LABORATORY INVESTIGATIONJ Neurosurg 130:207–212, 2019

The occipital artery (OA) is a frequently used donor vessel for extracranial-intracranial bypass proce-dures to the posterior circulation, by virtue of its

proximity to the recipient vessels and its optimal caliber, length, and flow rate.3 After Sundt and Piepgras first re-

ported early experience with posterior circulation revas-cularization achieved using the OA,13 the OA has been widely used as a donor vessel in treating posterior circula-tion aneurysms, ischemic neurological disorders, and rees-tablishing blood flow after resection of skull base tumors,

ABBREVIATIONS AICA = anterior inferior cerebellar artery; DG = digastric groove; DM = digastric muscle; OA = occipital artery; OG = occipital groove; OMS = occipito-mastoid suture; PICA = posterior inferior cerebellar artery; SOM = superior oblique muscle; VA = vertebral artery. SUBMITTED February 26, 2017. ACCEPTED June 13, 2017.INCLUDE WHEN CITING Published online January 26, 2018; DOI: 10.3171/2017.6.JNS17518.* Drs. Benet and Tabani contributed equally to this work.

The transperiosteal “inside-out” occipital artery harvesting technique*Arnau Benet, MD,1,2 Halima Tabani, MD,1,2 Xinmin Ding, MD, PhD,1,2 Jan-Karl Burkhardt, MD,1,2 Roberto Rodriguez Rubio, MD,1,2 Ali Tayebi Meybodi, MD,1,2 Peyton Nisson, BS,2 Olivia Kola,2 Sirin Gandhi, MD,1,2 Sonia Yousef, BS,2 and Michael T. Lawton, MD1,2

1Department of Neurological Surgery, and 2Skull Base and Cerebrovascular Laboratory, University of California, San Francisco, California

OBJECTIVE The occipital artery (OA) is a frequently used donor vessel for posterior circulation bypass procedures due to its proximity to the recipient vessels and its optimal caliber, length, and flow rate. However, its tortuous course through multiple layers of suboccipital muscles necessitates layer-by-layer dissection. The authors of this cadaveric study aimed to describe a landmark-based novel anterograde approach to harvest OA in a proximal-to-distal “inside-out” fashion, which avoids multilayer dissection.METHODS Sixteen cadaveric specimens were prepared for surgical simulation, and the OA was harvested using the classic (n = 2) and novel (n = 14) techniques. The specimens were positioned three-quarters prone, with 45° contralater-al head rotation. An inverted hockey-stick incision was made from the spinous process of C-2 to the mastoid tip, and the distal part of the OA was divided to lift up a myocutaneous flap, including the nuchal muscles. The OA was identified us-ing the occipital groove (OG), the digastric muscle (DM) and its groove (DG), and the superior oblique muscle (SOM) as key landmarks. The OA was harvested anterogradely from the OG and within the flap until the skin incision was reached (proximal-to-distal technique). In addition, 35 dry skulls were assessed bilaterally (n = 70) to study additional craniometric landmarks to infer the course of the OA in the OG.RESULTS The OA was consistently found running in the OG, which was found between the posterior belly of the DM and the SOM. The mean total length of the mobilized OA was 12.8 ± 1.2 cm, with a diameter of 1.3 ± 0.1 mm at the suboccipital segment and 1.1 ± 0.1 mm at the skin incision. On dry skulls, the occipitomastoid suture (OMS) was found to be medial to the OG in the majority of the cases (68.6%), making it a useful landmark to locate the OG and thus the proximal OA.CONCLUSIONS The anterograde transperiosteal inside-out approach for harvesting the OA is a fast and easy tech-nique. It requires only superficial dissection because the OA is found directly under the periosteum throughout its course, obviating tedious layer-by-layer muscle dissection. This approach avoids critical neurovascular structures like the vertebral artery. The key landmarks needed to localize the OA using this technique include the OMS, OG, DM and DG, and SOM.https://thejns.org/doi/abs/10.3171/2017.6.JNS17518KEY WORDS aneurysms; bypass; occipital artery; occipital groove; revascularization; posterior circulation; far-lateral approach; surgical technique

