Rheumatology International (2019) 39:169–185 Rheumatology https://doi.org/10.1007/s00296-018-4157-3 INTERNATIONAL

REVIEW

Diagnosis and differential diagnosis of large-vessel vasculitides

Gokhan Keser1 · Kenan Aksu1

Received: 16 July 2018 / Accepted: 10 September 2018 / Published online: 17 September 2018 © Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract There are no universally accepted diagnostic criteria for large-vessel vasculitides (LVV), including giant cell (GCA) and Takayasu arteritis (TAK). Currently, available classification criteria cannot be used for the diagnosis of GCA and TAK. Early diagnosis of these two diseases is quite challenging in clinical practice and may be accomplished only by combining the patient symptoms, physical examination findings, blood test results, imaging findings, and biopsy results, if available. Awareness of red flags which lead the clinician to investigate TAK in a young patient with persistent systemic is helpful for the early diagnosis. It should be noted that clinical presentation may be highly variable in a subgroup of GCA patients with predominant large-vessel involvement (LVI) and without prominent cranial symptoms. Imaging modalities are especially helpful for the diagnosis of this subgroup. Differential diagnosis between older patients with TAK and this subgroup of GCA patients presenting with LVI may be difficult. Various pathologies may mimic LVV either by causing systemic inflammation and constitutional symptoms, or by causing lumen narrowing with or without formation in the aorta and its branches. Differential diagnosis of is crucial. Infectious aortitis including mycotic due to septicemia or endocarditis, as well as causes such as syphilis and mycobacterial infections should always be excluded. On the other hand, the presence of non-infectious aortitis is not unique for TAK and GCA. It should be noted that aorti- tis, other large-vessel involvement or both, may occasionally be seen in various other autoimmune pathologies including ANCA-positive vasculitides, Behçet’s disease, ankylosing spondylitis, sarcoidosis, and Sjögren’s syndrome. Besides, aortitis may be idiopathic and isolated. should always be considered in the differential diagnosis of LVV. Other pathologies which may mimic LVV include, but not limited to, congenital causes of aortic coarctation and middle aortic syndrome, immunoglobulin G4-related disease, and hereditary disorders of connective tissue such as Marfan syndrome and Ehler–Danlos syndrome.

Keywords · Large vessel · · Temporal arteritis · Takayasu · Diagnosis · Differential diagnosis · Criteria · Mimickers · Aortitis

Introduction muscle and joint aches, accompanied by variable involve- ment of many organs and systems. The current trend is to Vasculitides include a heterogeneous group of diseases, classify vasculitides based upon the size of the involved ves- characterized mainly by inflammation of blood vessels sels. However, the presence of anti-neutrophilic cytoplas- which may result in damage and necrosis of the vessel mic antibodies (ANCA), being isolated in a single organ, or wall. Patients with vasculitides typically present with con- being associated with systemic disease, or having a probable stitutional symptoms such as fever, fatigue, weakness, and etiology, are also considered within supportive parameters for classification [1]. Large vessels include aorta, its major branches, and * Gokhan Keser extremity and the analogous according to [email protected] the 2012 International Chapel Hill Consensus Conference Kenan Aksu (CHCC) nomenclature of vasculitides. Large-vessel vascu- [email protected] litis (LVV) is defined as a vasculitis that affects large arter- 1 Division of Rheumatology, Department of Internal ies more often than other vasculitides do [1]. In the present Medicine, Ege University School of Medicine, Bornova, review, we concentrate on the diagnosis and differential Izmir, Turkey

