pathology of the carotid space - insights into imaging...carotid space anatomy the carotid space is...

16
REVIEW Open Access Pathology of the carotid space Harris U. Chengazi * and Alok A. Bhatt Abstract The complex anatomy of the carotid space within a small confined area is unique to the head and neck and allows for a vast array of pathology. This paper will review the anatomy of the carotid space from the skull base to the thorax, defining its borders at multiple levels, as well as its contents. The paper will also describe the myriad of mass lesions and vascular pathologies that may occur within the carotid space. The discussion will include anatomic considerations in differential diagnoses, imaging features, and lesion characteristics across multiple imaging modalities including CT, MRI, ultrasound, and conventional angiography. Entities discussed include paragangliomas, nerve sheath tumors, meningioma, fibromuscular dysplasia, carotidynia, thrombus, dissection, pseudoaneurysm, and pathology of the deep cervical chain lymph nodes. Understanding the complex and unique anatomy of the carotid space, as well as the nuances of navigating a broad differential, will empower the reader to make an accurate diagnosis. Keywords: Carotid space, Paraganglioma, Meningioma, Carotidynia Key points A lesion centered within the carotid space will displace the ipsilateral parapharyngeal fat anteromedially. The infrahyoid carotid space contains the vagus nerve, as well as the common carotid artery and internal jugular vein. Carotid body tumors will splay the internal and external carotid arteries. Acute internal jugular vein thrombus can be associated with fluid in the retropharyngeal space. A metastatic cystic deep cervical chain lymph node may be from squamous cell carcinoma or papillary thyroid carcinoma. Introduction The complex anatomy of the carotid space within a small confined space in the neck allows for a vast array of pathology. This article will review the anat- omy of the carotid space, as well as the various types of pathology that may occur within this confined re- gion. Masses within this space include paraganglio- mas, nerve sheath tumors, lipomas, and pathology involving the deep cervical chain lymph nodes. As the name implies, the carotid artery and jugular vein may also be involved as part of the pathology. Carotid space anatomy The carotid space is a paired space defined by the ca- rotid sheath, a connective tissue boundary in the neck, that is made by the superficial, middle, and deep layers of the deep cervical fascia. Extending from the jugular foramen at the skull base to the aor- tic arch at the thoracic inlet, the carotid space is di- vided craniocaudally into the supra- and infrahyoid regions. The suprahyoid carotid space is surrounded anteriorly by the masticator and parapharyngeal spaces, laterally by the parotid space, medially by the retropharyngeal space, and posteriorly by the periver- tebral space. A mass centered within the carotid space will displace the parapharyngeal fat/space ante- romedially [1]. The suprahyoid portion of the carotid space contains the internal carotid artery, the internal jugular vein, cranial nerves 9 through 12, the ansa cervicalis, the sympathetic plexus, and deep cervical lymph nodes [1]. The infrahyoid carotid space is surrounded anteriorly by the anterior cervical space, medially by the visceral and retropharyngeal spaces, and posteriorly by the peri- vertebral and posterior cervical spaces. Below the level * Correspondence: [email protected] Department of Imaging Sciences, University of Rochester Medical Center, 601 Elmwood Avenue, P.O. Box 648, Rochester, NY 14642, USA Insights into Imaging © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Chengazi and Bhatt Insights into Imaging (2019) 10:21 https://doi.org/10.1186/s13244-019-0704-z

Upload: others

Post on 20-Jul-2021

3 views

Category:

Documents


0 download

TRANSCRIPT

Page 1: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

REVIEW Open Access

Pathology of the carotid spaceHarris U. Chengazi* and Alok A. Bhatt

Abstract

The complex anatomy of the carotid space within a small confined area is unique to the head and neck andallows for a vast array of pathology. This paper will review the anatomy of the carotid space from the skullbase to the thorax, defining its borders at multiple levels, as well as its contents. The paper will also describethe myriad of mass lesions and vascular pathologies that may occur within the carotid space. The discussionwill include anatomic considerations in differential diagnoses, imaging features, and lesion characteristicsacross multiple imaging modalities including CT, MRI, ultrasound, and conventional angiography. Entitiesdiscussed include paragangliomas, nerve sheath tumors, meningioma, fibromuscular dysplasia, carotidynia,thrombus, dissection, pseudoaneurysm, and pathology of the deep cervical chain lymph nodes. Understandingthe complex and unique anatomy of the carotid space, as well as the nuances of navigating a broaddifferential, will empower the reader to make an accurate diagnosis.

Keywords: Carotid space, Paraganglioma, Meningioma, Carotidynia

Key points

� A lesion centered within the carotid space willdisplace the ipsilateral parapharyngeal fatanteromedially.

� The infrahyoid carotid space contains the vagusnerve, as well as the common carotid artery andinternal jugular vein.

� Carotid body tumors will splay the internal andexternal carotid arteries.

� Acute internal jugular vein thrombus can beassociated with fluid in the retropharyngeal space.

� A metastatic cystic deep cervical chain lymph nodemay be from squamous cell carcinoma or papillarythyroid carcinoma.

IntroductionThe complex anatomy of the carotid space within asmall confined space in the neck allows for a vastarray of pathology. This article will review the anat-omy of the carotid space, as well as the various typesof pathology that may occur within this confined re-gion. Masses within this space include paraganglio-mas, nerve sheath tumors, lipomas, and pathology

involving the deep cervical chain lymph nodes. As thename implies, the carotid artery and jugular vein mayalso be involved as part of the pathology.

