Bowhunter Syndrome in the Pediatric Population

Original Research

Baranoski J, Khan N, Ronecker J, McClendon J, Appavu B, White A, Chung C, de Oliveira Sillero R, Hui F, Huisman T, Lawton M, Abruzzo T.

CORRESPONDENCE
Todd Abruzzo, MD, Dept of Radiology, Phoenix Children’s Hospital, 1919 East Thomas Road, Phoenix, AZ 85016, USA. Telephone 602-933-1207, Fax 602-933-0309, tabruzzo@phoenixchildrens.com

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Abstract:

Bowhunter syndrome (BHS) is increasingly recognized as a cause of cervical vertebral artery dissection (VAD) and arterial ischemic stroke (AIS) in children and young adults. In older adults, BHS is not commonly associated with VAD or AIS, and anatomical risk factors are unique from those encountered in the pediatric population. In this article, we present a unified model of the different patterns of BHS according to age and anatomical distribution. The history of BHS is reviewed. Modern principles of pattern-oriented pathophysiology, diagnosis and management are covered in detail.

Definition.

What are the defining elements of Bowhunter syndrome?

Defining Elements of BHS

  • Vertebrobasilar ischemia
  • Dynamic Vascular-Musculoskeletal conflict
  • Head movement mechanism
    • Physiologic movements
    • Chiropractic manipulation
    • Athletic maneuvers
    • Surgical positioning

Bowhunter syndrome (BHS) may be broadly defined as symptomatic vertebrobasilar ischemia secondary to dynamic external mechanical forces exerted on a vertebral artery by adjacent musculoskeletal structures during head movement [1, 2]. The head movements associated with BHS classically fall within the physiological range but may also include a range of head movements considered supra-physiological such as in chiropractic neck manipulation, athletic maneuvers, high-risk recreational activities or surgical head/neck positioning [3, 4].

Terminology & History.

How have anatomical concepts of BHS and terminology evolved over time?

Key anatomical concepts and terms

  • Distinct supra-axial & sub-axial types
  • Bowhunter dissection
  • Bowhunter stroke
  • BHS is all inclusive umbrella term

The conceptual progenitor of BHS may be considered to be “cervical vertigo”. The concept of “cervical vertigo” took shape between 1930 and 1960, when DeKleyn and Versteegh postulated that the basis of vertigo was diminished vertebrobasilar blood flow accompanying head rotation [5, 6]. Initial support for this hypothesis came from cadaver experiments which demonstrated that head rotation can result in vertebral artery occlusion [7, 8]. Further interest in “cervical vertigo” was fueled by reports of vertebral artery dissection (Bowhunter dissection) and stroke precipitated by chiropractic neck manipulation in the 1940’s and 1950’s [9-11]. Over the subsequent years, cadaveric studies reported that head rotation within a 45-degree range could affect vertebral artery occlusion at the C1-C2 vertebral level [12, 13]. During the same period of time, the emerging practice of cerebral angiography in adult patients revealed that volitional head rotation by awake patients could restrict anterograde angiographic filling of the vertebral artery [14].

In the early 1960s, two patterns of adult BHS were already recognized in the literature: 1) spondylotic vertebral artery compression (SVAC), and 2) infra-foraminal musculotendinous vertebral artery compression (IFVAC). SVAC, the far more common adult pattern, was initially characterized by Sheehan et al. in a seminal report of 26 patients which included the first description of vertebral artery angiography with a head rotation challenge [15]. The patients were all males with a mean age of 57 years. The authors showed that SVAC is the result of uncovertebral osteophytes impinging on adjacent transforaminal vertebral artery segments during head rotation. Offending osteophytes were most commonly found at the C5-C6 vertebral level, and less commonly at the C4-C5 vertebral level. While Sheehan recommended bedrest and anticoagulation, the potential benefit of spinal fusion surgery was suggested. IFVAC, the far less common adult pattern of BHS, was found to be secondary to scalenus muscle impingement upon the vertebral artery in the scalenovertebral triangle at the C6 vertebral level. Powers et al. reported his success with the treatment of affected patients by scalenotomies [16].

The term “Bowhunter’s stroke” was first used in a 1978 report describing a 39-year-old male with acute onset of a lateral medullary infarction during archery practice [1]. Catheter-directed angiography in that patient revealed an underlying supra-axial vertebral artery dissection between the C1 and C2 transverse foramina, misinterpreted as “vasospasm”. Similarities between the “Bowhunter’s stroke” resulting from supra-axial vertebral artery injury and sub-axial patterns of vertebral artery injury involved in patients with SVAC and IFVAC were recognized. Eventually, both patterns of vertebrobasilar disease became grouped together within the same category described by the umbrella term BHS.

What evidence supports our current understanding of the mechanism of BHS?

  • Evidence supporting contemporary models of BHS
  • Early angiographic experiments
  • MRI studies

In the mid to late 1960s, clinicians remained skeptical about the true nature of vertebral artery occlusion during head rotation. Many expressed concerns that examiners artificially produced the phenomenon by hyper-rotation of the head beyond its physiological range. A series of angiographic experiments performed on 43 healthy middle-aged male volunteers showed that vertebral artery occlusion resulting from volitional head rotation occurs in less than 12% of subjects [17]. The authors of that study reported that rotational occlusion of the vertebral artery in healthy males could be the result of compression by osteophytes (7%) or soft tissue bands (4%). A contemporary magnetic resonance (MR) imaging study utilizing phase-contrast and arterial spin labeling sequences in 18 healthy adult volunteers found no significant change in cervical artery flow metrics as head position was varied throughout the physiologic range of rotation, flexion and extension [18]. The authors concluded that reductions in cervical artery flow associated with physiologic head movements, in patients with vertebrobasilar ischemic stroke, should be considered pathologic and mechanistically related to the stroke.