Vol.:(0123456789)1 3 170 Rheumatology International (2019) 39:169–185 diagnosis of large LVV, which include giant cell arteritis revisions: One current suggestion for revising the ACR cri- (GCA) and Takayasu arteritis (TAK). teria is to avoid TAB for the diagnosis of GCA [9]. There is also a growing tendency to use CDU for diagnosing GCA [8]. There is an ongoing multi-national observational study Methods called as DCVAS (diagnostic and classification criteria for vasculitis study), designed to develop and validate diagnos- We conducted a comprehensive review of the literature for tic criteria for six different primary systemic vasculitides, English articles published between 1980 and 2018, using including GCA and TAK [10]. PubMed, Scopus, and Web of Science as databases. The keywords of “vasculitis”, “large vessel”, “giant cell arte- The contribution of medical history, physical ritis”, “temporal arteritis”, and “Takayasu” “aortitis” were examination, and laboratory tests to the diagnosis searched in combination with the keywords of “diagnosis”, of large‑vessel vasculitides “differential diagnosis”, “criteria”, and “mimickers”. We also manually searched the references of the selected arti- Symptoms suggestive of TAK and GCA may change depend- cles for any relevant reference that we might have missed. ing upon the time from the disease onset and the extent of organ/system involvement. Most of the initial symptoms The general approach to the concepts are non-specific, mostly reflecting vague constitutional of “diagnostic” and “classification” criteria symptoms caused by systemic inflammation, which may increase as the disease progresses. Transmural, granuloma- Currently, there are no universally accepted diagnostic cri- tous, inflammatory process within the arterial wall leads to teria, neither for LVV nor other systemic vasculitides and intimal hyperplasia and vessel occlusion, thereby causing other autoimmune diseases such as systemic lupus erythe- ischemia and damage of the affected organs. Destruction of matosus (SLE). Diagnostic and classification criteria are not the large elastic arteries may lead to progressive dilatation, the same. Ideal diagnostic criteria must cover the different aneurysm formation, and potentially fatal vascular events and heterogenic features of a disease, including those with such as or rupture [11, 12]. unusual presentations. Naturally, such an approach will Palpation of arterial pulses, measure- increase the sensitivity, at the expense of lowering specific- ments of all extremities, and cardiac and neck auscultation ity. However, classification criteria are standardized defi- for detecting bruits are crucial parts of the physical exam- nitions aiming to cover familiar and homogenous clinical ination. There are no unique, highly sensitive or specific scenarios for a particular disease. Therefore, classification diagnostic tests. Elevated erythrocyte sedimentation rate criteria do not aim to capture all patients, and may easily (ESR), and serum C-reactive protein (CRP), leukocytosis miss those patients with atypical features, resulting in lower with granulocytosis, thrombocytosis, and normochromic/ sensitivity, but higher specificity. Therefore, classification normocytic anemia reflect the acute phase response [13, 14]. criteria are not appropriate for the diagnosis of LVV in Leukopenia and thrombocytopenia are not expected in LVV routine clinical care; instead, they serve to classify already except in case of immunosuppressive agent usage. As the diagnosed vasculitis patients and include them in clinical systemic inflammation persists, hypoalbuminemia and poly- studies [2]. clonal hyperglobulinemia may accompany [13]. However, Ishikawa performed the first attempt to develop diagnos- the absence of an elevated acute phase response by itself is tic criteria for TAK in 1988, and these criteria were later not sufficient to exclude the diagnosis of LVV [15]. Given modified by Sharma et al. in 1995 (Table 1) [3–5]. The tra- that serum amyloid A (S-AA) protein increases rapidly even ditional classification criteria of the American College of in the presence of minimal systemic inflammation, it may Rheumatology (ACR) for TAK and GCA were defined in be useful to measure S-AA levels in the presence of normal 1990 (Table 1) [6, 7]. Considerable progress occurred in ESR and CRP levels [16]. diagnostic imaging modalities for both diseases, including Given that vascular wall and systemic inflammation may magnetic resonance angiography (MRA), computerized be discordant especially in TAK, ESR and CRP levels may tomography angiography (CTA), color Doppler ultrasonog- be normal despite ongoing disease activity [17]. Inflam- raphy (CDU), and positron emission tomography (PET) with matory molecules that are produced at sites of vascular 18F-fluorodeoxyglucose (18F-FDG-PET), since then. Arte- inflammation may be expected to reflect the degree of cur- riogram included in the 1990 ACR criteria for TAK is no rent vascular wall inflammation better. Pentraxin-3 (PTX- longer the gold standard for the diagnosis of TAK [8]. Simi- 3) is involved in the maintenance of vascular homeostasis, larly, temporal biopsy (TAB) included in the 1990 and measuring plasma levels of PTX-3 was suggested as a ACR criteria for GCA is no longer the only tool for diagnos- more reliable biomarker to reflect current vascular disease ing GCA [8]. Thus, these criteria certainly need appropriate activity in TAK [18]. Although PTX-3 certainly had some

1 3 Rheumatology International (2019) 39:169–185 171 - 50 years ≥ to palpation or decreased pulsation, palpation or decreased to to unrelated of cervical arteries method characterized by vasculitis men showing of mononuclear cell infil - predominance or granulomatoustration inflammation, with multinucleated giant cells usually at disease onset Age New headache New artery abnormality:Temporal tenderness the Westergren ESR ≥ 50 mm/h by Abnormal artery Arterial biopsy: speci - – At least three of the five criteria three of the least five At 93.5% 91.2% Five criteriaFive American Clas - of Rheumatology College (1990) [ 7 ] sification Criteriafor GCA tolic pressure between two limbs two between pressure tolic or occlusion of the aorta, its primary arteries- or large in thebranches, proxi extremities mal upper or lower – At least three of the least six criteriaAt 90.5% 97.8% Six criteria American of Rheumatology College TAK (1990) Classification Criteriafor [ 6 ] Age of onset before 40 years before of onset Age Extremity artery brachial Decreased pulse - of more Difference than 10 mmHg sys arteries subclavian or the aortaBruit over of narrowing Angiographic evidence ria, OR removed criterion as major accepted TAK” lesions in than 30 years in patients younger as a minor the absence of risk factors criterion Acceptance of aorto-iliacAcceptance involvement Two major criteria, major OR Two criterionA major minor crite - plus two minor criteriaFour 92.5% 95.0% Three major and ten minor criteria major Three Sharma modification of Ishikawa’s diag - Sharma modification of Ishikawa’s (1995) [ 5 ] criteria TAK nostic for Obligatory criterion ≤ 40 years) (age “Characteristic of Other modifications in the definition of of age Removal of the absence of aorto-iliacExclusion Inclusion of coronary artery lesions at the age ≤ 40 years, for at for ≤ 40 years, at the age a criteria, OR criteria, OR a requisite of defined characteristic signs and of defined ­ symptoms and nine minor criteria least 1 month least dence of right and left mid subclavian artery lesions common or bilateral ESR, unilateral arterycarotid tenderness, hypertension, aortic and angiographic regurgitation, of pulmonary leftevidence artery, mid distal brachiocephalic common carotid, trunk, descending thoracic and abdomi - nal aorta lesions Obligatory criterion major plus two criterion minor A major two plus at least minor criteria four least At 84% 100% Absence of aorto-iliac involvement was was of aorto-iliacAbsence involvement The obligatory criterion: occurrence Ishikawa diagnostic criteria for TAK criteria TAK diagnostic for Ishikawa (1988) [ 4 ] An obligatory criterion, major plus two Two major criteria: major - angiographic evi Two Nine minor criteria: included high Summary of the diagnostic and classification criteria for Takayasu arteritis (TAK) and giant cell arteritis arteritis (GCA) Takayasu (TAK) Summary of theand classification criteriafor diagnostic Defined characteristic signs and symptoms of TAK: absence of pulses, differences in pulses TAK: absence of pulses, differences the arms, unobtainable differences pressure significant blood in thepressure, blood characteristic of arms, easy signs and symptoms Defined