Carotid space anatomyThe carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in theneck, that is made by the superficial, middle, anddeep layers of the deep cervical fascia. Extendingfrom the jugular foramen at the skull base to the aor-tic arch at the thoracic inlet, the carotid space is di-vided craniocaudally into the supra- and infrahyoidregions. The suprahyoid carotid space is surroundedanteriorly by the masticator and parapharyngealspaces, laterally by the parotid space, medially by theretropharyngeal space, and posteriorly by the periver-tebral space. A mass centered within the carotidspace will displace the parapharyngeal fat/space ante-romedially [1].The suprahyoid portion of the carotid space contains

the internal carotid artery, the internal jugular vein,cranial nerves 9 through 12, the ansa cervicalis, thesympathetic plexus, and deep cervical lymph nodes [1].The infrahyoid carotid space is surrounded anteriorlyby the anterior cervical space, medially by the visceraland retropharyngeal spaces, and posteriorly by the peri-vertebral and posterior cervical spaces. Below the level

* Correspondence: [email protected] of Imaging Sciences, University of Rochester Medical Center, 601Elmwood Avenue, P.O. Box 648, Rochester, NY 14642, USA

Insights into Imaging

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made.

Chengazi and Bhatt Insights into Imaging (2019) 10:21 https://doi.org/10.1186/s13244-019-0704-z

Page 2: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

of the hyoid, the ansa cervicalis (a loop of the first 3cervical nerves) and cranial nerves 9, 11, and 12 haveexited, thus leaving only cranial nerve 10. The internaljugular vein and the common carotid artery are alsocontained within the infrahyoid carotid space [2].Knowledge of the location of particular structures

within the carotid space can lead to the correct diag-nosis, if not narrow, the differential to a few lesions.The carotid artery is the center of the carotid space,and the jugular vein lies posterolateral to the carotidartery. The 10th cranial nerve lies in the posteriorgroove between these two vessels. The remaining cra-nial nerves 9, 11, and 12 all pierce the carotid sheathanteriorly. The ansa cervicalis is embedded in the an-terior carotid sheath, and the sympathetic plexus isfound posteriorly [3]. Lesions of the carotid spacemay arise from any of the above structures, andradiographic imaging is valuable in aiding diagnosis(Fig. 1).

ParagangliomasParagangliomas, often referred to as glomus tumors,are rare neuroendocrine tumors that may occur any-where in the body where healthy paraganglia occur.They are named for their location within the carotidsheath. These tumors tend to be well-marginated andhighly vascular masses that are rubbery and firm onexam [4]. Paragangliomas can vary greatly in size andmay be associated with germline mutations in thesuccinate dehydrogenase gene family; at least 30% ofpatients with a paraganglioma and no other risk fac-tors may have a genetic mutation that increases therisk for these tumors [5, 6]. The majority of paragan-gliomas are nonfunctional. While functional tumorsare rare, they can be life-threatening and may presentclinically with signs of catecholamine hypersecretion

[7]. Nonfunctioning tumors grow insidiously andpresent as palpable masses or pain at the site of thetumor [8]. It is important to remember that 10% oftumors may be clinically silent and are often detectedincidentally on imaging studies [9]. Due to the highly vas-cular nature of these masses, biopsy carries significantrisk; thus, their diagnosis on imaging is the key [10].Due to their hypervascularity, paragangliomas typic-

ally demonstrate arterial spectral waveforms on ultra-sound imaging, and intense homogenous contrastenhancement on computed tomography (CT) andmagnetic resonance imaging (MRI). Feeding anddraining vessels can also be identified on angiography.Larger tumors may enhance heterogeneously due toareas of necrosis and/or hemorrhage [6]. The classic-ally described “salt and pepper” appearance of thesetumors on MRI refers to high signal areas with slowflow or hemorrhage and low signal areas due to sig-nal voids of tumor vessels classically described onT1-weighted imaging, but can also be on T2-weightedimages [6].

Carotid body tumorThe carotid body is the largest collection of paragan-glia in the head and neck and is found on the medialaspect of the carotid bifurcation bilaterally. Carotidbody tumors are usually found in the fourth or fifthdecade of life and are the most common head andneck paraganglioma. These tumors tend to growslowly and painlessly and present as a lateral neckmass at the level of the carotid bifurcation. Given thelesion’s close proximity to cranial nerves 10–12, pa-tients may also present with dysphagia, odynophagia,hoarseness of voice, or other cranial nerve deficits[11]. Due to their location, and when large enough,

Fig. 1 The carotid space. Illustration demonstrating the contents and configuration of the left carotid space, including cranial nerves IX, X, XI,and XII

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 2 of 16

Page 3: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

they tend to splay the internal and external carotidarteries apart from each other [4] (Fig. 2).

Glomus jugulareParagangliomas at the jugular foramen may arise fromthe tympanic branch of the glossopharyngeal nerve(Jacobson’s nerve), or the auricular branch of thevagus nerve (Arnold’s nerve), and are referred to asglomus jugulare (Fig. 3). These tumors have a 3:1predilection for females over males and typicallypresent in the fifth or sixth decades of life. Patientsclinically present with pulsatile tinnitus, hearing lossor vertigo, and other symptoms related to the cranialnerves within the jugular foramen (glossopharyngeal,vagus, and accessory) [4]. Demineralization of thebony cortex surrounding the jugular foramen causesan enlargement of the foramen due to permeative,“moth-eaten” appearance of erosion on CT [6]. Thesetumors can extend into the tympanic cavity (glomusjugulotympanicum) and may also involve the internalcarotid artery or internal jugular vein.