Attempts to localize and quantify the range of head rotation causing vertebral artery occlusion in cadavers indicated that the vertebral artery begins to stretch between the C1 and C2 transverse foramina at approximately 30 degrees of contralateral head rotation [19]. Severe stretching, resulting in reversible luminal occlusion, was shown at 45 degrees or more of contralateral head rotation.

Anatomical Types and Subtypes of Bowhunter Syndrome.

How are the main anatomical types of BHS and associated subtypes different?

Anatomical spectrum of BHS

  • Sub-axial type in older adults
    • Osteophytic subtype
      • Degenerative disc disease
      • C5-C6 & C4-C5 levels
    • Musculotendinous subtype
      • Hypertrophic anterior scalene
      • C6 level
  • Supra-axial type in children & young adults
    • Atlanto-occipital subtype
      • Vertebral artery dissection between C1 foramen transversarium & foramen magnum
    • Atlanto-axial subtype
      • Vertebral artery dissection between C1 & C2 foramen transversaria

There are two broadly differentiated, anatomical types of BHS. These two types of BHS express different phenotypes with respect to age, vertebral artery pathology, level of the vertebral artery lesion, cerebral pathology, and anatomical/musculoskeletal risk factors (Table 1) [2].

The sub-axial type of BHS is more common in older adults. As stated previously, osteophytic and musculotendinous subtypes have been reported. The characteristic features are outlined in Table 1. The more common osteophytic subtype is a manifestation of degenerative disc disease. Affected patients typically present with symptoms of reversible, positional vertebrobasilar insufficiency rather than acute brain infarction [20]. Vertebrobasilar insufficiency is the result of transient vertebral artery compression by impinging uncovertebral joint osteophytes [5]. The site of vertebral artery compression reflects the anatomical distribution of osteophytes that is characteristic of degenerative disc disease, most common at the C5-C6 and C4-C5 levels. Since cervical spine mobility is pathologically reduced in affected patients, the excessive and rapidly accelerating forces needed to create a dissecting stretch injury or impact-induced arterial intramural hemorrhage are prohibited. Consequently, vertebral artery dissection and intramural hemorrhage are not a feature of this type of BHS. Less frequently, the sub-axial form of BHS may be a result of musculotendinous vertebral artery impingement by a hypertrophic anterior scalene muscle at the C6 vertebral level [16].

The supra-axial form of BHS is the type more commonly found in children and young adults. Two subtypes have been reported in the literature: 1) atlanto-axial and 2) atlanto-occipital [2]. Both subtypes present with vertebral artery dissection or intramural hemorrhage complicated by posterior circulation brain infarction due to embolus. In contrast to the common musculoskeletal risk factors in sub-axial BHS (degenerative osteophytes), musculoskeletal risk factors correspond to congenital osseous anomalies, soft tissue bands or synechiae (between vertebral artery and congenital osseous anomalies), and hypermobility. Vertebral artery dissection or intramural hemorrhage is a consistent feature of supra-axial BHS, particularly in children. Multiple pediatric case series have shown that bilateral vertebral artery dissection occurs in a significant portion of patients (Table 2, Figure 1) [21-34]. This feature of pediatric BHS critically impacts therapeutic decision-making as further detailed later in this review. In patients with supra-axial BHS, rapidly increasing traction and/or compression forces brought to bear upon a vertebral artery segment immobilized between two fixation points, result in intimal tearing due to stretching or intramural hemorrhage due to impaction. As in cases of traumatic vertebral artery dissection, the mural damage process is most likely acute, rather than a product of chronic repetitive injury [28, 32]. This pathogenesis contrasts with the compression forces that are at play in sub-axial forms of BHS. In theory, vertebral artery thrombosis due to prolonged occlusion and stasis of blood flow may occur without dissection when the vertebral artery is stretched or compressed for extended periods. In such cases, thrombophilia may be a pathogenetic cofactor. Vulnerability to vertebral artery dissection injury in supra-axial BHS seems unique to children and young adults owing to their high degree of ligamentous laxity, immaturity of osseous elements, and resultant increased cervical spine mobility [35]. This can result in acute vertebral artery injury and resultant arteriopathy during athletic maneuvers and chiropractic manipulations [22, 26-28].

Do vertebral artery segmentation schemes correlate with dissection sites in supra-axial BHS subtypes?

Vertebral artery segmentation vs Supra-axial BHS subtype

  • Atlanto-occipital subtype
    • V3 segment in Barbieri & Power scheme
  • Atlanto-axial subtype
    • V3 segment in Barbieri scheme vs V2 segment in Power scheme
  • Poor correlation due to interchangeable use of Barbieri & Power scheme

The anatomical location of the vertebral artery dissection in supra-axial BHS differs according to subtype (Table 1). In the atlanto-axial subtype, which is more common, the vertebral artery dissection occurs at the C1-C2 vertebral level, typically just distal to the C2 foramen transversarium, and colocalizes to the vertebral artery segment that is reversibly occluded during contralateral head rotation (Figure 2 and Video 1). While this corresponds to the V3 segment in the chiropractic classification system or Barbieri scheme, it corresponds to the distal foraminal V2 segment in the anatomical-radiological classification system or Power scheme (Figure 4) [36, 37].

In contrast, the less common atlanto-occipital BHS subtype is characterized by vertebral artery dissection distal to the C1 foramen transversarium, where the vertebral artery courses along the posterior neural arch of C1. In affected patients, these dissections colocalize to the vertebral artery segment that is reversibly occluded during contralateral head rotation (Figure 3 and Video 2). Less commonly, angular movements (extension, lateral flexion) or combined angular and rotational movements will be the offending motion that produces mechanical stress on the vertebral artery in the C1 sulcus arteriosus. The affected segment of vertebral artery corresponds to the V3 segment in both the anatomical-radiological classification system (Power scheme) and the alternative chiropractic classification system (Barbieri scheme) (Figure 4) [36, 37].