limb fatigability or pain, unexplained fever or high ESR (≥ 20 mm/h; Westergren) or both, neck pain, transient amaurosis or blurred amaurosis transient or palpitations pain, hyper both, or or dyspnea or syncope, vision or both, neck ESR (≥ 20 mm/h;or high Westergren) fever pain, unexplained or limb fatigability tension or aortic regurgitation Required criteriaRequired Sensitivity Specificity Special note 1 Table ESR erythrocyte sedimentation rate a Details of criteria Number of criteriaNumber

1 3 172 Rheumatology International (2019) 39:169–185 advantages compared to CRP, and some studies reported CTA, or in selected cases 18F-FDG-PET-CT, for establish- promising results, unfortunately, PTX-3 could not solve ing the diagnosis of TAK. the dilemma of effectively detecting ongoing vascular wall Recently, PET/CT was reported to be valuable in the inflammation in TAK [19–21]. assessment of local inflammatory and vascular remodeling events independent from systemic inflammation in TAK. Role of imaging modalities for clinical diagnosis PET/CT was also reported to detect even the lesions where of large‑vessel vasculitides the arterial wall was less than 4 mm [40]. The authors suggested that PET/CT might serve as a complementary Imaging modalities are essential for the diagnosis of modality in addition to the traditional inflammatory mark- patients with LVV [8, 22–25]. Advantages and disadvan- ers for the assessment of current disease activity. Inter- tages of imaging methods including conventional angiog- estingly, there are also attempts for combining functional raphy [23], MRA [26–30], CTA [26, 31, 32], CDU [25, PET data with morphological data derived from magnetic 33–35], and 18F-FDG-PET-CT [36–40] were given in resonance imaging (MRI). Hybrid PET/MRI offers lower Table 2. In summary, the conventional angiography is no radiation exposure compared to PET/CT, which may be an longer considered as the gold standard for the diagnosis advantage for the imaging of LVV [40, 41]. of TAK. Currently, many physicians prefer to use MRA or

Table 2 Comparison of the imaging methods for the diagnosis of large-vessel vasculitides Advantages Disadvantages

Conventional angiography [22–25] Assessing the extent and localization of vascu- Visualizing only the lumen of the vessel, lar involvement without giving any information about the Detecting , occlusions, and aneurysms vessel wall in large and medium-sized arteries Missing minor, non-occlusive vascular lesions Lack of adequate resolution for small vessels Being an invasive method Causing radiation and contrast media exposure Computerized tomography angiography (CTA) Evaluation of aorta and its primary branches Unable to visualize relatively small vessels [22–26, 31, 32] Excellent anatomical characterization of struc- Less resolution than CDU tural changes Causing radiation and contrast media exposure Differentiating vascular and perivascular structures Detecting calcifications Shorter scanning time Magnetic resonance angiography (MRA) Evaluation of aorta and its primary branches Overestimation of vascular occlusions [22–24, 26–30] Excellent anatomical characterization of struc- Inability to visualize small branch vessels and tural changes vascular calcifications Detecting vessel wall thickening, edema and More expensive contrast enhancement Longer scanning time No risk of radiation exposure Less resolution than CDU Color Doppler ultrasonography (CDU) [25, Evaluation of temporal, carotid, axillary, and Diagnostic accuracy varies depending on the 33–35] femoral arteries skill and experience of the operator Visualizing luminal changes, stenosis and May miss cases with early disease having aneurysms patchy mural inflammation without transmu- Detecting the characteristic, homogeneously ral disease and associated tissue edema thickened vessel wall, mural inflammation Fails to depict the thoracic aorta unless per- and edema formed as a transesophageal examination Providing better resolution than MRA and CTA​ No risk of radiation exposure Cheaper Positron emission tomography with Combining the functional information from Vascular uptake of 18F-FDG not specific for 18F-fluorodeoxyglucose (18F-FDG-PET) PET and anatomical information from CT vasculitis [36–40] Most sensitive imaging method for early vessel Discrimination between atherosclerotic and inflammation vasculitic lesions may be challenging Detecting early vascular inflammation and its No information for vessel wall structure and location in the aorta and its branches luminal flow High radiation exposure

