8 Nonatherosclerotic Arterial Diseases: Vasculitis, Fibromuscular Dysplasia, Cystic Adventitial Disease, Compression Syndromes

Exploring all relevant causes of nonatherosclerotic vascular occlusions would exceed our scope. The most frequent causes are listed in Table 8.1, where they are categorized as diseases of the vessel wall or diseases of the vessel contents.

Table 8.1 Arterial occlusive diseases without atherosclerosis (Modified from Amendt²)

It is rare for the symptoms of decreased arterial blood flow to indicate the etiology of a disease. More commonly, eliciting information on patient’s age and history, the occlusion site, associated symptoms, and typical duplex ultrasound findings will direct the attentive examiner to an alternative diagnosis other than peripheral arterial occlusive disease (PAOD). Many patients will already have suffered a long ordeal of going from one specialist to the next, or they may present with irreversible complications of their underlying disease. The use of color duplex sonography (CDS) in this setting will often supply us with typical and sometimes pathognomonic findings that allow for immediate therapeutic action.³³

8.2 Examination Technique

Similar to a vascular survey in PAOD, ultrasound imaging should cover the arteries of the upper and lower extremities, the abdominal vessels, the extracerebral arteries, and also the intracerebral arteries in patients with suspected giant-cell arteritis (GCA). When superficial vessels are imaged for the assessment of superficial vascular disease (superficial temporal artery [STA], subcutaneous veins), the result will depend critically on transducer selection. Images obtained with different transducers are compared in Fig. 8.1. The temporal arteries should be scanned with a high-frequency (at least 10 MHz) linear array transducer. First, the common temporal artery is imaged in a longitudinal scan anterior to the ear. Next, its parietal and frontal branches are defined in longitudinal and transverse scans over their full accessible lengths. This examination is then repeated on the contralateral side. Additional information will be found by transducer-induced compression of temporal artery, resulting in luminal collapse and delineation of the true arterial wall thickness by summation of the proximal and distal wall (see below). Extra coupling gel may have to be used behind the hairline. The probe should be applied gently, as too much pressure can compromise vascular imaging. Color Doppler mode should be used rather than power Doppler. The color box should be aligned with the vessel direction, which can vary. Care should be taken to image the center of the vessel and to use correct color gain and pulse repetition frequency (PRF) settings. This will avoid false-positive findings (color gain too low: echo-free rim around faint color) and false-negative findings (color gain too high: color obscures edematous wall swelling).

In vasculitis, the vessel wall appears thickened and hypoechoic. Stenosis may be present, characterized by aliasing or at least a twofold increase in peak flow velocity. Occlusions are less common than stenoses. If uncertainty exists, the artery can be lightly compressed to display inflammatory vessel wall thickening without color artifacts. Inflammatory wall changes in relatively small arteries such as the temporal artery, facial artery, and occipital artery will generally resolve in 2 to 3 weeks. Ultrasound diagnosis in some patients becomes more difficult by the third day of corticosteroid therapy (Table 8.2).

Table 8.2 Recommended pulse repetition frequency (PRF) for various arteries that are significant in vasculitis imaging

Plenty of coupling gel should be used for superficial vessels to avoid pressure artifacts. To improve the coupling path and perhaps relieve cold-induced vasospasms, warm water-bath immersion is recommended in patients with suspected digital artery occlusions.

Fibromuscular dysplasia (FMD) may also show multifocal involvement and requires the investigation of other abdominal vessels plus the extracranial carotid and vertebral arteries in patients with detectable renal artery stenosis.²²

Compression syndromes are of special interest among the nonatherosclerotic vascular occlusions. Imaging results depend greatly on the creativity of the examiner and on active cooperation from the patient. Although findings are usually normal when the patient is scanned in a neutral position, certain provocative maneuvers can reproduce the stenosis or occlusion caused by pressure from adjacent ligaments, bones, tendons, or muscles. The most common compression syndromes include thoracic outlet syndrome (TOS) and popliteal entrapment syndrome.^{7 , 21 , 42} The provocative maneuvers most often used to elicit arterial or venous compression are illustrated in Fig. 8.2 and Fig. 8.3.³⁶ All four maneuvers suppress the radial pulse while the subclavian artery is auscultated. If significant compression is suspected, the stenosis or occlusion is documented by CDS. It should be noted that the detection of stenosis in itself does not have pathologic significance. Provocative tests in the shoulder and knee region will produce significant luminal narrowing in over 50% of patients; thus, the findings can be classified as pathogenically significant only when correlated with the clinical presentation and in the presence of a vascular complication.

Primary vasculitis is classified by the size of the affected vessels, and four more categories have been added based on the 2012 revision of the Chapel-Hill nomenclature: variable-vessel vasculitis, single-organ vasculitis, vasculitis associated with systemic disease, and vasculitis associated with probable etiology (Table 8.3). The latter type corresponds to the older secondary vasculitides.

