing end-to-end reimplantation of the frontal and temporal trunks with intraluminal suturing of these two M2 segments. F: Photograph of the completed MCoA bypass with distal clip occlusion of the aneurysm. G: Postoperative angiogram (left ICA angiogram, anterior oblique view) showing the patency of the bypass and the filling of the distal MCA territory. Panels B–F published with permission from Barrow Neurological Institute, Phoenix, AZ.

  • 1

    Wessels L, Fekonja LS, Vajkoczy P. Bypass surgery of complex middle cerebral artery aneurysms—technical aspects and outcomes. Acta Neurochir (Wien). 2019;161(10):19811991.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Natarajan SK, Zeeshan Q, Ghodke BV, Sekhar LN. Brain bypass surgery for complex middle cerebral artery aneurysms: evolving techniques, results, and lessons learned. World Neurosurg. 2019;130:e272e293.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Tayebi Meybodi A, Huang W, Benet A, et al. Bypass surgery for complex middle cerebral artery aneurysms: an algorithmic approach to revascularization. J Neurosurg. 2017;127(3):463479.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Sanai N, Zador Z, Lawton MT. Bypass surgery for complex brain aneurysms: an assessment of intracranial-intracranial bypass. Neurosurgery. 2009;65(4):670683.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Baranoski JF, Przybylowski CJ, Mascitelli JR, et al. Anterior inferior cerebellar artery bypasses: the 7-bypass framework applied to ischemia and aneurysms in the cerebellopontine angle. Oper Neurosurg (Hagerstown). 2020;19(2):165174.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Tayebi Meybodi A, Benet A, Lawton MT. The V3 segment of the vertebral artery as a robust donor for intracranial-to-intracranial interpositional bypasses: technique and application in 5 patients. J Neurosurg. 2018;129(3):691701.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Rubio RR, Gandhi S, Vigo V, et al. an anatomic feasibility study for revascularization of the ophthalmic artery, part I: intracanalicular segment. World Neurosurg. 2020;133:e893e901.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Tayebi Meybodi A, Lawton MT, Griswold D, et al. Revascularization of the upper posterior circulation with the anterior temporal artery: an anatomical feasibility study. J Neurosurg. 2018;129(1):121127.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Russin JJ. The arborization bypass: sequential intracranial-intracranial bypasses for an unruptured fusiform MCA aneurysm. J Clin Neurosci. 2017;39:209211.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Kato N, Prinz V, Finger T, et al. Multiple reimplantation technique for treatment of complex giant aneurysms of the middle cerebral artery: technical note. Acta Neurochir (Wien). 2013;155(2):261269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Mirzadeh Z, Sanai N, Lawton MT. The azygos anterior cerebral artery bypass: double reimplantation technique for giant anterior communicating artery aneurysms. J Neurosurg. 2011;114(4):11541158.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Lee SH, Choi SK. In situ intersegmental anastomosis within a single artery for treatment of an aneurysm at the posterior inferior cerebellar artery: closing omega bypass. J Korean Neurosurg Soc. 2015;58(5):467470.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Ravina K, Yim B, Lam J, et al. Three-vessel anastomosis for direct bihemispheric cerebral revascularization. Oper Neurosurg (Hagerstown). 2020;19(3):313318.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Benet A, Montemurro N, Lawton MT. Management of a ruptured posterior inferior cerebellar artery (PICA) aneurysm with PICA-PICA in situ bypass and trapping: 3-dimensional operative video. Oper Neurosurg (Hagerstown). 2017;13(3):400.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Meybodi AT, Lawton MT, Benet A. Sequential extradural release of the V3 vertebral artery to facilitate intradural V4 vertebral artery reanastomosis: feasibility of a novel revascularization technique. Oper Neurosurg (Hagerstown). 2017;13(3):345351.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Lawton MT, Abla AA, Rutledge WC, et al. Bypass surgery for the treatment of dolichoectatic basilar trunk aneurysms: a work in progress. Neurosurgery. 2016;79(1):8399.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Abla AA, Lawton MT. Revascularization for unclippable posterior inferior cerebellar artery aneurysms: extracranial-intracranial or intracranial-intracranial bypass? World Neurosurg. 2014;82(5):586588.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Tayebi Meybodi A, Lawton MT, Griswold D, et al. The anterior temporal artery: an underutilized but robust donor for revascularization of the distal middle cerebral artery. J Neurosurg. 2017;127(4):740747.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Kalani MY, Ramey W, Albuquerque FC, et al. Revascularization and aneurysm surgery: techniques, indications, and outcomes in the endovascular era. Neurosurgery. 2014;74(5):482498.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Abla AA, Lawton MT. The superficial temporal artery trunk-to-M2 middle cerebral artery bypass with short radial artery interposition graft: the forgotten bypass. World Neurosurg. 2015;83(2):145146.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Abla AA, Lawton MT. Anterior cerebral artery bypass for complex aneurysms: an experience with intracranial-intracranial reconstruction and review of bypass options. J Neurosurg. 2014;120(6):13641377.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Tayebi Meybodi A, Lawton MT, Griswold D, et al. Assessment of the temporopolar artery as a donor artery for intracranial-intracranial bypass to the middle cerebral artery: anatomic feasibility study. World Neurosurg. 2017;104:171179.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Mura J, Riquelme F, Cuevas JL, et al. Simplified azygos anterior cerebral bypass: y-shaped superficial temporal artery interposition graft from A2 with double reimplantation of pericallosal arteries: technical case report. Neurosurgery. 2013;72(2 Suppl Operative):onsE235ons240.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Lawton MT. Seven Bypasses: Tenets and Techniques for Revascularization. Thieme; 2018.