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Role of tissue biopsy for diagnosis of large‑vessel 1990 criteria for TAK was the limitation of the age to less vasculitides than 40 years, which led to modification of Ishikawa’s crite- ria by Sharma et al. in 1996 [5]. They removed the obliga- Obtaining tissue biopsy and showing histopathological fea- tory criterion (age ≤ 40 years) and accepted the “charac- tures of vessel wall inflammation are critical to confirm the teristic signs and symptoms of TAK” as a major criterion. diagnosis of LVV. However, in clinical practice, histopatho- Ishikawa diagnostic criteria, Sharma modification of these logical diagnosis using temporal artery biopsy (TAB) may criteria, and ACR 1990 classification criteria for TAK are only be possible in GCA, which is discussed in the following summarized in Table 1. paragraphs. ACR 1990 criteria generally cover the cases with TAK in the late stages, where it is not difficult to make the diagnosis. ACR 1990 criteria were also criticized for the selection of Diagnosis of Takayasu arteritis the control group used, which included patients mainly with small-vessel vasculitis, rather than those with atherosclerotic Definition of TAK or congenital aortic diseases [3]. TAK may also be seen in childhood, and recently, clas- TAK is a frequently granulomatous vasculitis, predomi- sification criteria for childhood TAK were proposed by the nantly affecting the aorta and its major branches. Age of European League Against Rheumatism (EULAR), the Pedi- onset is usually less than 50 years [1]. atric Rheumatology European Society (PRES), and by the Pediatric Rheumatology International Trials Organization Clinical features of TAK (PRINTO) for patients younger than 18 years. These criteria also aimed to include these patients in epidemiologic studies TAK presents with different symptoms and clinical findings, and clinical trials (Table 3) [46]. depending upon the duration and phase of the disease. The first phase is characterized by non-specific constitutional Angiographic classifications and heterogeneity inflammatory symptoms, including fever of unknown origin. of TAK The second phase is characterized by vascular inflamma- tion. Involvement of carotid arteries may cause carotidynia Initial clinical findings of TAK may be different and het- and neck pain. Similarly, mural inflammation in thoracic erogeneous based upon the location and extent of vessel aorta may cause dorsal pain. In the late phase of the dis- involvement. For this reason, there have been attempts to ease, severe narrowing or occlusions may occur mainly in classify patients with TAK according to involved vessels, the proximal parts of the arterial branches originating from based upon angiographic findings. Both Sheikhzadeh et al. arcus aorta. Decreased or absent upper extremity pulses, [47] and Nasu [48] reported angiographic classifications for with or without discrepant measurements of arterial blood TAK, in 1982. However, Numano’s angiographic classifica- pressure between upper extremities, arterial bruits, and inter- tion for TAK is currently the most widely used classification mittent extremity claudication are among typical features [49]. Summary and comparison of these three angiographic of late-stage TAK. Severe hypertension may also occur in classifications are given in Table 4. TAK; it may be caused by atypical coarctation of the aorta, loss of vascular compliance, aortic valve regurgitation due Trying to make diagnosis of TAK earlier to aortitis, or [12, 42–44]. The occurrence of new and severe ischemic lesions is The early diagnosis of TAK is the real goal, which is difficult most common in TAK, although ischemic vascular manifes- to establish. For the early diagnosis, the clinician should tations including transient ischemic attack and stroke may consider the possibility of this disease in suspected cases. occur in almost all types of vasculitides [45]. There are red flags which may notify the clinician to investi- gate TAK in a young patient with persistent systemic inflam- Diagnostic and classification criteria for TAK mation (Table 5) [50]. Heterogeneity of TAK should also be kept in mind for the Ishikawa diagnostic criteria for TAK were published in 1988 early diagnosis. Genetic and ethnic factors may affect the [4]. Ishikawa defined “characteristic signs and symptoms primary location of vessel involvement. For example, vas- for TAK”, and the occurrence of those signs and symp- cular lesions tend to occur primarily in the ascending aorta, toms starting before 40 years of age for at least 1 month aortic arch, or its branches, and extend into the abdominal was accepted as an obligatory criterion. ACR classification aorta in Japanese patients with TAK. On the other hand, criteria for TAK were published 2 years later than Ishikawa abdominal aorta including renal arteries and thoracic aorta criteria [6]. The main criticism for Ishikawa 1988 and ACR are primarily involved in Indian patients [49]. Type V

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Table 3 EULAR/PRINTO/ Criterion Definition PRES criteria for childhood Takayasu arteritis [46] Angiographic abnormality (man- Angiography (conventional, computed tomography, or magnetic reso- datory criterion) nance imaging) of the aorta or its main branches and pulmonary arter- ies showing aneurysm/dilatation, narrowing, occlusion or thickened arterial wall not due to , or similar causes; changes usually focal or segmental Pulse deficit or claudication Lost/decreased/unequal peripheral artery pulse(s) Claudication: focal muscle pain induced by physical activity Blood pressure (BP) discrepancy Discrepancy of four limb systolic BP > 10 mmHg difference in any limb Bruits Audible murmurs or palpable thrills over large arteries Hypertension Systolic/diastolic BP greater than 95th percentile for height Acute phase reactants Erythrocyte sedimentation rate > 20 mm per first hour or C-reactive protein any value above normal (according to local laboratory)