Differential Pathogenesis in Anatomical Sub-types of Supra-axial Bowhunter Syndrome.

What accounts for different vertebral artery dissection sites in supra-axial BHS subtypes?

Mechanisms of vertebral artery dissection in supra-axial BHS

  • Atlanto-axial
    • Contralateral head rotation > lateral flexion > extension
    • Traction forces between C1 &C2 foramen transversaria
      • Manifest as reversible occlusion by angiography
  • Atlanto-occipital
    • Contralateral head rotation > lateral flexion > extension
    • Craniocervical junction impaction or traction forces
      • Manifest as reversible occlusion by angiography

In the majority of patients with BHS, regardless of anatomical type/subtype, the vertebral artery is compromised when the head is rotated to the contralateral side. This can be demonstrated during catheter-directed vertebral artery angiography. In a minority of cases, the vertebral artery is compromised by asymmetric lateral head flexion to the side of the affected vertebral artery. Even less commonly, head extension results in vertebral artery compromise. The effects of contralateral head rotation upon the vertebral artery are central to the pathogenesis of supra-axial BHS (Videos 1 and 2). In the normal spine, the vast majority of natural motion during volitional head rotation is believed to occur at the C1-C2 vertebral level (atlantoaxial motion). As the mechanical limits of C1-C2 mobility are approached, atlanto-occipital mobility is engaged, as demonstrated by dynamic video fluoroscopy (atlanto-occipital motion) (Video 2). Notably, rotational forces may be redistributed, and mobility redirected in the setting of injury, surgery or anatomical variation.

Vertebral artery dissection mechanism in Atlantoaxial BHS Subtype

The atlantoaxial subtype of supra-axial BHS is the most common form encountered in children and young adults (Table 2) [2]. In patients with the atlantoaxial subtype of supra-axial BHS, injurious traction forces are exerted on the segment of vertebral artery interposed between the C1 and C2 transverse foramina during contralateral head rotation. This process is demonstrated as reversible occlusion of the vertebral artery as it is stretched between the C1 foramen transversarium and C2 foramen transversarium during contralateral head rotation. As expected, vertebral artery dissections in patients with the atlantoaxial subtype of supra-axial BHS are located between the C1 and C2 transverse foramina. The mechanism of vertebral artery injury in affected patients is due to fixation of the vertebral artery within the transverse foramina of the C1 and C2 vertebrae. Typically, during head rotation to one side, the ring of C1 pivots around the axis of C2. Consequently, as the head is rotated contralaterally, the C1 foramen transversarium moves further away from the subjacent C2 foramen transversarium, resulting in traction forces on the interposed vertebral artery. These traction forces stretch the vertebral artery, causing it to become reversibly occluded. If excess stretching of the vertebral artery occurs, mural disruption may occur (dissection or intramural hemorrhage).

Vertebral artery dissection mechanism in Atlanto-occipital BHS Subtype

The atlanto-occipital subtype of supra-axial BHS accounts for a significant minority of BHS in children and young adults (Table 2) [2]. In the atlanto-occipital subtype of supra-axial BHS, injurious mechanical forces are exerted on the segment of vertebral artery interposed between the C1 transverse foramen and the foramen magnum during contralateral head rotation. This process is demonstrated as reversible occlusion of the vertebral artery segment interposed between the C1 foramen transversarium and the foramen magnum during contralateral head rotation, lateral flexion of the head, neck extension or some combination of these movements. As expected, vertebral artery dissections involve the vertebral artery segment located in the sulcus arteriosus of C1, between the C1 foramen transversarium and the foramen magnum. Our experience suggests that the mechanism of vertebral artery injury in affected patients is related to atlanto-occipital mobility. The mechanisms of atlanto-occipital mobility have not been well characterized. The corresponding forces exerted on the affected segment of vertebral artery may involve traction, impaction or some combination of these. When such forces are excessively exerted on the anatomically vulnerable segment of vertebral artery, mural disruption manifesting intramural hemorrhage or dissection may result.

Musculoskeletal Risk Factors in Supra-axial BHS.

How do musculoskeletal factors predispose to supra-axial BHS?

Contribution of musculoskeletal factors to supra-axial BHS pathogenesis

  • Soft tissue factors
    • Altered range of motion
    • Vascular frailty
    • Vessel fixation/tethering
  • Osseous factors
    • Altered range of motion
    • Traction forces
    • Impaction forces
    • Scissoring forces

Musculoskeletal risk factors in supra-axial BHS may be osseous, soft tissue or both and vary according to subtype (atlanto-axial vs atlanto-occipital) [33]. The spectrum of soft-tissue factors includes ligamentous laxity/hypermobility, impinging fibrous tissue bands and synechiae. Heritable vulnerabilities may influence soft tissue factors such as ligamentous laxity and hypermobility [21, 34]. These same vulnerabilities may also influence vascular frailty in some cases of collagenopathy. Many musculoskeletal risk factors for vertebral artery dissection in BHS shorten the length of vertebral artery immobilized between fixation points that spread apart during head rotation. A ponticulus posticus, arcuate foramen or other anomalous bony protuberance that becomes adherent to the adjacent vertebral artery may have such an effect (Figure 5). This mechanism of interaction between vessel and bone contrasts sharply with the compressive interactions that are observed in sub-axial types of BHS. In supra-axial BHS, fibrous soft-tissue bands tethering the vertebral artery along its course can similarly aggravate injurious mechanical traction forces acting on the vertebral artery during head movement even in the absence of anomalous bony structures [33, 46]. Other factors such as odontoid dysplasia and ligamentous laxity increase the rotational range of the cervical spine, aggravating traction forces on vertebral artery segments interposed between divergent fixation points [49-53]. Still other musculoskeletal risk factors expose vulnerable segments of vertebral artery to impaction or scissoring forces. It is also possible that individual or sex-related variability in osseous vertebral morphology such as pedicle length and vertebral body thickness could influence the mechanical forces acting on the vertebral artery during head rotation, lateral flexion or extension. Such effects could contribute to the strong predilection that BHS shows for the male sex.