Glomus vagaleThe vagus nerve is the longest cranial nerve, and al-though paragangliomas may arise anywhere along itstract, they are most commonly found at the ganglionnodosum (inferior ganglion) at the level of the C1 lateralmass [12]. These tumors have a heavy predilection forfemales in the fifth or sixth decades of life, however theyare less common than the carotid body tumor or glomusjugulare [13]. Clinically, these present as asymptomaticmasses posterior to the angle of the mandible; however,symptoms of vagal nerve dysfunction such as dysphagia,hoarseness, and vocal cord paralysis may develop late inthe course. Although usually confined to the carotidspace, these tumors can grow superiorly into the poster-ior fossa, entering via the jugular foramen, or inferiorlyto the carotid bifurcation. As mentioned previously, thevagus nerve lies within the posterior aspect of the ca-rotid space, and therefore, a large glomus vagale will an-teriorly displace the carotid artery (Figs. 4 and 5).

Fig. 2 Carotid body tumor. a Axial CT image demonstrates awell-circumscribed, enhancing mass centered in the right carotidspace (arrows) that causes splaying of the right internal (i) andexternal (e) carotid arteries. There is mass effect on the internal jugularvein (j). The left carotid space (dotted circle) demonstrates the normalrelationship of the carotid and jugular vessels. b Axial T2-weighted MRimage shows a well-circumscribed hyperintense mass (white arrows)with multiple internal flow voids (black arrows). c DSA demonstratesan intensely hypervascular mass (arrowheads) centered at the carotidbifurcation. Again seen is splaying of the internal and external carotidarteries. d Spectral Doppler ultrasound confirms hypervascularity(arrows) and internal arterial flow (spectral tracing) of this lesion

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 3 of 16

Page 4: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

Nerve sheath tumorsPrimary neurogenic tumors that arise from nerve sheathsoutside of the central nervous system are termed periph-eral nerve sheath tumors. The overwhelming majority of

these tumors are benign; however, malignant nerve sheathtumors can occur. Although major nerve trunks are mostcommonly affected, almost any peripheral nerve can beinvolved. Typically, peripheral nerve sheath tumors arecategorized as either schwannoma or neurofibroma, bothof which are associated with neurofibromatosis. Both cat-egories of nerve sheath tumors have similar imaging find-ings; however, they can be differentiated by theirconfiguration relative to the affected nerve (Fig. 6). On CTimaging, they tend to be hypoattenuating relative tomuscle and enhance with contrast administration. OnMRI, nerve sheath tumors present as low T1 signal andhigh T2 signal lesions which have avid contrast enhance-ment [14].

NeurofibromaNeurofibromas are most frequently solitary lesions inyoung patients between 20 and 30 years of age. Tenpercent of these neurofibromas are associated withneurofibromatosis and can be categorized as localized,plexiform, or diffuse. Diffuse neurofibromas are asubcutaneous lesion that do not present within thecarotid space. Localized neurofibroma appear similarto solitary lesions but tend to be larger, multiple, anddeeper in location. Due to a neurofibroma’s intimate

Fig. 4 Glomus vagale. Axial T2-weighted MR image with fat suppressionshows a well-circumscribed hyperintense mass (white arrows) with aninternal “salt and pepper” appearance. This appearance is due to signalvoids of tumor vessels (black arrows) and high signal areas due to slowflow and/or hemorrhage. Note the anterior displacement of the rightinternal (i) and external (e) carotid arteries, and lateral displacement ofthe right internal jugular vein (j). The vessels are labeled in their normalconfiguration on the left

Fig. 3 Glomus Jugulare. Sagittal (a) and axial (b) T1 post-contrastimages demonstrate an enhancing mass (white arrows) centeredat the jugular foramen (arrowheads). Note the prominent flowvoids (black arrows) typical of a glomus tumor (paraganglioma)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 4 of 16

Page 5: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

association with the affected nerve, these tumorsgrow in a longitudinal and fusiform manner (Fig. 6).Tapered ends of the tumor, with an appearance of theparent nerve “entering and exiting,” the tumor canalso be seen. A characteristic target sign or fish-eyeappearance of the lesion referring to a central hypoin-tense region has also been described [15]. Plexiformneurofibromas are pathognomic for neurofibromatosistype I (Fig. 7); these tumors are extensive and growalong a nerve and plexus and carry an increased riskof malignant transformation.

SchwannomaSchwannomas represent up to 5% of benign soft tis-sue neoplasms and typically present in patients 20–

40 years of age. Most schwannomas are solitary; how-ever, they are associated with neurofibromatosis, inwhich case they can be multifocal and plexiform aswell. Schwannomas are also typically asymptomaticuntil late in the disease course, where neurologicsymptoms associated with compression of the associ-ated nerve may present. As mentioned previously, en-hancement pattern of schwannoma can be similar toneurofibroma, and therefore, a salient differentiatingimaging finding between the two is the eccentric pos-ition relative to the parent nerve in schwannoma(Figs. 6 and 8). Schwannomas are also more likely tobe heterogeneous in appearance with areas of degen-eration and cystic cavitation when large [15]. “An-cient” schwannoma, presenting with very advanceddegeneration, calcification, and hyalinization, have alsobeen described in the literature [14]. It is importantto remember that in addition to schwannomas involv-ing the cranial nerves, they may also be found withinthe sympathetic chain. These lesions will be locatedanteriorly or medially within the carotid space, dis-placing the carotid vessels laterally (Fig. 9).

LipomaLipomas are common, benign, well-circumscribed,and encapsulated soft masses comprised of matureadipocytes. Although these are most commonly foundas subcutaneous nodules, they can be found anywherein the body. These tumors demonstrate characteristiclow (fat) attenuation on CT imaging and follow sub-cutaneous fat signal on all MRI sequences. Persistentareas of high T2 signal after fat saturation are a wor-risome feature. When no suspicious features arepresent, MRI is 100% specific, and if suspicious fea-tures are present, MRI is 100% sensitive, and thus,MRI is the preferred imaging modality [16].