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particularly those involving the vertebral artery (VA) or posterior inferior cerebellar artery (PICA).3,13

Although the OA has sufficient length and caliber to effectively redirect blood flow to the posterior circula-tion,10 it has a tortuous course in which it passes through multiple layers of suboccipital muscles, necessitating lay-er-by-layer dissection for exposure. Therefore, harvesting the OA has been regarded as time consuming and more challenging than harvest of the superficial temporal ar-tery.2,7 The conventional method used to harvest the OA entails removing it from its distal to its proximal segment, using layer-by-layer muscle dissection through the nuchal and suboccipital musculature.6,8 The transitional segment of the OA, which runs between the superior edge of the splenius capitis muscle and the superior nuchal line, has been deemed the most challenging segment of the OA to harvest because it is known to traverse vertically through several layers, including the tendon of the splenius capitis muscle and the galea aponeurotica.7 Recently, Fukuda et al. proposed 3 variations of the conventional OA harvest-ing technique, all of which directed the dissection toward the transitional segment of the OA, using 3 different skin incisions.7 The authors concluded that the most critical step during OA harvest is the dissection of the transitional segment, and that layer-by-layer dissection of muscles is required to safely and effectively harvest this segment.

Several studies have described the microanatomy of the OA in detail for its use in posterior circulation bypass.2,3 However, an efficient, technically less challenging, and minimally invasive technique for harvesting the OA is still lacking.

In this cadaveric surgical simulation study, we propose a novel technique for harvesting the OA via an antero-grade (from proximal to distal) approach performed using a myocutaneous flap. Our objective was to describe the approach in a stepwise manner and define key landmarks to safely and efficiently harvest the OA by using the pro-posed technique.

MethodsCraniometric Study

Thirty-five dry skulls were assessed bilaterally (n = 70) to study the bony landmarks that can be used to identify and locate the proximal segment of the OA. The occipi-tal groove (OG) was bilaterally identified in each skull. The shape of the OG was classified into canal, groove, or impression. Next, the asterion was located and the origin of the occipitomastoid suture (OMS) was identified. The OMS was then followed inferiorly to assess its relationship with the course of the OA: medial to the OA, lateral to the OA, or crossing the OA.

Development and Feasibility Assessment of the Proposed Technique

Eight adult cadaveric heads (16 specimens) were pre-pared for surgical simulation following our published protocol for embalming.5 The conventional OA harvest-ing technique was performed in 2 specimens to assess the shortcomings of this technique and to design the new approach. The proposed novel anterograde (proximal to

distal) approach for harvesting the OA was performed in the rest of the specimens (n = 14) to test the feasibility of the technique and to define the surgical landmarks for identification of the OA (Video 1).

VIDEO 1. Clip showing anterograde inside-out OA harvest. The 3D video depicts stepwise dissection of the OA aided by the antero-grade inside-out technique. Copyright Arnau Benet. Published with permission. Click here to view.The specimens were positioned in a three-quarter

prone position with the head turned 45° toward the contra-lateral side by using the 3-pin head clamp (Mizuho Amer-ica), and the neck was slightly flexed, allowing flattening of the suboccipital musculature. This position allowed exposure of the mastoid process as well as easy access to the inion and the spinous process of C-2. The classic inverted hockey-stick incision was performed, connecting the spinous process of C-2 to the tip of the mastoid process (Fig. 1A). The incision began along the avascular midline through the nuchal ligament and was extended superiorly 3 cm above the superior nuchal line. At this point, it was turned laterally in a horizontal fashion until reaching the asterion region and then continued inferiorly to end 1 cm below the mastoid tip. While performing the incision, care was taken to keep the cut shallow near the lateral third of the superior nuchal line to prevent inadvertent damage to the distal segment of the OA, which runs subcutaneously.