Table 8.3 Revised Chapel-Hill nomenclature (Based on Jennette et al¹⁵)

Large-vessel vasculitis affects arteries from 3 cm (aorta) to 0.7 mm (digital arteries) in diameter and having a wall structure composed of intima, media, and adventitia. Medium-vessel vasculitis occurs predominantly in the main visceral arteries and their branches, such as the superior mesenteric artery and the segmental branches of the renal arteries, usually presenting in the form of occlusions and occasionally as aneurysms. Like small-vessel vasculitis, there are rare cases in which medium-vessel vasculitis is accessible to ultrasound imaging but only if there is associated involvement of large arteries.²⁶

Giant-Cell Arteritis (GCA)

Age 50 years or older, when combined with degenerative vessel-wall changes and immune-system changes, is considered the principal risk factor for the development of GCA.²⁵ Bacterial or viral triggers can activate toll-like receptors (TLRs) on dendritic cells in the vessel wall, leading to a breakdown of immune tolerance. They can initiate and sustain a granulomatous infiltration by the activation of CD4* T-cells and, based on recent discoveries, a shift of B-cell homeostasis. The varying profiles of TLRs in the vessels explain the predilection of GCA for specific vascular segments.

Approximately 50% of all GCA patients have symptoms of polymyalgia rheumatica (PMR), which is characterized by bilateral shoulder and pelvic-girdle pain of sudden onset, malaise, and marked inflammatory signs (erythrocyte sedimentation rate [ESR], C-reactive protein [CRP]). Ultrasound in patients with PMR shows inflammatory changes in the shoulder region (subdeltoid bursitis, long biceps tenosynovitis, glenohumeral joint effusion) and hip region (hip joint effusion, trochanteric bursitis). New classification criteria for PMR have recently adopted an algorithm that includes ultrasound imaging of the shoulder and hip joints (Table 8.4). In approximately 20% of patients with PMR and no symptoms of temporal arteritis, a thorough angiologic examination that includes duplex scanning of the temporal arteries and the proximal upper and lower extremity arteries will detect an underlying vasculitis.^{19 ,​ 38}

Table 8.4 EULAR/ACR criteria for giant-cell arteritis (GCA) and polymyalgia rheumatica (PMR)

The diagnosis of temporal arteritis is traditionally based on clinical findings and biopsy, despite a biopsy sensitivity of only 80% to 90%, or even 39% in a current study.³⁹ If patients with large-vessel GCA are included, the sensitivity falls to 50%.¹⁴ This underscores the value of CDS, which in one meta-analysis achieved a sensitivity of 87% and specificity of 96% compared with clinical criteria.¹⁶ The main criterion is hypoechoic edematous swelling of the vessel wall of the STA, as illustrated in Fig. 8.4. This change can lead to stenoses and occlusions and is no longer detectable in most patients after 2 to 3 weeks of corticosteroid therapy.²⁶

According to receiver operating characteristic (ROC) curve analysis, an intima-media thickness of ≥ 0.7 mm by compression sonography of the temporal arteries showed the best diagnostic accuracy for the diagnosis of cranial GCA with a sensitivity of 85% and a specificity of 95%, respectively.³⁸

According to Stammler et al,³¹ biopsy is unnecessary in cases with a low or high clinical probability and normal or typical CDS findings; consequently, only one-third of patients with suspected temporal arteritis require biopsy. Today, fast-track protocols have been established for the diagnosis of temporal arteritis. At experienced centers, biopsy is necessary only in a few equivocal cases.²⁶

Rare atherosclerotic transformation of the STA has also been reported by duplex sonography, as illustrated in Fig. 8.5. Echogenic plaques in the artery wall will generally distinguish the condition from vasculitis, so it is rarely necessary to obtain a biopsy.

In up to 45% of cases, temporal artery involvement is accompanied by typical vasculitic changes in the upper extremity arteries, which are asymptomatic in almost half of the cases and would go undetected without the above recommendation for a duplex vascular survey.^{10 ,​ 27}

Large-Vessel Giant Cell Arteritis

Patients with large-vessel GCA tend to be younger than patients with classic temporal arteritis (66 vs. 72 years) and there is usually a longer delay in diagnosis (7 vs. 2 months). While temporal arteritis is detectable sonographically or histologically in only 60% of cases, patients with large-vessel GCA typically show involvement of the axillary artery, proximal brachial artery, and less commonly the subclavian artery, usually on both sides.^{9 ,​ 27}

Typical sonographic changes consist of long, concentric, homogeneous, iso- to hypoechoic areas of segmental vessel wall thickening, which is also called the macaroni sign (Fig. 8.6). In most cases the vessel wall is initially less edematous than in temporal arteritis, changes much more slowly with treatment, and shows increased echogenicity.