Carotid sheath meningiomaMeningiomas are the most common extra-axial neo-plasms of the central nervous system. Most meningi-omas occur intracranially and are by definition closelyassociated with the dura. Tumors in the region of theskull base, in particular at the jugular foramen, canextend inferiorly and into the carotid space (Fig. 10).Primary extradural meningiomas are very rare, buthave also been described, and are thought to originatefrom embryologic arachnoid rests. Meningiomas aretypically mildly hyperattenuating on CT (60%), andup to 20% are associated with calcifications. The boneoverlying meningioma is also often affected, mostcommonly with reactive hyperostosis. On MRI, men-ingiomas typically demonstrate iso- to hypointensityrelative to gray matter on T1-weighted images andiso- to hyperintensity on T2-weighted images. A

Fig. 5 Glomus vagale. a Sagittal T1-weighted fat-saturated post-contrastimage demonstrates anterior displacement of the left internal carotid artery(i) by a well-circumscribed and enhancing mass (arrows). b Axial T2-weighted fat-saturated image demonstrates the lesion to be hyperintense(arrows), causing anterior displacement of the left internal carotid artery (cl).The normal position of the right internal carotid artery (cr) is also seen

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 5 of 16

Page 6: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

characteristic “dural tail” sign may be present, whichconfirms the tumors’ association with the dura. MRIcan also detect sequelae of the mass effect such asvenous sinus thrombosis and invasion, as well as par-enchymal edema [17].

Pathology of the carotid artery and internal jugular veinThe vascular components of the carotid space are alsosubject to a variety of pathologies. These may be con-genital or acquired.

Carotid dissectionArterial dissection occurs when the innermost andleast elastic layer of an arterial wall, the tunica in-tima, tears and allows the blood to enter, and formhematoma, in the tunica media (Figs. 11 and 12). Anintimal tear can occur spontaneously, or may be re-lated to trauma or iatrogenic causes. Regardless ofthe cause, it usually results in narrowing of the truevessel lumen. Carotid arterial dissection accounts forroughly 20% of causes of stroke in patients under 45years of age. Typical symptoms include pain, ipsilat-eral Horner syndrome, and sequelae of brain ischemia[18]. It is important to remember the sympathetic fi-bers that carry innervation for a facial sweating runalong the external carotid artery; thus, a dissectionthat involves only the internal carotid artery will onlyresult in ptosis and meiosis, or a partial Horner’s

syndrome [19]. A conventional angiogram is consid-ered the gold standard for diagnosis but is invasiveand only assesses luminal diameter and not arterialwall thickness or configuration. Color duplex ultra-sound detects mural hematoma/thrombus as a thick-ened hypoechoic wall and can demonstrate the effectsof luminal compromise dynamically. CT angiographyoffers a higher spatial resolution for evaluation of theintimal flap and vessel expansion than MRI, but is lesssensitive for intracranial sequelae of ischemia and can belimited by artifact when in close proximity to the bone.MRI with T1 fat-suppressed sequences are highly sensitivefor intramural blood, and post-contrast imaging can reli-ably characterize luminal narrowing [20].

Carotid pseudoaneurysmPseudoaneurysm occurs when there is an injury of the tu-nica intima and media, resulting in a hematoma that is con-tained only by the thin outer adventitial layer of the vessel(Fig. 13). A pseudoaneurysm can form as a result of trauma(Fig. 14), dissection, vasculitis, infection, or be iatrogenic(Fig. 15). This entity can often be asymptomatic, and dis-covered incidentally; however, it carries a significant risk ofrupture with high mortality rates. On ultrasound, a hypoe-choic cystic structure can be demonstrated adjacent to thetrue vessel. Color duplex imaging can demonstrate a “toand fro” color flow and bidirectional Doppler waveform inthe pseudoaneurysm neck. Within the sac itself, swirling

Fig. 6 Nerve sheath tumors. a Illustration demonstrating the relatively eccentric configuration of a schwannoma relative to the affected nerve. bConversely, neurofibromas tend to be fusiform, longitudinal, and interspersed in the nerve bundle

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 6 of 16

Page 7: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

blood can create the so-called “yin-yang” sign. CT imagingcan demonstrate irregularity of a vessel wall and irregularoutpouching. Hematoma with contrast extravasation seenon angiographic studies is compatible with rupture and ac-tive bleeding. When a pseudoaneurysm is large enough, itis important to note that the entire sac may not enhance, as

Fig. 7 Plexiform neurofibroma. a Axial T1-weighted MR imagedemonstrates a mass that is iso−/hypointense to muscle (arrows). bAxial T2-weighted MR image demonstrates numerous hyperintensemasses involving the left carotid space (white arrows). The leftinternal carotid artery (i) is displaced posterolaterally. Note thecharacteristic “fish-eye” or “target” appearance of this lesion (blackarrows). This patient had neurofibromatosis, and extensive trans-spatial neurofibromas can be seen in other portions of theneck (arrowheads)

Fig. 8 Schwannoma. a Axial T1 weighted MR image shows a well-circumscribed mass (arrows), which is low in signal. b T2-weightedMR image show that this mass is T2 hyperintense (arrows). c Post-contrast T1-weighted image shows avid and uniform enhancementof the mass (arrows)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 7 of 16

Page 8: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

the pseudoaneurysm can partially thrombose. MRI withT1-weighted fat-suppressed sequences allows for evaluationof intraluminal thrombus and of pseudoaneurysm sac size.Digital subtraction angiography remains the gold standardfor evaluation of pseudoaneurysm and simultaneously of-fers a therapeutic potential [21].