Some authors have observed that focally increased tortuosity of the vertebral artery segment extending between the C1 and C2 transverse foramina is associated with atlanto-axial BHS and have thus proposed that this excess tortuosity is a risk factor for vertebral artery dissection during head rotation [68]. Applying the biomechanical principles outlined above, it follows that pre-existing tortuosity, which increases vascular length and laxity between divergent fixation points, would protect against vertebral artery dissection during head rotation. It is more likely therefore, that focally increased tortuosity of the vertebral artery at the atlanto-axial level, which is associated with atlanto-axial BHS, is a manifestation of vertebral artery dissection, and an acquired consequence of rotational vertebral artery injury rather than a cause of it. Beyond inter-foraminal tortuosity, variations in supra-axial vertebral artery course, such as in the case of a persistent proatlantal intersegmental artery or a persistent hypoglossal artery, are likely to have a strong effect on individual susceptibility to Bowhunter dissection and stroke.

What spinal anomalies predispose to each of the supra-axial BHS subtypes?

Spinal anomalies predisposing to supra-axial BHS

  • Atlanto-occipital subtype
    • Ponticulus posticus
    • Congenital arcuate foramen
    • Occipital condyle spurs
    • Klippel Feil anomaly
    • Odontoid dysplasia
    • Craniocervical junction anomalies
  • Atlanto-axial subtype
    • Ponticulus posticus
    • Congenital arcuate foramen
    • Klippel Feil anomaly
    • Odontoid dysplasia
    • Craniocervical junction anomalies

Osseous factors most commonly associated with supra-axial BHS include anomalous bone structures that form fibrous adhesions to the vertebral artery and act to shorten the length of vertebral artery between spreading fixation points (ponticulus posticus, congenital arcuate foramen, occipital condyle spurs) [33, 46-48] and bony anomalies that alter the rotational mechanics of the cervical spine (Klippel-Feil anomaly with or without Sprengel deformity, odontoid dysplasia, and craniocervical junction anomalies) [38, 43-45]. The former group of musculoskeletal risk factors is commonly associated with atlanto-occipital BHS, while the later may be associated with atlanto-occipital BHS or atlanto-axial BHS depending on the rostro-caudal level of altered rotational mechanics (Table 2).

The congenital arcuate foramen is a variant osseous structure bridging the posterior neural arch of C1 to the superior articular facet of C1, encircling the vertebral artery below [39]. The ponticulus posticus is the posterior portion of this anomalous bony ring. Arcuate foramen or ponticulus posticus has been reported in 3 to 15% of the population, with some studies reporting increased prevalence in males [39-42]. As noted, osseous anomalies of C1 (ponticulus posticus and arcuate foramen) and the occiput are strongly associated with atlanto-occipital BHS [21, 25, 33, 59] (Figure 3, Figure 5, Video 2, Table 2). Rarely, congenital C1 anomalies have also been found in association with atlanto-axial BHS [71]. Notably, adhesions and other alterations of craniospinal anatomy resulting from surgery, including hardware failure, can lead to the development of or recurrence of BHS.

Supra-axial BHS is a Major cause of Childhood Posterior Circulation Stroke.

What are the major features of Bowhunter stroke in children?

Major features of Bowhunter stroke in childhood

  • Vertebrobasilar distribution brain infarction/s
  • Non-traumatic vertebral artery dissection
  • Wake up presentation in infants and younger children
  • Activity induced stroke in older children
    • Golfing
    • Swimming
    • Water polo
    • Rave concerts
    • Roller coasters
    • Weightlifting
    • Shoulder checking
    • Chiropractic neck manipulation

Posterior circulation stroke is very uncommon in childhood, representing just a small fraction of non-perinatal arterial ischemic stroke [54]. Unfortunately, vertebral artery dissections which are the hallmark lesion of BHS are frequently unrecognized in children with posterior circulation stroke due to underutilization of cervical vascular imaging in pediatric clinical practice [55]. Studies have shown that non-traumatic vertebral artery dissection complicated by artery-to-artery embolus is responsible for the majority of childhood posterior circulation stroke [22, 32] (Figure 1). BHS most commonly affects children between the ages of 2 and 16 years (with a mean around 9-10 years), but children 1 year of age or younger can also be affected (Table 2). As noted, stroke is the result of vertebral artery dissection complicated by artery-to-artery embolus, rather than dissection related steno-occlusive flow restriction. In our experience, BHS dissections are rarely flow-limiting (Figure 3b). Even when the dissections are flow-limiting, the collateral flow contributed by the contralateral vertebral artery and ipsilateral external carotid artery is capable of reconstituting adequate blood flow beyond the index vertebral artery lesion.