Takayasu arteritis is classified when the mandatory criterion is present plus any other criteria involvement of Numano’s angiographic classification is most It is not difficult to diagnose GCA in the presence of a common in Indian patients with TAK (Table 4) [49]. For this new-onset headache and temporal artery abnormalities, asso- reason, renovascular hypertension together with persistent ciated with a systemic inflammatory syndrome and proximal systemic inflammation may lead the clinician to the possible muscle pain in an elderly patient. Likewise, acute ocular early diagnosis of TAK in Indian patients [51]. symptoms such as impaired vision, diplopia, and amaurosis In summary, the first step for the early diagnosis is a high fugax should always remind the clinician the possibility of index of suspicion in selected cases, and the second step is to GCA. Such ophthalmological emergencies generally result confirm the diagnosis of TAK by appropriate imaging meth- from anterior ischemic optic neuropathy due to occlusion of ods, as summarized in Table 2. Our approach is to use MRA the posterior ciliary or ophthalmic arteries. Similarly, clau- for confirming the diagnosis of TAK. We tend to use CTA dication of the jaw or tongue or both, and upper respiratory when MRA is not available for technical reasons. Although symptoms such as a non-productive cough, sore throat, or FDG-PET-CT scan has gained considerable acceptability, hoarseness may direct the clinician to consider the possibil- we use this imaging method for the diagnosis of TAK in ity of GCA [52]. selected difficult cases. Given that MRA has no radioactiv- PMR is characterized by inflammatory pain and stiffness ity and is very useful both to assess wall thickening/edema affecting the neck, shoulders, hips, and proximal extremities, and to detect the presence of aneurysms/thrombus, we and with frequent occurrence of subdeltoid bursitis, biceps teno- many authors recommend MRA in patients with TAK for synovitis, glenohumeral synovitis, or trochanteric bursitis. close follow-up. Symptoms are usually bilateral and more pronounced in the morning or after periods of inactivity, and there is severe systemic inflammation. PMR shares many epidemiologic Diagnosis of giant cell arteritis (GCA) and pathogenic features with GCA and may accompany GCA with a reported wide range of frequency from 17 to Definition of GCA​ 66% [52]. Different subgroups of GCA​ GCA, also known as temporal arteritis, is an LVV, often granulomatous, and usually affecting the aorta and its major • Two different subgroups of GCA were reported con- branches. GCA has a predilection for the branches of the cerning the severity of systemic inflammation. The first carotid and vertebral arteries, especially the temporal artery subgroup is mainly characterized by severe systemic [1]. inflammation, while, in the second subgroup, there is less inflammation, but a prominent vaso-occlusive pro- Clinical features of GCA​ cess. Acute vision loss is generally seen in the second subgroup [17, 53]. It is usually seen in patients older than 50 years and often • There is also a subgroup of GCA patients presenting with associated with polymyalgia rheumatica (PMR). Extensive large-vessel involvement (LVI) without cranial arteritis systemic inflammation, accompanying vascular inflamma- [54]. The clinical presentation may be highly variable tion is present in the majority of the cases [1]. in this subgroup. Thoracic aorta and extremity arter-

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Table 5 Red flags to investigate Takayasu arteritis in a young Carotidynia patient with persistent systemic Hypertension inflammation [50] Angina pectoris Vertigo and syncope Extremity claudication Absent/weak peripheral pulses Discrepant blood pressure in the upper limbs (> 10 mmHg) Arterial bruits Aortic regurgitation

ies may be involved in those patients. Although lower extremities may also be affected, upper extremities are affected more often, which may cause symptoms of vas- cular insufficiency such as claudication. This subgroup of GCA patients with LVI was reported to be younger, more

arteries indicated as C (+) or P (+), respectively likely to be women and to have less cranial symptoms Numano 1996 [ 49 ] Numano Type I: branches of aortic I: branches arch Type IIa: ascending aorta, aortic and its branches Type arch IIa IIb: thoracic descending aorta plus Type Type III: thoracic descending aorta, abdominal aortaType and/or renal abdominal aorta arteries and/or renal IV: Type IV IIb and Type the combination of Type V: Type of coronary or pulmonary arteries should be involvement Note: and PMR. More importantly, GCA patients with LVI had an increased risk of aortic dilation [55]. Therefore, the presence of aortic insufficiency murmur in cardiac aus- cultation may implicate the possibility of this subgroup of GCA in a suspected patient. • Recently, it has been suggested that there are two more different subgroups of GCA with regard to type of sub- clavian arterial involvement: The first subgroup, being more common, is characterized by wall thickening, ste- nosis, and occlusion of subclavian arteries, while dila- tion of subclavian arteries characterizes the second less common subgroup. Interestingly, aortic dilation has been reported to be more common and aortic wall thickening less common in the second subgroup. The authors recom- mend that patients with GCA having subclavian artery dilation should be evaluated and monitored carefully for Nasu 1982 [ 48 ] Nasu Type I: primarily branches of aortic I: primarily branches arch Type II: aortic and its branches arch Type III: abdominal aorta arteries renal and particularly Type whole aorta and its branches IV: Type possible aortic dilation and aneurysm [56].

Classification criteria for GCA​

ACR 1990 criteria for the classification of GCA (Table 1) [7] concentrate on occurrence in older patients, new-onset typical headache, prominent constitutional symptoms, abnormalities of temporal artery in physical examination, and typical histological findings obtained from TAB. Ocular symptoms and claudication of the jaw and tongue are not included within these criteria. More importantly, the sub- group of GCA with LVI is not covered in these criteria.