Carotid thrombusCarotid thrombus can occur as a result of direct traumaor in relation to severe carotid artery stenosis with

Fig. 9 Sympathetic plexus schwannoma. a Axial CT imagedemonstrates a well-circumscribed mass (white arrows) that laterallydisplaces the left internal carotid artery (black arrowhead) and leftinternal jugular vein (white arrowhead). The left parapharyngeal fat ismedially displaced (black arrow). Note the normal configuration of theright carotid space and parapharyngeal fat (dotted circle). b Axial T2fat-suppressed MR image demonstrates homogenous hyperintensity ofthis mass (white arrows). c Axial T1 post-contrast fat-saturated MRimage demonstrates homogenous enhancement of the lesion. Notethe anteromedial location of the lesion relative to the carotid vessels,indicating sympathetic plexus origin

Fig. 10 Meningioma. a Sagittal T1-weighted post-contrast MR imagedemonstrates an enhancing mass (white arrows) extending from theposterior fossa through the jugular foramen (black arrows) into theright carotid space. An enhancing dural tail is seen (arrowhead). bAxial T2-weighted MR image demonstrates the mass to beintermediate in signal (white arrows), anteriorly displacing theinternal carotid artery (i). The normal position of the left internalcarotid artery is also seen. c Axial non-contrast CT imagedemonstrates hyperostosis of the bone adjacent to the knownlesion (white arrows). Note the thickness of the normal left mastoidbone cortex (black arrow)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 8 of 16

Page 9: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

atherosclerotic plaque. Patients with internal carotid ar-tery thrombosis carry a 5 times higher rate of recurrentstroke than patients without thrombosis. Duplex sonog-raphy is capable of demonstrating intraluminalthrombus; however, CT angiography is more sensitive[22]. Magnetic resonance (MR) angiography can alsodemonstrate intraluminal filling defects, and concur-rent MRI is important when looking for downstreamsequelae of thrombus, such as infarct. In patients withocclusive thrombus, inflammatory changes about thecarotid arteries including surrounding tissue edema,free fluid, and vessel expansion may also be visualized.

Fibromuscular dysplasiaFibromuscular dysplasia of the carotid vessels is an un-common and often asymptomatic pathology and there-fore often an incidental finding. However, symptomaticpatients can present with cerebral infarction, transientischemia, or subarachnoid hemorrhage. Although fibro-muscular dysplasia can occur in any of the three arterialwall layers, the involvement of the tunica media is mostcommon, representing over 90% of cases. The arterialwall becomes dysplastic due to fibrous thickening anddestruction of the elastic lamina, often leading to multi-focal stenosis and areas of luminal expansion (Fig. 16). Itis important to note that the mural dilation is oftengreater than the normal vessel diameter, thus helpingdistinguish fibromuscular dysplasia from atheroscleroticdisease. This yields the characteristic “string-of-beads”appearance of the dysplastic vessel, a sign that is seen inover 80–90% of cases. In severe cases, fibrous dysplasiacan be complicated by arterial dissection, saccularaneurysm formation, or arteriovenous fistula formation.CT angiography and MRI angiography are both utilizedregularly; however, CTA is preferred due to being readily

available, fast scan time, higher spatial resolution, anddecreased potential for artifact [23].

CarotidyniaAlso known as Fay syndrome, carotidynia is a rare entitycharacterized by unilateral pain in the region of the ca-rotid bifurcation. Pain tends to be pulsating and con-tinuous in sensation, but is a self-limiting process, andoften spontaneously resolves in 1–2 weeks. Laboratory

Fig. 11 Arterial dissection. Illustration of the normal layers of anarterial vessel (left). Dissection occurs when a tear in the intimal layerallows blood to collect between the tunica intima and tunica media,creating a false lumen (right)

Fig. 12 Carotid arterial dissection. a Axial contrast-enhanced CTimage demonstrates an intimal flap (black arrow) and "doublelumen" sign (white arrows) in the right common carotid artery. bSagittal grayscale ultrasound image confirms the diagnosis,demonstrating the intimal flap (arrows)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 9 of 16

Page 10: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

workup is negative for immunological markers, and pa-tients are often treated with NSAIDs. Although contro-versial, the etiology of carotidynia is stipulated to berelated to an idiopathic inflammatory process of the ca-rotid bifurcation and, therefore, has recently beentermed transient perivascular inflammation of the ca-rotid artery syndrome (TIPIC). Ultrasound, CT, andMRI of the carotid arteries demonstrate fusiform trans-mural thickening without luminal compromise. Dopplerultrasound demonstrates normal flow velocities withoutevidence of turbulent flow, as opposed to other patholo-gies that may cause narrowing of the lumen (such as se-vere atherosclerotic disease). CT and MRI fail todemonstrate signs of vascular inflammation outside ofthe carotid vessels. MRI demonstrates hypointensity ofthe vessel wall on fat-saturated T1-weighted imaging,precluding the possibility of a mural hematoma.Post-contrast MR images demonstrate intense enhance-ment of the carotid bifurcation, supporting the proposedinflammatory etiology (Fig. 17). Follow-up imaging afterresolution of symptoms usually demonstrates a normalappearance of the carotid bifurcation [24].