Posterior circulation stroke in children with BHS has two patterns of clinical presentation: 1) wake up stroke and 2) activity induced stroke [2]. Wake up strokes, which are named as such because neurological symptoms first become apparent immediately after the patient awakens from sleep, are usually seen in infants and younger children that have limited participation in high-risk physical activities. These strokes are unique in that they most likely occur while the patient is sleeping. We hypothesize that loss of skeletal muscle tone associated with sleeping results in abruptly, unsupported passive rotation of the infant head. The stresses attributable to this motion result in vertebral artery dissection. Activity induced stroke is typically manifested in older children and young adults. Relevant activities are associated with exaggerated head rotation postures and movements or may involve marked acceleration and deceleration forces. Reported high-risk activities span a wide range of endeavors including golfing, swimming, water polo, rave concert participation, roller coaster riding, weightlifting, shoulder checking in hockey and chiropractic neck manipulation [5, 20-22, 28, 33, 34]. Straining to reach for objects with exaggerated head postures has also been reported as a cause of BHS-type vertebral artery dissections.

Interestingly, there is a marked male predominance in reported cases of supra-axial BHS (Table 2). Whether this is due to anatomical/developmental predisposition, increased participation in higher-risk activities, or other yet-to-be determined factor remains to be elucidated.

Diagnosis of Supra-axial BHS in Children and Young Adults.

What are the clinical clues to Bowhunter stroke?

Clinical clues to Bowhunter stroke

  • Recent high-risk activity
    • Chiropractic manipulation
    • Recreational sports
  • Characteristic behavioral traits
    • Habitual self-adjustment of C-spine
  • Characteristic postures
    • Torticollis
    • “Turtle necking”

In children and young adults presenting with posterior circulation stroke, a history of recent participation in high-risk activities such as chiropractic neck manipulation, and recreational sports is an important clinical clue to supra-axial BHS. Habitual self-adjustment of the cervical spine, often associated with objective and/or subjective audible “clicking” sounds, is a behavior frequently associated with supra-axial BHS [21, 22, 27, 28, 34]. If questioned, parents of affected children often report torticollis or less commonly “turtle-neck” posturing [31]. Headaches are a common but non-specific feature in older children with BHS [54].

How do neuroimaging studies support the diagnostic evaluation of suspected Bowhunter stroke?

Neuroimaging diagnosis in pediatric BHS

  • Initial neuroimaging evaluation
    • Brain imaging for stroke assessment
      • Brain MRI
  • Vascular imaging to delineate VAD and intracranial emboli
    • MRA of head and neck
    • MRI vessel wall imaging or Fat sat T1WI of neck
    • CT angiography of head and neck
    • Diagnostic catheter-directed angiography
  • Spinel imaging to reveal musculoskeletal factors
    • 3D recons of spine from CT angiogram of neck
  • Delayed neuroimaging evaluation
    • Vascular imaging with head maneuvers
      • Non-invasive approaches have limited utility
        • Multiphase CT angiography
        • Doppler ultrasound
      • Catheter-directed angiography preferred

Initial neuroimaging evaluation

Emergency imaging evaluation of the brain and cervico-cerebral vasculature is indicated whenever posterior circulation stroke and/or supra-axial BHS is suspected [54, 55]. Initial imaging evaluation should begin with anatomical and advanced (diffusion-weighted imaging) brain MRI; and MRA of the intracranial and extracranial vasculature. Infarction in the posterior-inferior cerebellum or lateral medulla is a helpful sign lateralizing the culprit vertebral artery dissection. Notably, if the index cerebellar artery supplying the affected posterior-inferior cerebellar territory arises from the basilar artery (a normal anatomical variant), the cerebellar infarction loses lateralizing specificity. In any child or young adult with posterior circulation stroke, a systematic investigation should be undertaken to exclude vertebral artery dissection. Fat-saturated T1-weighted imaging of the neck and black-blood vessel wall imaging may be useful [56, 57]. CT angiography will often reveal underlying anomalous bone structures that form the basis of BHS anatomical vulnerability. Surface-rendered 3D reconstructed images should be obtained as these are particularly revealing (Figure 3c). Multiplanar reformatted images in coronal, sagittal and axial planes, and surface rendered 3D reconstructions derived from the CT angiogram, and windowed to emphasize the bony and vascular anatomy, are essential for planning definitive surgical treatment of the patient. Catheter-directed digital subtraction angiography is the most sensitive and specific study for the diagnostic identification of vertebral artery dissection. We recommend diagnostic catheter-directed angiography in any child with un-explained posterior circulation stroke, especially if the stroke is recurrent.

Delayed neuroimaging evaluation

Definitive diagnosis of BHS relies on vascular imaging with provocative head maneuvers (Figures 2, 3, Videos 1, and 2). Importantly, we advocate that such studies should not be performed in the acute or subacute stroke phase of clinical presentation. Affected patients often present with neck pain and severe spasm of the paraspinal skeletal muscles. Consequently, examiners will be unable to achieve the requisite degree of head manipulation needed to demonstrate the BHS diagnosis. Even under general anesthesia with effective neuromuscular blockade, provocative head maneuvers in affected patients may aggravate vertebral artery dissection or destabilize mural thrombus. Consequently, it is advisable to postpone vascular imaging with head maneuvers until the index vertebral artery dissection has healed and skeletal muscle spasm has resolved. This can be assessed on follow-up MRA prior to performing catheter-directed angiography. Importantly, in cases with a high-index of suspicion, neck immobilization with a cervical collar and continuation of anticoagulation or antiplatelet therapy should be performed in the interim.

In cooperative patients, it is possible to perform multi-phase CT angiography with the patient’s head in neutral, dextro-rotated, and levo-rotated positions. Additional phases needed to characterize the effects of lateral head flexion and head extension have multiplicative effects on patient radiation exposure. While multi-phase CT angiography may be diagnostic in some cases, it lacks information about flow and can be difficult to interpret. Moreover, it may be associated with excess radiation exposure, which is a particular concern in children. While duplex Doppler ultrasound examination of the vertebral arteries with dynamic head maneuvers avoids radiation exposure, provides information about flow and may be used to diagnose BHS, it provides limited anatomical detail relative to catheter-directed angiography [56].