Histologic diagnosis of GCA​

TAB is still vital for diagnosing GCA, especially in patients Proposed angiographic classifications for Takayasu arteritisTakayasu for angiographicProposed classifications with symptoms of cranial arteritis. The artery specimen should be at least 1 cm in length to avoid missing inflamma- or without pulmonary or coronary artery involvement 4 Table Sheikhzadeh 1982 [ 47 ] Type I: aortic type (cervicobrachial type) arch Type II: thoracoabdominal type Type III: peripheral type; iliac arteriesType types with of the or more previous combination of two IV: Type tory segments of the vessel. Supporting this view, the rate

1 3 176 Rheumatology International (2019) 39:169–185 of positive findings was only 25.7% in specimens less than 1 cm in length, while 74.3% in specimens ≥ 1 cm in length [57]. Whether TAB should be made unilateral or bilateral is controversial. Some authors recommend routine bilateral TAB for all patients, while others perform unilateral biopsy initially, and make a contralateral biopsy only if the initial biopsy is negative. We also prefer to perform unilateral TAB initially. Breuer et al. reported that performing bilateral TAB increased the diagnostic sensitivity of the procedure by up to 12.7%, compared to unilateral TAB [58]. However, the rate of discordant results in bilateral TAB was calculated as 5.9% in another study [59]. If the patient needs urgent corticosteroid (CS) treatment such as in the presence of an Fig. 1 Power Doppler ultrasound image of the right superficial tem- ophthalmic emergency, the treatment should not be delayed. poral artery of a 73-year-old woman delineates blood flow and con- Fortunately, TAB remains a valuable diagnostic procedure centric thickening of the vessel wall (“halo sign”). The thickness of the hypoechoic wall was measured as 0.5 mm all along its preauricu- even after several weeks of CS treatment. Nevertheless, lar segment approximately 10% of patients with the clinical diagnosis of GCA will have negative TAB [52]. TAB versus CDU of superficial temporal arteries for the diagnosis of GCA with cranial symptoms Diagnosis of GCA with cranial symptoms by imaging methods TABUL study is an excellent multicenter prospective study which compared CDU and TAB in the new cases of sus- Imaging of the superficial temporal arteries with CDU or pected GCA. A training program was given to sonographers MRA is an alternative method for the diagnosis of GCA to standardize the CDU assessment of temporal and axillary with cranial symptoms, and may be tried in selected cases arteries. Analysis of 381 patients who underwent both USG [8]. CDU may evaluate temporal, carotid, axillary, and femo- and TAB within 10 days of starting treatment for suspected ral arteries, by visualizing luminal changes, stenosis, and GCA showed that sensitivities of TAB and USG were 39% aneurysms. CDU may detect the characteristic, homogene- and 54%, respectively; while the specificities were 100% and ously thickened vessel wall and mural inflammation in the 81%, respectively [33]. presence of vasculitis. The hypoechoic area surrounding the lumen of the artery is thought to represent edema and vascu- Diagnosis of GCA with large‑vessel involvement lar inflammation of the arterial wall and called as ‘halo sign’ by imaging methods which may contribute to the diagnosis of GCA [25] (Fig. 1). Overall sensitivity and specificity of CDU for detecting In such cases presenting with LVI, without cranial arteritis, abnormalities such as halo sign, stenosis, or occlusion in appropriate imaging methods including MRA or CTA may GCA were 88% and 78%, respectively, as compared to TAB confirm the diagnosis of GCA. However, 18F-FDG-PET/CT [8, 25]. A recent study aimed to evaluate the intima-media scanning is generally the first option in selected cases, and thickness of temporal, facial, and axillary arteries involved may also be useful to exclude malignancy in the differential in GCA for determining cut-off values which may be helpful diagnosis of GCA. for diagnosis and follow-up of GCA. The authors reported that CDU could correctly distinguish vasculitic from normal Similarities and differences between Takayasu arteries in patients with suspected GCA [34]. arteritis and giant cell arteritis As discussed above, discontinuous and skip inflamma- tory changes in the temporal artery may cause false-negative Whether TAK and GCA represent a spectrum of the same biopsy results in nearly 13–44% of patients, mainly if the disease is an ongoing debate [60–63]. Despite similarities length of the biopsy specimen is too short. Therefore CDU- [64–66], there are also striking differences between GCA guided TAB might be expected to improve the sensitivity and TAK including major histocompatibility complex asso- for GCA diagnosis. However, in a recent study, CDU-guided ciations [67], localization of prominent vessel wall inflam- TAB did not result in improved sensitivity [35]. The authors mation [68], type of aortic involvement [69], and distribution reported that the probability of a positive TAB is high in the of the involved arteries [70]. Cytokine response patterns to presence of the halo sign on CDU, regardless of whether the CS treatment [61, 71–73], and clinical responses to anti- TAB is guided by CDU or not [35]. TNF treatment [74–76] and abatacept treatment [77, 78] are