Internal jugular vein thrombosisThe paired internal jugular veins drain the majority ofblood from the cranium, serving as cervical extensionsof the dural venous sinuses. Thrombosis of the internaljugular veins can occur for many reasons, including ex-trinsic compression, chronic indwelling catheter, recentsurgery, head and neck infections (Lemierre syndrome),malignancy, hypercoagulability syndromes, an extensionof dural sinus thrombosis, and spontaneous thrombosis.Venous duplex ultrasonography is the diagnostic test ofchoice and demonstrates a dilated and incompressible

vein; the intraluminal thrombus is often visualized aslow-level echogenicity (Fig. 18). There is a limited evalu-ation of the vessels behind the clavicle and sternum, butDoppler ultrasound can demonstrate abnormal, mono-phasic waveforms due to a more proximal occlusivethrombus, and no significant flow change with Valsalvamaneuver. CT findings of IJ thrombus include vessel ex-pansion, surrounding inflammatory change and fluid/edema within the retropharyngeal space (Fig. 18) [25].Contrast-enhanced CT can also help delineate the intra-luminal thrombus, and enhancement of the vessel wallcan be seen due to contrast uptake by the vasa vasorum.MRI is not used routinely for primary diagnosis of veinthrombosis due to expense and inconvenience in theacute setting; however, similar findings of vessel expan-sion, surrounding inflammatory change and T1 hyperin-tense intraluminal filling defect can be visualized.

Pathology of the deep cervical lymph node chainThe cervical lymph nodes have well-defined regionalclassification criteria and myriad pathology; thecomplete discussion of which is beyond the scope of thispaper. In general, lymph nodes are classified as abnor-mal when they measure greater than 1 cm in the shortaxis or demonstrate other size independent indicators ofpathology such as loss of the fatty hilum, rounded shape,and focal necrosis or cystic change.

InfectiousInfections in the head and neck can result in cervical ad-enitis, or inflammatory change of the deep cervicallymph nodes. The most common cause of cervical ade-nitis is a viral infection of the upper respiratory tract;however, there is a broad differential including bacterial

Fig. 13 Arterial pseudoaneurysm. Illustration of the normal layers of an arterial vessel (left). Pseudoaneurysm occurs when a tear through thetunica intima and media layers results in blood only contained by the adventitial layer (right)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 10 of 16

Page 11: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

Fig. 14 Traumatic carotid artery pseudoaneurysm. a Axial CTangiogram image demonstrates irregularity of the left common carotidartery (arrowheads) after stab wound to the neck. The left internaljugular vein (black arrow) is also injured. Note medialization (paralysis)of the left vocal fold (white arrow), due to concomitant vagus nerveinjury. b Sagittal curved reformatted CT angiogram image betterdemonstrates the focal pseudoaneurysm (arrowheads) of the leftcommon carotid artery, proximal to the bifurcation

Fig. 15 Iatrogenic pseudoaneurysm. a Conventional angiogram andb axial CT angiogram images demonstrating the appearance of apseudoaneurysm (white arrows)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 11 of 16

Page 12: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

infection, tuberculosis, and HIV. Affected lymph nodesare generally enlarged (greater than 1 cm in the shortaxis). In advanced infections, lymph nodes can undergoliquefactive necrosis, and are then referred to as sup-purative lymph nodes. If left untreated, the suppurativelymph node may rupture, spilling into the deep spaces ofthe neck (Fig. 19). The most common causative agentsfor suppurative adenitis are Staphylococcus aureus andgroup A streptococcus bacterium [26]. CT scan withcontrast is the exam of choice to evaluate these patients,since it is quick and readily available in the emergencysetting.

NeoplasticHodgkin lymphoma (HL) and non-Hodgkin lymphoma(NHL) commonly involve the head and neck. HL andNHL cannot be reliably distinguished via imaging, how-ever should be considered in patients with B symptoms(fever, unintentional weight loss, or night sweats).Lymphoma typically presents as painless or growinglymphadenopathy [27]. On CT imaging, lymphomatousinvolvement can have varying degrees of enhancement,and involvement can be extensive. A conglomeration oflymph nodes may insinuate within the deep spaces ofthe neck, encasing important structures. It is importantto remember that lymphoma does not typically cause lu-minal narrowing of arterial vasculature, a feature whichmay help distinguish the disease from others (Fig. 20).Although CT is the gold standard for the initial evalu-ation and staging of lymphoma, it only provides struc-tural information. Positron emission tomography (PET)has an increasing role in lymphoma evaluation as it addsfunctional information. PET is the key to assessing dis-ease response to therapy, as well as finding residual orrecurrent disease after treatment.Metastatic disease is also a common cause of adenopa-

thy in the deep cervical chain. Although squamous cell

Fig. 16 Fibromuscular dysplasia. MR angiography image of the bilateralinternal carotid arteries demonstrates a "string-of-beads"appearance (arrows)

Fig. 17 Carotidynia. a Axial time of flight image demonstrates a rindof soft tissue surrounding the left internal carotid artery (LIC). Notethe normal appearance of the right internal carotid artery (RIC). bCoronal post-contrast T1-weighted image shows avid enhancementof the rind of soft tissue (arrows) surrounding the left internalcarotid artery (LIC). Note the normal appearance of the right internalcarotid artery (RIC). c Follow-up approximately 4 months later,coronal post-contrast T1-weighted fat-saturated image showsdecreased thickness of the rind of soft tissue (arrows)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 12 of 16

Page 13: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

carcinoma is the most common (representing 90% ofhead and neck cancers) [28], many other malignanciesincluding EBV-related nasopharyngeal carcinoma, thy-roid carcinoma, breast carcinoma, melanoma, and evenlung carcinoma are also seen to metastasize to the necklymph nodes [29]. Squamous cell carcinoma and papil-lary thyroid carcinoma are well known to demonstratecystic nodal metastasis (Fig. 21) [30].