There is extensive literature reporting on the definitive diagnosis of BHS by catheter-directed angiography with provocative head maneuvers in awake adults [3, 5, 20, 59]. Catheter-directed angiography with provocative head maneuvers is also the most widely reported approach to diagnosis in the pediatric population [30, 33, 34]. We strongly favor the definitive catheter-directed diagnosis of BHS regardless of patient age.

Technical aspects of catheter-directed angiography with head maneuvers in children

In young children, catheter-directed diagnosis begins with rotation of the patient’s head by the angiographic team under general anesthesia with neuromuscular blockade. Safe manipulation of the patient’s cervical spine is possible because it is performed with live fluoroscopic guidance. The effect of head manipulation on vertebral artery flow is monitored in real time as the index vertebral artery is simultaneously injected with contrast media (Videos 1 and 2). In order to prevent a pseudo-occlusion misdiagnosis, movement of the patient’s head should not be initiated until the vertebral artery is completely filled with contrast media [59]. Each vertebral artery is initially examined with rotational head maneuvers in each direction. If maximal head rotation in each direction fails to cause a significant change in vertebral artery luminal caliber or flow, lateral flexion maneuvers are performed in each direction. If these maneuvers are negative, flexion and extension maneuvers are performed. Manipulation of the patient’s head should be performed slowly, during continuous contrast injection of the vertebral artery. Each manipulation is continued until resistance precludes further manipulation, or until there is a significant reduction in vertebral artery lumen and/or flow. Head manipulation should be stopped as soon as a significant vertebral artery flow change is demonstrated in order to prevent iatrogenic vertebral artery injury, which has been reported [22]. When the range of motion limit for each manipulation is reached, the head is briefly held in position until a biplane digital subtraction angiogram is completed, documenting the effect of that maneuver on vertebral artery structure and flow.

The examination is positive for the diagnosis of BHS if any head maneuver causes a marked reduction in vertebral artery luminal caliber and/or flow. The segmental location of motion induced alterations in vertebral artery structure and/or flow defines the anatomical subtype of BHS. A critical goal of definitive catheter-directed diagnosis is anatomical localization of the vertebral artery pathology and underlying musculoskeletal factors to facilitate surgical treatment planning. Differentiation of the atlantoaxial and atlanto-occipital subtypes is essential.

Management of Supra-axial BHS in Children and Young Adults.

How should management of the child with Bowhunter stroke be approached?

Approach to management of the child with Bowhunter stroke

  • Hyperacute and acute management
    • Reperfusion therapies as indicated
    • Cerebral/Cerebellar decompression as indicated
    • Secondary stroke prevention
      • Antiplatelet or antithrombotic therapy
    • Secondary vascular injury prevention
      • Cervical spine immobilization
  • Definitive management
    • Cervical spine surgery
  • Pitfalls to avoid
    • Therapeutic vertebral artery occlusion
    • Vertebral artery stenting

Hyperacute and acute management

Most pediatric patients with BHS will present with posterior circulation stroke. Consequently, the initial management should be directed at the treatment of acute arterial ischemic stroke according to recommended guidelines [54]. If BHS is suspected, we also initiate cervical spine immobilization with a hard cervical collar. Secondary stroke prevention is achieved with antithrombotic agents or antiplatelet agents as soon as permitted by other considerations such as stroke burden, need for surgical intervention and recent administration of thrombolytics. Although randomized clinical trials of cervical artery dissection in adults have shown equal stroke prevention and index vessel reconstitution with equivalent rates of major bleeding by antiplatelet and warfarin therapy to date, studies in pediatric patients and studies of alternative or newer anticoagulant agents are lacking [60]. A complete review of this topic is beyond the scope of this article. Depending on the extent of cerebellar infarction and clinical exam, external ventricular drainage or posterior fossa decompressive surgery may be indicated for some patients.

Foundational principles of definitive surgical management

Supra-axial BHS is, by definition, a dynamic disease process and warrants definitive surgical management to prevent recurrent stroke. Conservative non-surgical management of supra-axial BHS in the pediatric population has been associated with a very high rate of recurrent stroke. In a recent series of 10 pediatric patients with BHS, Fox et al. found that 8 of these 10 patients (80%) had recurrent ischemic events despite appropriate medical therapy [33]. For comparison, in a large adult patient study, only 2 of 132 adults (1.5%) with strokes from vertebral artery dissection who were medically managed had recurrent ischemic events during 12 months of follow-up [60].

Pitfalls to avoid

Although therapeutic vertebral artery occlusion has been reported as a treatment for supra-axial BHS [33], we generally advise against this given the frequent occurrence of synchronous or asynchronous contralateral vertebral artery dissection in pediatric case series (Table 2, Figure 1) [22, 24, 30, 33]. Notably, in such cases, predisposing osseous risk factors may only be apparent unilaterally, or may not be apparent at all. Supra-axial BHS patients with a single vertebral artery, owing to a prior therapeutic occlusion of the contralateral vertebral artery, may face unnecessarily increased stroke morbidity if their remaining vertebral artery is compromised by dissection or other vascular pathology over time. Even children with an adequate circle of Willis may face increased long-term morbidity due to flow-loading of the posterior communicating arteries over a period of decades, since flow-loading of the posterior communicating arteries in this way may increase the lifetime risk of intracranial aneurysm formation and rupture.