1 3 Rheumatology International (2019) 39:169–185 177 also different. Similarities and differences between GCA and atherosclerotic plaque, aneurysm sac, or any other injury TAK are summarized in Table 6. Although the debate goes in any segment of the aortic wall may predispose to the on, we believe that GCA and TAK are different diseases. colonization of microorganisms [84–89]. Going into details of infectious aortitis is beyond the scope of this Differential diagnosis between TAK review. However, the message to the clinician is straight- and the subgroup of GCA with LVI forward: in the presence of aortitis, infectious causes should always be excluded using the standard microbio- Since typical cranial symptoms are rare in the subgroup logical diagnostic tests. of GCA with LVI, differential diagnosis with older TAK Non-infectious causes of aortitis should be considered patients may occasionally be difficult. Peripheral vascular after the exclusion of infectious aortitis. Although GCA and abnormalities on examination, lower extremity claudica- TAK are the most frequent causes of autoimmune aortitis, tion, fever, arthralgia/myalgia, and stroke/transient ischemic other systemic autoimmune diseases, such as SLE [90], attacks are more common in TAK, while upper extremity Sjögren’s syndrome [91], [92], ANCA- claudication occurs more often in GCA with LVI. The pres- associated vasculitides [93, 94], HLA-B27 associated spon- ence of aortic aneurysms is more likely in GCA with LVI, dyloarthropathies [95], psoriatic arthritis [96], sarcoidosis while aortic stenotic lesions occur more commonly in TAK. [97], Cogan’s syndrome [98], relapsing polychondritis [99], Aortic aneurysms occur mostly in the ascending thoracic inflammatory bowel diseases 91[ , 100, 101], Behçet’s dis- aorta in GCA [62, 63, 69]. ease [102], and IgG4-related disease [103], and possibly some other diseases may also cause occurrence of aortitis. Differential diagnosis between large‑vessel Aortitis may also occur in PMR patients without GCA. In vasculitides and mimickers the presence of atypical symptoms such as unexplained thigh pain, low back pain or lower limb pain, and an inadequate Various pathologies may mimic LVV either by causing response to low-to-medium doses of CS, associated aortitis systemic inflammation and constitutional symptoms or by should be suspected in PMR [91]. causing lumen narrowing or aneurysm formation in the aorta It should be noted that aortitis may occasionally be idi- and its branches. As a general rule, infectious and malignant opathic and may occur in isolation, with a prevalence rang- diseases should be considered in the differential diagnosis of ing between 4.3 and 8.4% [104, 105]. Histologically isolated elevated acute phase response, before making the diagnosis aortitis is virtually indistinguishable from GCA and TAK of LVV, especially of PMR. These pathologies may not only [106]. The risk factors for the development of isolated aor- mimic LVV, but may also cause secondary vasculitis with titis were reported as advanced age, history of connective a wide range of vasculitic symptoms [79, 80]. In selected tissue disease, diabetes mellitus, and heart valve pathology cases, 18F-FDG-PET/CT may be useful to exclude malig- [105]. nancy in the differential diagnosis of GCA, as well as to Differences between isolated aortitis and GCA-associated confirm the diagnosis of GCA with LVI. aortitis have recently been described by Talarico et al. [107]. Since aortitis is a critical component seen both in TAK Isolated aortitis is seen predominantly in male and younger and in the subgroup of GCA with LVI, any pathology caus- patients when compared to GCA. Aortic arch, and thoracic ing aortitis may confuse differential diagnosis. The early and abdominal aortas are involved, while aortic branches diagnosis of aortitis is of primary importance to prevent seem to be spared. Unfortunately, whether patients with iso- serious complications, such as aneurysmal rupture or aortic lated aortitis represent variants of GCA or TAK, or how they dissection. The term “aortitis” is, indeed, a histopathologi- will evolve in the future is indefinite [107]. cal term implicating inflammation of media and adventitia, After a differential diagnosis of aortitis is over, other accompanied with the classic appearance of “tree-barking” pathologies which may mimic LVV should also be consid- of the aortic intima [81]. However, in clinical practice, the ered. Among pathologies affecting aorta and its branches, diagnosis of aortitis is generally made based on imaging atherosclerosis is probably the most common mimicker, techniques such as FDG-PET/CT, MRA, or CTA [81–83]. especially in older patients. Association between inflam- Aortitis may be infectious or non-infectious. Among mation and atherosclerosis is well known, and vasculitic/ infectious agents, the most common pathogenic spe- atherosclerotic lesions may be present together even in cies involved are Salmonella, Staphylococcus aureus, young patients [108, 109]. Given that atherosclerosis is Streptococcus pneumonia, Mycobacterium tuberculosis, also an inflammatory process, atherosclerotic plaques may human immunodeficiency virus, and, even if now rare, show increased uptake of gadolinium contrast in MRA Treponema pallidum [83]. In most cases of infectious and increased FDG uptake in PET-CT imaging, resulting aortitis, the responsible microorganism may colonize the in further confusion in differential diagnosis [110]. How- aorta by entering via the vasa vasorum. The presence of ever, there are some clues which may help to differentiate