Fig. 18 Acute jugular vein thrombosis. a Sagittal color flow Dopplerultrasound image demonstrates an occlusive hypoechoic thrombus(arrows) within the jugular vein. There is an absence of color fillwithin the vessel. b Axial contrast-enhanced CT image shows anexpanded and non-enhancing right internal jugular vein (RIJ).Compare to the normal left internal jugular vein (LIJ). Note theretropharyngeal fluid (arrows), a common finding with acute jugularvenous thrombosis

Fig. 19 Suppurative lymph node. Patient presenting with fever, sorethroat, cough, and a palpable left neck mass. a Axial contrast-enhanced CT image demonstrates an enhancing left deep cervicalchain lymph node (white arrows), with a hypoattenuating center(star). The left internal carotid artery (IC) is medially displaced. b Axialcontrast-enhanced CT image 3 days later demonstrates rupture(arrows) of the suppurative node. Note the preserved fat planes inthe normal right carotid space (dotted circle). c Sagittal CT imagedemonstrates fluid tracking along the left carotid space from thelymph node rupture (arrows)

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 13 of 16

Page 14: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

It is important to remember that primary malignancy ofthe head and neck has the potential to directly invade thecarotid space, which ultimately has staging and treatmentimplications. For example, in the setting of oropharyngealnon-HPV associated squamous cell carcinoma, encase-ment of the carotid artery upstages the lesion to T4b dis-ease using the American Joint Committee on Cancer(AJCC) 8th edition criteria (Fig. 22) [31].

MimicsIncomplete obliteration of a branchial tract during de-velopment can result in a branchial cleft cyst (BCC).The second branchial cleft yields 95% of all branchial le-sions. It is important not to confuse a developmentalanomaly such as a BCC for a cystic lymph node, as theformer is a completely benign entity. These lesions areusually well-defined, thin-walled cystic structures. A sec-ond BCC typically occurs lateral to the carotid space,along with the anterior margin of the sternocleidomas-toid muscle, and can extend deep to the muscle (Fig. 23).Occasionally, these cysts may demonstrate a “beaked”appearance, when they invaginate between the internaland external carotid arteries. They can occasionally becomplex and demonstrate low-level echoes on ultra-sound, as well as internal septa. These lesions do nottypically appear hyperemic on ultrasound or enhance onCT and MR; however, if they are infected or inflamed,thickening of the wall with intense enhancement andsurrounding fat stranding can also be seen [32].

Fig. 20 Lymphoma. Axial T1 post-contrast fat-suppressed imagedemonstrates a conglomerate of heterogeneously enhancingmasses that completely encase the left internal (LIC) and external(LEC) carotid arteries. Note that the lumen of the LIC is similar incaliber to the right internal carotid artery (RIC)

Fig. 21 Cystic metastatic lymph node. Patient presenting with apalpable left neck mass, no other symptoms. a Axial contrast-enhancedCT image demonstrates a well-circumscribed, low attenuation lymphnode in the left carotid space (white arrows); note some areas ofperipheral nodularity. This node causes mass effect with anteriordisplacement of the left internal jugular vein (LIJ), and lateraldisplacement of the sternocleidomastoid muscle (SCM). b Axial contrast-enhanced CT image at a higher level in the same patient demonstratesan ill-defined mass centered at the left tongue base (arrows). Biopsy ofthis lesion demonstrated squamous cell carcinoma

Fig. 22 Direct spread of non-HPV-associated squamous cellcarcinoma into the carotid space. Axial contrast-enhanced, fat-suppressed T1 image demonstrates a large, avidly enhancing andinfiltrating mass that invades the right carotid space (whitearrowheads). The right carotid artery (RIC) is encased, narrowed, andlaterally displaced when compared to the left internal carotid artery(LIC). Encasement of the carotid artery upstages the disease to T4b.There is also a left retropharyngeal lymph node (black arrows), justmedial to the LIC

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 14 of 16

Page 15: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

ConclusionClearly, the carotid space has a complex anatomy confinedto a small space. Knowledge of the anatomy within this spaceallows for the radiologist to correctly identify pathology. If alesion involving the carotid space is suspected, one must in-terrogate from the level of the skull base at the jugular for-amen inferiorly to the mediastinum. Pathology involving oroccurring along cranial nerves 9 through 12, the carotid ar-tery, and internal jugular vein, as well as deep cervical lymphnode chain, must all be considered.

AcknowledgementsWe would like to thank Nadezdha Kiriyak and Gwen Mack for theillustrations, as well as Sarah Klingenberger for her help in image formattingand annotation.

Authors’ contributionsBoth authors read and approved the final manuscript.

Competing interestsThe authors declare that they have no competing interests.

Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations.

Received: 7 September 2018 Accepted: 24 October 2018

References1. Gervasio A, D'Orta G, Mujahed I, Biasio A (2011) Sonographic anatomy of

the neck: the suprahyoid region. J Ultrasound 14:130–1352. Gervasio A, Mujahed I, Biasio A, Alessi S (2010) Ultrasound anatomy of the

neck: the infrahyoid region. J Ultrasound 13:85–893. Kuwada C, Mannion K, Aulino JM, Kanekar SG (2012) Imaging of the carotid

space. Otolaryngol Clin North Am 45:1273–12924. Lee KY, Oh YW, Noh HJ et al (2006) Extraadrenal paragangliomas of the

body: imaging features. AJR AJR Am J Roentgenol 187:492–5045. Sridhara SK, Yener M, Hanna EY, Rich T, Jimenez C, Kupferman ME (2013)

Genetic testing in head and neck Paraganglioma: who, what, and why? JNeurol Surg B Skull Base 74:236–240