Some authors have reported utilizing endovascular stenting as a treatment for pediatric BHS [27, 28, 33]; however, this contradicts the well-established principle of avoiding stenting across mobile segments that predispose the stent to permanent mechanical damage [61]. Multiple examples of stent-failure due to persistent conflict of bone with stented cervical arteries have been reported across a range of stent devices with different mechanical properties and design [62, 63]. Additionally, technical constraints limit the ability of endovascular stents to prevent vessel injury due to traction, impaction or scissoring forces. Balloon-mounted stents would permanently kink, under head rotation forces. The stretching forces that accompany head rotation would render self-expanding stents ineffective as a means of preventing occlusion and recurrent dissection. Therefore, at present, most authors agree that supra-axial BHS should receive surgical treatment directed at correcting the underlying anatomical vulnerabilities. We recommend delaying definitive surgical treatment of supra-axial BHS in children and young adults until the index vertebral artery dissection heals, definitive diagnostic evaluation including catheter-directed angiography with provocative head maneuvers can be performed, and secondary stroke prevention with anti-thrombotic drug therapy can be safely discontinued. Approaches to definitive surgical management broadly include vertebral artery decompression/transposition and spinal fusion surgery [20, 64]. Surgical decision making relies to some extent on the anatomical subtype of supra-axial BHS and underlying musculoskeletal factors revealed by the patient’s diagnostic evaluation.

Surgical Management of Supra-Axial BHS in Children and Young Adults.

What are advantages and disadvantages of alternative surgical approaches to supra-axial BHS?

Pros and Cons of alternative surgical approaches to supra-axial BHS

  • Vertebral artery decompression and transposition
    • Stroke recurrence rate varies depending on technique & experience
    • Addresses atlanto-occipital BHS caused by discrete anomalies
    • Preserves C-spine mobility
  • C1-C2 spinal fusion
    • Low stroke recurrence rate
    • Concurrently treats contralateral BHS
    • No major loss of C-spine mobility
    • May be ineffective for atlanto-occipital BHS
  • Occipital-cervical fusion
    • Low stroke recurrence rate
    • Addresses atlanto-occipital BHS
    • Debilitating loss of C-spine mobility

The two surgical strategies employed in the definitive treatment of supra-axial BHS are vertebral artery decompression/transposition and spinal fusion. The strategy and specific technique should be individualized to each patient based on a critical analysis of their clinical and imaging data. The patient’s vertebral artery pathology and associated musculoskeletal factors should guide selection of the optimal surgical intervention. Differentiation of atlanto-occipital and atlanto-axial subtypes is essential.

Vertebral artery decompression and transposition

Vertebral artery decompression and transposition using a posterior-lateral or far-lateral approach has been widely reported as a definitive treatment for the atlanto-axial subtype of supra-axial BHS in children and adults [5, 20-23, 24, 33, 65]. Similar techniques have frequently been reported for management of the atlanto-occipital subtype of supra-axial BHS in adults and children with good results [5, 20, 46, 66]. Pirozzi Chiusa et al. reported successful treatment of an 8-year-old boy with recurrent stroke by surgical removal of an occipital bone spur [67]. Lu et al. reported their success using a minimally invasive tubular decompression technique for a pediatric patient with atlanto-occipital BHS [29]. Others have identified alternative sites of bony impingement to target for surgical decompression in cases of pediatric atlanto-occipital BHS [47, 48]. Notably, ponticulus posticous, congenital arcuate foramen, and other bony anomalies of the occiput, atlas, and axis have been successfully targeted for resection in patients with atlantoaxial and atlanto-occipital subtypes of supra-axial BHS (Table 2) [21, 24, 25, 29, 31, 33, 47, 67].

Authors describing vertebral artery decompression emphasize resection of anomalous bony structures, release of soft-tissue bands, C1 hemilaminectomy, and transposition of the vertebral artery out of the sulcus arteriosus. Follow up angiography with head rotation challenge is performed in 8-12 weeks after the patient has fully recovered from surgery and muscle spasm has resolved. Some residual kinking of the affected vertebral artery is considered normal. Examination of both vertebral arteries is recommended as unilateral vertebral artery decompression and transposition may unmask contralateral BHS.

If an obvious unilateral bony anomaly is recognized as the cause of supra-axial BHS, vertebral artery decompression/transposition is favored by many surgeons. However, while some authors have reported excellent outcomes with vertebral artery decompression and transposition alone [20, 29, 33], others have reported high stroke recurrence rates due to residual vertebral artery adhesions, continued underlying structural abnormalities, or unrecognized contralateral BHS [20, 21, 24, 25, 34, 64]. While proper patient-oriented treatment selection plays a critical role in determining outcomes, the relative success of vertebral artery decompression is somewhat proportional to the surgeon’s experience with the technique [20, 24].

Spinal fusion surgery

The second type of surgical treatment strategy for BHS is spinal fusion/arthrodesis. The obvious rationale for this treatment approach is that by restricting the movement of the cervical spine that results in vertebral artery injury, recurrent vertebral artery injury and stroke will be prevented. Surgical fusion of C1 to C2 has also been widely reported as a definitive treatment for the atlanto-axial subtype of supra-axial BHS in the pediatric and adult populations [20, 22, 24, 28, 33, 34, 64, 68]. Advocates for surgical fusion cite benefits which include superior treatment efficacy and durability, and concurrent protection of both vertebral arteries with a single operative procedure. Additionally, recent advances in surgical technique have afforded for less invasive procedures with an enhanced safety profile [21, 64, 68]. The most commonly reported fusion techniques include C1-2 fixation using C1 lateral mass screws and C2 pars or pedicle screws. Critics of fusion for pediatric BHS cite the permanent limitation on cervical motion and the potentially negative impact on growth and development associated with fusion of the immature spine. Notably, Braga et al. reported no apparent loss of neck mobility following C1-2 fusion in their series of patients who were less than 10 years old and underwent treatment for pediatric BHS [68]. While this argues against concerns about adverse spinal growth and development, it raises questions about the long-term efficacy of C1-2 fusion in this setting since restricted mobility is the therapeutic objective (Figure 3). While Braga et al. reported no recurrent ischemic events in their series of patients undergoing C1-2 fusion, only limited follow-up was presented.