The subcutaneous segment of the OA was then iden-tified, ligated, and transected. In 2 cases, longer grafts were obtained by dissecting distally (superiorly) into the scalp as proof of concept, but measurements were taken only to the skin incision for statistical consistency. Blunt dissection was then continued in the avascular plane in the midline until the occipital bone was exposed. The nu-chal muscles were then elevated from medial to lateral into the flap, keeping the periosteal sheath intact within the flap (Fig. 1B). Dissection then continued through the suboccipital space, and the C-1 and C-2 vertebrae were exposed between the posterior rectus capitis major and minor muscles. The suboccipital muscles were elevated subperiosteally along the inferior nuchal line into a single myocutaneous flap. As dissection continued inferiorly, the longissimus capitis was freed from its insertion at the posterior margin of the mastoid process and the poste-rior belly of digastric muscle (DM) was detached from its attachment at the digastric groove (DG), and both were included in the flap.

The OA was then identified in the OG, which was found medial to the DG (Fig. 1C). It was bound medially by the superior oblique muscle (SOM) and laterally by the poste-rior belly of DM. Once the OA was identified, it was dis-sected proximally by using sharp microdissection under the microscope, freeing it from its surrounding connective and periosteal tissue. Dissection was then continued dis-tally with 45° Pott scissors, following the course of the OA under the periosteum. The course of the OA was followed distally, freeing it circumferentially from its surrounding connective tissue attachments, ending at the superior edge of the hockey-stick incision (Fig. 1D and Video 1).

The lengths and calibers of the suboccipital and occipi-tal segments of the OA were measured. Also, the spatial relationship of the OA with key defined landmarks (OG,

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DM, DG, and SOM) was assessed and recorded. All mea-surements of length were taken with the vessel fully ex-tended and straight. Any caliber measurements were made using the microscope and a caliper tool.

ResultsThe OA was successfully harvested in all 14 specimens

by using the proposed technique without any damage to the vessel, as evidenced by preserved adventitia of the vessel and absence of latex exposure. The mean total har-vested length of the OA was 12.8 ± 1.2 cm, and the mean length of the suboccipital segment was 8.1 ± 0.6 cm. The mean diameter of the suboccipital segment was 1.3 ± 0.1 mm and that of the occipital segment was found to be 1.1 ± 0.1 mm. The most consistent landmarks for identifying and localizing the proximal OA were lateral to the SOM, medial to the DG, and within the OG. At the superior nu-chal line, the OA was located at an average of 3.3 cm from the midline, whereas at the incision site it was found at an average of 5.3 cm from the midline. No muscle perfo-rator vessels were transected during exposure of the OA from the periosteum because all the muscular branches of

the OA were found to be arising from the muscular side, which was located in a deeper plane of dissection.

In our observations of dry skull specimens, we found that the OA ran in a groove in 71.5% of the specimens, whereas it carved an impression in the rest of the cases (28.5%). In none of the specimens was the OA found to run in a bony canal. The OMS was found to be medial to the OA groove or impression in 68.6% of the cases, whereas in 31.4% it ran centrally through the OA groove or impression (Fig. 2). In none of the specimens was the OMS found lateral to the OA.

Illustrative CaseA 59-year-old man presented with complaints of gait

instability and imbalance. On radiological investigation, he was found to have a subacute infarct in the cerebellum in the PICA territory. Angiography revealed vertebro-basilar insufficiency due to intracranial atherosclerosis; in particular, occluded bilateral VAs beyond the PICAs. The patient had a history of prior small-vessel middle cerebral artery strokes on the left side as well as a right-sided pontine ischemic stroke, leading to left-sided hemi-paresis. The patient opted for surgical management, and