6. Woolen S, Gemmete JJ (2016) Paragangliomas of the head and neck.Neuroimaging Clin N Am 26:259–278

7. Roman S (2004) Pheochromocytoma and functional paraganglioma. CurrOpin Oncol 16:8–12

8. Saurborn DP, Kruskal JB, Stillman IE, Parangi S (2003) Best cases from the AFIP:paraganglioma of the organs of Zuckerkandl. Radiographics 23:1279–1286

9. Dunnick NR, Korobkin M (2002) Imaging of adrenal incidentalomas: currentstatus. AJR AJR Am J Roentgenol 179:559–568

10. Vanderveen KA, Thompson SM, Callstrom MR et al (2009) Biopsy ofpheochromocytomas and paragangliomas: potential for disaster. Surgery146:1158–1166

11. Davidovic LB, Djukic VB, Vasic DM, Sindjelic RP, Duvnjak SN (2005) Diagnosisand treatment of carotid body paraganglioma: 21 years of experience at aclinical center of Serbia. World J Surg Oncol 3:10

12. Gray H, Davies DV, Coupland RE (1967) Gray’s anatomy: descriptive andapplied. Longmans, London

13. Rao AB, Koeller KK, Adair CF (1999) From the archives of the AFIP.Radiographics 19:1605–1632

14. Schultz E, Sapan MR, Mcheffey-Atkinson B, Naidich JB, Arlen M (1994) Casereport 872. “Ancient” schwannoma (degenerated neurilemoma). SkeletalRadiol 23:593–595

15. Lin J, Martel W (2001) Cross-sectional imaging of peripheral nerve sheathtumors: characteristic signs on CT, MR imaging, and sonography. AJR AJRAm J Roentgenol 176:75–82

16. Gaskin CM, Helms CA (2004) Lipomas, lipoma variants, and well-differentiated liposarcomas (atypical lipomas): results of MRI evaluations of126 consecutive fatty masses. AJR AJR Am J Roentgenol 182:733–739

17. Nadgir R, Yousem DM (2017) Neuroradiology: the requisites, 4th edition.Elsevier

18. Kadkhodayan Y, Jeck DT, Moran CJ, Derdeyn CP, Cross DT 3rd (2005)Angioplasty and stenting in carotid dissection with or without associatedpseudoaneurysm. AJNR Am J Neuroradiol 26:2328–2335

19. Borgman CJ (2012) Horner syndrome secondary to internal carotid arterydissection after a short-distance endurance run: a case study and review. JOptom 5:209–216

20. Cruciata G, Parikh R, Pradhan M, Shah J, Greif E, Stein EG (2017) Internalcarotid artery dissection and pseudoaneurysm formation with resultantipsilateral hypoglossal nerve palsy. Radiol Case Rep 12:371–375

21. Saad NE, Saad WE, Davies MG, Waldman DL, Fultz PJ, Rubens DJ (2005)Pseudoaneurysms and the role of minimally invasive techniques in theirmanagement. Radiographics 25:S173–S189

Fig. 23 Second branchial cleft cyst. a Axial contrast-enhanced CTimage demonstrates a well-circumscribed and hypoattenuatinglesion (arrowheads) along the anterior margin of the rightsternocleidomastoid muscle (SCM) and anterolateral to the rightcarotid space, internal carotid artery (RIC), and internal jugularvein (RIJ). b Color Doppler ultrasound image demonstrates thatthis lesion (arrows) is hypoechoic with low-level echoes. There isno internal vascularity or peripheral hyperemia

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 15 of 16

Page 16: Pathology of the carotid space - Insights into Imaging...Carotid space anatomy The carotid space is a paired space defined by the ca-rotid sheath, a connective tissue boundary in the

22. Pisimisis GT, Kantor B, Kalra M, Pipinos II (2010) Thrombus of the internalcarotid artery: the contribution of computed tomographic angiography toclinical management. Vasc Endovascular Surg 44:302–304

23. Furie DM, Tien RD (1994) Fibromuscular dysplasia of arteries of the headand neck: imaging findings. AJR Am J Roentgenol 162:1205–1209

24. Santarosa C, Stefanelli S, Sztajzel R, Mundada P, Becker M (2017) Carotidynia:a rare diagnosis for unilateral neck pain revealed by cross-sectional imaging.Case Rep Radiol 2017:7086854

25. Bhatt AA (2018) Non-traumatic causes of fluid in the retropharyngeal space.Emerg Radiol 25:547-551

26. McKellop JA, Bou-Assaly W, Mukherji SK (2010) Emergency head & neckimaging: infections and inflammatory processes. Neuroimaging Clin N Am20:651–661

27. Aiken AH, Glastonbury C (2008) Imaging Hodgkin and non-Hodgkinlymphoma in the head and neck. Radiol Clin North Am 46:363–378 ix-x

28. Sanderson RJ, Ironside JA (2002) Squamous cell carcinomas of the head andneck. BMJ 325:822–827

29. López F, Rodrigo JP, Silver CE et al (2016) Cervical lymph node metastasesfrom remote primary tumor sites. Head Neck 38:E2374–E2385

30. Mokhtari S (2012) Mechanisms of cyst formation in metastatic lymph nodesof head and neck squamous cell carcinoma. Diagn Pathol 7:6–6

31. Amin MB, Edge S, Greene F et al. (2017) AJCC cancer staging manual, 8thedition. Springer, Chicago

32. Mittal MK, Malik A, Sureka B, Thukral BB (2012) Cystic masses of neck: apictorial review. Indian J Radiol Imaging 22:334–343

Chengazi and Bhatt Insights into Imaging (2019) 10:21 Page 16 of 16