Recurrent Bowhunter stroke after surgical treatment

While some studies have found vertebral artery decompression to be an effective treatment strategy [20, 25, 29, 33, 46], others have found decompression surgery to be less reliably protective against recurrent stroke. In the adult population, Matsuyama et al. reported that posterior C1-2 fixation achieved better outcomes than vertebral artery decompression [64]. In their series, three of nine patients experienced postoperative stroke recurrence after decompression surgery while there was no stroke recurrence in eight patients after posterior spinal fusion. Importantly, it appears that in the pediatric population, decompressive surgery is most efficacious when an offending musculoskeletal structure is found to be in conflict with the vertebral artery on pre-surgical imaging studies (i.e. ponticulus posticus, arcuate foramen, soft-tissue band, etc.) [33]. C1-2 fusion, on the other hand, is most efficacious for the atlanto-axial subtype of supra-axial BHS when there is no apparent focal target for decompression, but dynamic occlusion of the vertebral artery is confirmed by catheter-directed angiography with head rotation challenge [68].

Unique considerations in the surgical management of atlanto-occipital BHS

Less well understood is the role of C1-2 fusion for the management of atlanto-occipital BHS. Some authors have asserted that Bowhunter dissections distal to the C1 foramen transversarium should not be related to a rotational mechanism that is primarily based on C1-C2 mobility [68]. In support of this view, it has been shown that contralateral head rotation in children with vertebral artery dissection at the atlanto-occipital level produces dynamic occlusion of the vertebral artery between the C1 foramen transversarium and the foramen magnum [21]. Our experience with the atlanto-occipital subtype of BHS also shows that contralateral head rotation produces dynamic vertebral artery occlusion that co-localizes to symptomatic atlanto-occipital dissection sites (Figure 3 and Video 2). While we have observed recurrent stroke due to Bowhunter dissection after C1-2 fusion in one patient with atlanto-occipital BHS, post-fusion angiographic analysis and comparison to pre-fusion angiography suggests that adequate restriction of rotational forces is established by C1-C2 fusion but that alternate modes of cervical spine motility and associated arterial conflict may persist or become active after C1-C2 fusion (Figure 3). Our experience further shows that patients should adhere to conservative activity restrictions, even after C1-C2 fusion is performed. In particular, straining to lift heavy weights while standing erect may lead to injurious degrees of head extension in young athletes with atlanto-occipital BHS, even after C1-C2 fusion. Given all of these considerations, some authors advocate for occipito-cervical fusion in patients with atlanto-occipital BHS, particularly if no surgical target for decompression is found [31, 69, 70].

Anatomically and physiologically oriented treatment guided by patient-specific data

The authors of this review favor an anatomically and physiologically oriented algorithm for the evaluation and treatment of supra-axial BHS (Figure 6). If a patient presents with a supra-axial vertebral artery dissection or posterior circulation stroke of unknown etiology, they are maintained in a collar while receiving medical management with either antiplatelet or anticoagulation therapy. After allowing time for the initial dissection to heal, a follow-up MRA or CTA is performed to assess for adequate improvement in the dissection. If adequately healed, the patient undergoes bilateral catheter-directed vertebral artery angiography with provocative head maneuvers as described above. Based on the results of cross-sectional imaging (multiplanar reformatted images and 3D reconstructions derived from CT angiogram) and the catheter-directed study, a treatment plan is formulated. If the dynamic vertebral artery occlusion demonstrated by angiography is unilateral and a focal musculoskeletal lesion is implicated, we favor surgical decompression as the initial approach, unless there is an instability that indicates a need for spinal fusion (Figure 5). If dynamic vertebral artery occlusion is bilateral, we favor spinal fusion oriented to BHS subtype as the initial approach. We favor occipito-cervical fusion for the atlanto-occipital subtype of supra-axial BHS and C1-C2 fusion for the atlantoaxial subtype of supra-axial BHS. If there is a focal musculoskeletal lesion amenable to simple resection during the fusion, adjunctive resection should be considered if it does not add significant complexity or risk to the fusion, since it may further reduce the probability of stroke recurrence. If dynamic vertebral artery occlusion is unilateral, and there is no musculoskeletal lesion, we favor surgical fusion oriented to the BHS subtype. If surgical exploration discloses a previously undiagnosed musculoskeletal lesion, adjunctive resection is considered.

A critical aspect of our proposed algorithm is that pediatric providers must have a heightened awareness of BHS pathology and a high index of suspicion in the pediatric patient with otherwise unexplained posterior circulation stroke. It is essential to begin the appropriate diagnostic evaluation and treatment for these patients prior to the development of recurrent stroke.

CONCLUSIONS

Posterior circulation stroke in children and young adults should raise a strong suspicion of vertebral artery dissection. In such cases, systematic and detailed neuroimaging investigation for vertebral artery dissection is indicated. When non-traumatic vertebral artery dissection is found in children and young adults, BHS should be suspected. Acute management should include cervical spine immobilization and secondary stroke prevention with anti-thrombotic or anti-platelet therapy. Definitive diagnosis comprising catheter directed angiography with provocative head maneuvers should be postponed until the vertebral artery dissection is healed and skeletal muscle spasm has resolved. Definitive treatment options including vertebral artery decompression and spinal fusion should be tailored to address the anatomical level of the vertebral artery lesion and underlying musculoskeletal factors revealed by detailed diagnostic evaluation. 

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Bowhunter Syndrome in the Pediatric Population

Pediatr Stroke. 2024;10: 1-30

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