Large-vessel GCA also differs from temporal arteritis in its therapeutic response. Only 30% of treated patients show a normalization of findings by 50 months. Regression or no change occurs in 60%, and progression in 10%.^{4 ,​ 26}

Hypoechoic occlusions of the axillary or brachial artery should be attributed to vasculitis until an equally plausible diagnosis has been found. A maximum intima-media thickness of ≥ 1.2 mm of both axillary arteries in a single patient had a sensitivity and specificity of 81.3% and 96.1% for diagnosis of extracranial GCA.⁴³ Although less common, GCA should always be considered as a potential cause of long-segment, hypoechoic stenosis of the femoral artery, especially in cases with rapid progression (Fig. 8.7).

Two conditions that merit special attention are idiopathic aortitis and retroperitoneal fibrosis (p. 342), possibly a local variant of GCA or Takayasu’s arteritis. Unexplained fever, back pain, abdominal or flank pain, and weight loss will lead the patient to seek medical attention. Cases with aortitis will exhibit a homogeneous hypoechoic mass predominantly extending anterolaterally to the infrarenal aorta like those shown in Fig. 8.8. Unlike the well-defined inflammatory wall changes of idiopathic aortitis, the changes in retroperitoneal fibrosis often go undetected by ultrasound until complications arise such as iliofemoral deep vein thrombosis, hydronephrosis, or iliac artery stenosis.

Although TA and GCA have comparable histologies and both may show aortic involvement, TA affects younger patients (≤ 40 years) and is distinguished by a poorer therapeutic response rate and a very protracted course. Table 8.5 describes the frequency distribution of the affected vessels in TA.

Table 8.5 Frequency distribution of affected vessels in Takayasu’s Arteritis (TA) (Based on Kerr¹⁷)

Through advances in imaging technology, pulmonary arterial involvement, usually mild, can be found in up to 70% of patients.³⁵ The diagnostic criteria defined by the American College of Rheumatology in 1990 describe the late stage of the disease in which symptomatic vascular stenoses or occlusions have already developed. They do not apply to the early inflammatory or “pre-pulseless” phase. This explains the very protracted course of the disease, especially in children, until the disease eventually presents clinically with severe complications. It is not uncommon for patients with early disease to have systemic manifestations in addition to pain along the course of the carotid or axillary artery (Fig. 8.9). Having the patient swallow during ultrasound scanning will sometimes help to display the uniformly thickened vessel wall of the common carotid artery (CCA) by shifting structures along the plane between the adventitia and adjacent tissue (Fig. 8.9, Fig. 8.10). The most important sonographic indicator of active disease is progressive wall thickening over time or new wall thickening in a previously unaffected segment.^{1 , 38 , 28}

Intracerebral Vasculitides

The intracerebral vessels occupy a special place among the vasculitides (Fig. 8.11). In a long-term observational study by the Mayo Clinic over a 17-year period, the great majority of cases were classified as isolated central nervous system (CNS) vasculitis (Table 8.6). Isolated CNS vasculitis may present as small-vessel disease or as uni- or bilateral focal cerebral angiopathy. The latter is associated with potentially impressive duplex ultrasound findings. Because a progression of findings has been described over a period of 1 to 2 years, regular long-term follow-ups should be maintained.⁸

Table 8.6 Central nervous system vasculitis

The findings on this topic are drawn from our own studies in patients with suspected large-vessel vasculitis due to various causes, as this question has not yet been addressed in the literature. The rationale for using contrast-enhanced ultrasound (CEUS) for large-vessel vasculitis is the assumption that active vascular inflammation positively correlates with the degree of neovascularization of the thickened arterial wall. Contrast-enhanced scans consistently show early contrast development in the thickened adventitia of vascular segments that already appeared abnormal in the B-mode image. The wall enhancement occurs a few seconds after enhancement of the perfused vessel lumen and is considerably earlier and more intense than in adjacent connective tissue (Fig. 8.12, Video 8.1). This enhancement may fade significantly after just a few days’ corticosteroid therapy, weeks or months before the B-mode image shows regression of the homogeneous wall thickening (Fig. 8.13, Video 8.2). Interestingly, increased enhancement is seen even in cases where positron emission tomography–computed tomography (PET-CT) shows no measurable uptake in patients who are still symptomatic (Fig. 8.14). Carotidynia is a rare condition that presents with painful swelling of the neck and an inflammation, usually of the carotid bulb, that are reversible over a period of weeks. The two-layered structure of the thickened vessel wall found in the B-mode image corresponds to an intense enhancement of the adventitia, detectable for a period of days, and a nonenhancing deeper wall layer on CEUS. As clinical complaints regress, the enhancement fades (Fig. 8.15, Fig. 8.16). Important differential diagnoses include common carotid involvement by GCA or TA, carotid artery dissection, and carotid glomus tumor or hypoechoic atherosclerotic plaque, the latter without pain.

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