FIG. 1. Stepwise depiction of the anterograde inside-out OA harvesting technique. A: The classic hockey-stick incision (dotted line) was performed, connecting the spinous process of C-2 to the mastoid process (solid curved line). The star depicts the posi-tion of the inion. B: The musculocutaneous flap was reflected, detaching the nuchal and occipital muscles from their insertions into a single myocutaneous flap. C: The proximal segment of the OA was identified in the OG, which was found medial to the DG. D: The OA was identified in the OG and was freed from the surrounding occipital musculature and connective tissue in an anterograde (proximal-to-distal) manner. C. = capitis; Ext. = external; LCM = longissimus capitis muscle; M. = muscle; Occ. = oc-cipital; Sup. = superior. Figure is available in color online only.

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an OA–anterior inferior cerebellar artery (AICA) bypass was planned.

The patient was placed in the lateral position with the head fixated in the Mayfield head holder. A hockey-stick skin incision was made, and scalp and muscle flaps were mobilized inferolaterally, taking care to preserve the peri-osteum. The OA was harvested via an inside-out trans-periosteal approach, pulling the OA through the perios-teum and harvesting it all the way to the edge of the flap. A right extended retrosigmoid craniotomy was then per-formed after drilling the sigmoid sinus. After dural open-ing, the cerebellopontine angle was entered and the AICA was identified. The OA was transected and fish-mouthed, and brought down into the surgical field. An OA-AICA end-to-side bypass was then performed. Intraoperative indocyanine green video angiography and postoperative angiography confirmed patency of the bypass (Video 2).

VIDEO 2. Clip showing a surgical case demonstrating the transperi-osteal inside-out OA harvesting technique for an OA-AICA bypass. Copyright Arnau Benet. Published with permission. Click here to view.

The patient recovered well from surgery and had no neu-rological deficits at discharge.

DiscussionWe propose an anterograde transperiosteal technique

for harvesting the OA that does not require layer-by-layer muscle dissection and is based on reliable, easily identifi-able surgical landmarks. This anterograde, transperiosteal dissection is potentially less invasive, more efficient, and technically less challenging than the existing techniques. The most consistent landmarks for identifying and local-izing the proximal OA in this study were the SOM, the DG, and the OG, all of which are easily identifiable dur-ing a conventional hockey-stick incision for a far-lateral approach.

The OA has been widely used for revascularization procedures of the posterior circulation because it has been demonstrated to offer a suitable length, caliber match, and flow rate for vessels in the posterior circulation, in particu-lar the PICA.1,3,4,9,11 In addition, it is located in the vicinity

of the recipient vessels and is commonly encountered en route to the pathological entity being addressed, sparing the patient the need for an additional incision for an in-terposition graft. Since the first description of its use in 1967,13 several variations of the harvesting technique for the OA have been proposed,6–8 but most of them are te-dious and time consuming due to the tortuous course of the OA through the nuchal and suboccipital musculature. The complex techniques needed to harvest the OA might be an important limiting factor for the widespread use of the OA as a donor vessel for extracranial-intracranial by-pass procedures.

The technique described in this study proposes har-vesting the OA from the myocutaneous flap. In contrast with the classic technique, our proposed technique in-volves identifying the proximal segment of the OA in the OG, and harvesting it circumferentially in a proximal to distal fashion, from deep to superficial, dissecting away from critical neurovascular structures. In its proximal segment, the OA has been described to course in a single layer of connective tissue termed the styloid diaphragm,7 making it easily identifiable. This method requires only superficial dissection because the OA is found directly un-der the periosteum throughout its course. This results in minimal manipulation of the nuchal and occipital muscu-lature, and does not require layer-by-layer muscle dissec-tion, decreasing the risk of muscular atrophy. In addition, because this technique requires minimal blind dissection, it is relatively safer and has less chance of damaging the graft. Thereby, this technique offers an easier, faster, and potentially safer OA harvesting technique than those that have been described previously (Table 1). On the other hand, inadvertent damage to the proximal portion of the OA can potentially be more hazardous than that to the dis-tal OA. Thus, we propose the use of anatomical landmarks including the OG, DG, and OMS to aid in the localization of the OA. In addition, adjunct use of modalities like neu-ronavigation and intraoperative Doppler can further aid in the identification of the proximal portion of the OA, if required.