  • 25

    Rhoton AL Jr. The supratentorial arteries. Neurosurgery. 2002;51 (4)(suppl):S53S120.

  • 26

    Rodríguez-Hernández A, Rhoton AL Jr, Lawton MT. Segmental anatomy of cerebellar arteries: a proposed nomenclature. Laboratory investigation. J Neurosurg. 2011;115(2):387397.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Lawton MT, Lang MJ. The future of open vascular neurosurgery: perspectives on cavernous malformations, AVMs, and bypasses for complex aneurysms. J Neurosurg. 2019;130(5):14091425.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Duckworth EA, Rao VY, Patel AJ. Double-barrel bypass for cerebral ischemia: technique, rationale, and preliminary experience with 10 consecutive cases. Neurosurgery. 2013;73(1 Suppl Operative):ons30-8ons37-8.

    • Search Google Scholar
    • Export Citation
  • 29

    Nakajima H, Kamiyama H, Nakamura T, et al. Direct surgical treatment of giant intracranial aneurysms on the anterior communicating artery or anterior cerebral artery. Neurol Med Chir (Tokyo). 2013;53(3):153156.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Cantore G, Santoro A, Guidetti G, et al. Surgical treatment of giant intracranial aneurysms: current viewpoint. Neurosurgery. 2008;63(4)(suppl 2):279290.

  • 31

    Hongo K, Horiuchi T, Nitta J, et al. Double-insurance bypass for internal carotid artery aneurysm surgery. Neurosurgery. 2003;52(3):597602.

  • 32

    Otani N, Wada K, Sakakibara F, et al. “Reverse” bypass using a naturally formed “bonnet” superficial temporal artery in symptomatic common carotid artery occlusion: a case report. Neurol Med Chir (Tokyo). 2014;54(10):851853.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Bulsara KR, Patel T, Fukushima T. Cerebral bypass surgery for skull base lesions: technical notes incorporating lessons learned over two decades. Neurosurg Focus. 2008;24(2):E11.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Wada K, Otani N, Toyooka T, et al. Superficial temporal artery to anterior cerebral artery hemi-bonnet bypass using radial artery graft for prevention of complications after surgical treatment of partially thrombosed large/giant anterior cerebral artery aneurysm. J Stroke Cerebrovasc Dis. 2018;27(12):35053510.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Endo H, Sugiyama SI, Endo T, et al. Revascularization of the anterior cerebral artery by Y-shaped superficial temporal artery interposition graft for the treatment of a de novo aneurysm arising at the site of A3-A3 bypass: technical case report. J Neurosurg. 2018;129(5):11201124.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36

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