The OA has traditionally been divided into 3 segments

FIG. 2. Dry skull images depicting important bony landmarks for the identification of the OA. A: The relationship between DG, OG, and OMS is depicted. The OG was medial to the DG, and the OMS was medial to the OG in the majority (68.6%) of cases. The foramen for the mastoid emissary vein is also shown. B: In 31.4% of the specimens, the OMS was running through the OG. The asterion is shown; the OMS can be followed from the asterion inferiorly to locate the OG, and thus the OA. Figure is available in color online only.

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based on its relationship with key structures throughout its course, from its origin from the external carotid artery to its distal bifurcation into terminal segments (i.e., digastric, suboccipital, and occipital segments).2 Other authors have proposed a classification based on the course of the OA through the musculature that it traverses (i.e., intramus-cular, transitional, and subcutaneous segments).7 Based on this classification, the transitional segment of the OA has been suggested as the safer segment to identify the OA for its harvesting. However, to identify this transitional segment, a clear identification of multiple muscular land-marks is required after a layer-by-layer dissection, becom-ing challenging when classic incisions are used, and still carrying a considerable risk of damaging the OA. To over-come the common limitations of all the previous methods, we designed a technique that allows shallow, superficial dissection of the OA. We propose the use of a classic hock-ey-stick incision with a myocutaneous flap, and then har-vest of the OA from the undersurface of the flap through the periosteum. This brings the OA superficial in the dis-section after the flap is reflected, similar to the depth of the superficial temporal artery on an anterolateral approach. This technique preserves the integrity of the nuchal and occipital muscles. By being relatively atraumatic to this musculature, this technique has a potentially less chance of postoperative pain and muscular atrophy. It also has less risk of inadvertent transection of the OA and less blood loss, because no muscular branches of the OA are encoun-tered and/or transected during the harvest.

In our study, we ended the dissection of the subcuta-neous segment at the incision site. However, in cases in which longer grafts are required, this segment can be further dissected distally superiorly into the scalp if the incision is extended superiorly. Another advantage of us-ing the proximal-to-distal technique is that because the diameter of the proximal segment is adequate, the dissec-tion can be terminated once adequate length is achieved, which is not the case when harvesting distal to proximal, where dissection has to be continued until adequate diam-eter is found proximally.

In our study, the OA diameter was 1.3 mm at the sub-occipital and 1.1 mm in the occipital segments. These findings are comparable to previous studies in which the average diameter of the suboccipital segment was report-ed to be 1.4 mm and that of the occipital segment was

found to be > 1 mm.2 We measured the length of the ar-tery after mobilizing the suboccipital segment and found a mean length of 8.1 cm. This is critical because the average length reported for OA bypass to the V3 segment of the VA is 4.0 cm, the V4 segment is 5.0 cm, the caudal loop of PICA is 5.8 cm, and the AICA is approximately 5.9 cm.3 Thus, dissecting the suboccipital segment provides adequate length for bypass, sometimes allowing for omis-sion of the more time-consuming occipital segment of the OA. This reduces the time needed for OA dissection and time of the operation, correlating with reduced mortality and lower hospital costs.12

The OMS is a key landmark for localizing the proximal OA. The OMS was consistently found within (31.4%) or medial (68.6%) to the OG. Because the OMS is exposed during the approach, it can be used as a landmark to lo-cate the proximal OA. The OMS can be followed inferi-orly from the asterion to the OA groove. Inadvertent dam-age to the proximal OA may be avoided by identifying the OMS and dissecting medially to it, because the proximal OA will be lateral to it in most cases. None of the 70 OGs studied had a bony canal, although this configuration may be found.2 Therefore, the impact of a canalicular configu-ration of the OG in identifying the OA using our proposed technique remains unknown and of minimal statistical relevance.

The scope of this study was to design and assess the feasibility of this new technique by using surgical simula-tion in cadavers. This study lays the foundation for an ev-idence-based, ethical use of the anterograde OA harvest-ing technique in patients. The illustrative case included validates the feasibility of this technique in clinical set-tings. However, further assessment of clinical outcomes, such as bleeding, vasospasm, postoperative pain, muscular atrophy, and length of hospital stay, may be studied with large-scale clinical application of this technique. More-over, evaluation of metrics such as operating room time, patency of bypass, intraoperative complications, and tech-nical ease is required to establish the superiority of this technique over the existing ones for harvesting the OA.

ConclusionsHarvesting the OA for bypass can be a challenging and

time-consuming task due to its tortuous course and the

TABLE 1. Comparison of the salient features of the classic versus the anterograde “inside-out” OA harvesting techniques

Classic Approach Anterograde “Inside-Out” Approach

Distal-to-proximal “retrograde” OA dissectionRequires layer-by-layer muscle dissection; is tedious & risky

Exposure of the OA is difficult, specifically the transitional segment, which traverses several muscle layers

Requires blind dissection of the OA as it traverses multiple muscle layers

Dissection has to be continued until adequate caliber is achieved proximally

Muscular perforators may be transected during layer-by-layer muscle dis-section

Proximal-to-distal “anterograde” OA dissectionRequires transperiosteal dissection of OA from a single myocutaneous

flap; is easier & fasterReliable landmark-based approach; it allows easy localization of the OA

Requires minimal blind dissection because the OA is under direct view throughout the dissection

Dissection starts from the proximal segment, which has larger caliber; the graft length w/ largest caliber can be tailored early

No muscular perforators transected; reduction of blood loss

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various layers of muscle it runs within. We propose a novel inside-out technique that uses the classic hockey-stick in-cision to harvest the OA in an anterograde manner (from proximal to distal) from the myocutaneous flap through the periosteum. By obviating the need for layer-by-layer dissection, this technique is potentially relatively safer, more efficient, and less technically challenging than the conventional techniques. The OMS, OG, DM, DG, and SOM are key landmarks for identifying and localizing the OA by using this technique.

AcknowledgmentsWe express our gratitude to the body donors and their families,

who, through their altruism, contributed to making this project possible.

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cranial-to-intracranial bypass for posterior inferior cerebellar artery aneurysms: options, technical challenges, and results in 35 patients. J Neurosurg 124:1275–1286, 2016

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occipital muscles under a reverse C-shaped skin incision. Br J Neurosurg 29:401–405, 2015

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DisclosuresThe authors report no conflict of interest concerning the materi-als or methods used in this study or the findings specified in this paper.

Author ContributionsConception and design: Benet, Ding. Acquisition of data: Tabani, Ding, Nisson. Analysis and interpretation of data: Tabani, Ding, Nisson, Yousef. Drafting the article: Benet, Tabani, Rodriguez Rubio, Nisson. Critically revising the article: Benet, Tabani, Burk-hardt, Rodriguez Rubio, Tayebi Meybodi, Gandhi, Yousef, Law-ton. Reviewed submitted version of manuscript: Benet, Tabani, Ding, Burkhardt, Tayebi Meybodi, Nisson, Kola, Gandhi, Yousef, Lawton. Approved the final version of the manuscript on behalf of all authors: Benet. Statistical analysis: Tabani. Administrative/technical/material support: Benet, Tabani, Kola. Study supervi-sion: Benet.

Supplemental InformationVideos

Video 1. https://vimeo.com/231692849.Video 2. https://vimeo.com/231692953.

CorrespondenceArnau Benet: University of California, San Francisco, CA. arnaubenet@gmail.com.

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