1 3 178 Rheumatology International (2019) 39:169–185 ment is not ​ in GCA suppressed easily are cytokines lary arteries tongue claudication, scalp tenderness,tongue and vision loss common inner layer ​ GCA - treat anti-TNF While abatacept is effective, Unlike Th1 cytokines, serum levels of Th17 serum Th1 cytokines, levels Unlike Older patients, especially Caucasian origin Older patients, especially MHC class II alleles Thoracic aneurysmalThoracic dilatation Symmetric subclavian with concomitant axil - Symmetric subclavian Cranial symptoms including headache, jaw or jaw including headache, symptoms Cranial Branches of the external carotid artery of the external carotid Branches more Vessel wall inflammation prominent in inflammation prominent the wall Vessel tive, abatacept is not tive, cytokines are easily suppressed in TAK suppressed easily are cytokines countries carotids, and also involvement of mesenteric and also involvement carotids, artery bruits, absent pulses and blood pressure discrepancies common TAK While anti-TNF treatment is generally effec - is generally treatment While anti-TNF Unlike Th17 cytokines, serum levels of Th1 serum Th17 cytokines, levels Unlike Young females from Far-Eastern and Asian Far-Eastern from females Young MHC class I alleles Stenotic lesions Stenotic Left subclavian arteryLeft with subclavian bilateral together Peripheral vascular abnormalitiesPeripheral including vascular Predominant adventitial scarring adventitial Predominant Branches of the internal arteryBranches carotid more 71 – 73 ] complex (MHC) [ 67 ] complex Differences Parameter Response to biologic treatments [ 61 , 74 – 78 ] biologic treatments to Response Demographic data [ 60 – 63 ] Cytokine response patterns response Cytokine [ 61 , treatment to Aortic involvement [ 69 ] involvement Aortic Association with major histocompatibility Association withhistocompatibility major Cluster analysis of involved arteries [ 70 ] of involved analysis Cluster Symptoms and physical findings [ 60 – 63 ] and physical Symptoms Histopathology [ 68 ] Histopathology Carotide involvement [ 70 ] involvement Carotide Similarities and differences between Takayasu arteritis (TAK) and giant cell arteritis arteritis (GCA) Takayasu (TAK) Similarities between and differences pathogenesis [ 60 – 63 ] pathogenesis [ 60 – 63 ] both diseases [ 66 ] for (IL)-6 and IL-17interleukin [ 61 , 63 ] IL-6 [ 63 – 65 ] treatments 6 Table Similarities Female dominance [ 60 – 63 ] Female of cell mediated immunity in Common role wall vessel inflammation in Granulomatous factor IL-12B genetic as theprominent most of expressions and vascular High serum levels corticosteroid to response and anti- Favorable

1 3 Rheumatology International (2019) 39:169–185 179 out inflammation dislocation tion NF1 cardiac murmurs, plus positive blood cultures murmurs,cardiac plus positive affecting the cardiac vegetations showing by endocarditis infective structures, aorta and ascending aorta root, wall erosion of thoracic and abdominal aorta erosion - wall with resulting forma aneurysmstion of true or false be helpful for differential diagnosis differential be helpful for parts of the arteries than thoracic than and long-segment stenosis concentric, smooth thickening, plasma cells, storiform fibrosis, obliterative and mild-to- obliterative fibrosis, plasma cells, storiform tissue eosinophilia moderate No systemic inflammation systemic No with or stenosis imaging arterialNo thickening wall with medial necrosis - withSimilar histopathology MFS, i.e., cystic Typical Marfanoid body status and clinical features including lens body status and clinical features Marfanoid Typical inflammation systemic No with or stenosis imaging arterialNo thickening wall without medial necrosis inflamma - cystic showing Histopathology Positive serology for Sy for serology Positive May be caused by various pathologies various be caused by May TAK, MFS, EDS, LDS, and diagnosis incudes Main differential Immunocompromised host Immunocompromised HIV for serology Positive Comments for differential diagnosis differential Comments for Presence of fever, abdominal pain, pulsatile mass and of fever, Presence confirm may the diagnosis of echocardiography Transesophageal Unlike typical arterial stenosis of TAK, TB aortitis causes vessel TB aortitis typical arterial causes vessel Unlike of TAK, stenosis Unlike TAK, more common in males more TAK, Unlike inflammation may Location of coarctation and absence of systemic Localized in bifurcation sites and in ostiums, rather than proximal rather than sites and in ostiums, Localized in bifurcation proximal ratherLocation of aortic intrarenal), aneurysms: abdominal (mostly limb arteries involved Upper rarely lesions plaque Punctate, linear calcifications and discrete rather than spots, linear smooth signals in PET-CT Localized hot rather of intima-media with ultrasonography, Localized thickening Increased serumIncreased IgG4 with infiltrate IgG4 increased lymphoplasmacytic shows Histology - section, rupture, or aneurysm mation, dissection, and, sometimes, aortic mation, dissection, and, sometimes, thereby regurgitation, LVV mimicking resulting in aortic wall thickening, aneurysm formation, formation, thickening, in aorticresulting wall and coronary incompetence arteryvalvular disease racic aortaracic of a bacterial infection, classically spreading from the from spreading heart, classically as in of a bacterial infection, endocarditis infective abdominal arteries involved leading to vessel wall thickening, stenosis, and aneurysm stenosis, in the thickening, wall vessel leading to LVV aorta mimicking thereby and its branches, descending aorta, immediately beyond the origin descending aorta,of the left beyond immediately arterysubclavian pancreas, major salivary glands, orbital tissue, lungs, kidneys, orbital salivary glands, major tissue, lungs, kidneys, pancreas, nodes, and retroperitoneum biliary lymph tree, branches and medium-sized arteriesbranches Autosomal dominant disorder of the connective tissue matrix of the dominant disorder connective Autosomal gene mutations from in the type III procollagen Results Descending and abdominal aortaresulting in dis - be affected, may Autosomal dominant disorder of the connective tissue matrix of the dominant disorder connective Autosomal mutations from in the fibrillin-1Results gene wall of the aortathoracic affect for the to aneurysm leading May Cardiovascular Sy may cause inflammation in the ascending aorta, Sy may Cardiovascular Wide range of vasculitides may be seen may of vasculitides range Wide occur disease may or occlusive Multiple aneurysm formation Segmental of the narrowing abdominal or distal descending tho - Definition May occur as a complication of septicemia, usually in the context in the context usually of septicemia, occur as a complication May and abdominal aorta,Thoracic peripheral, and intracranial, may cause granulomatous arteritis may tuberculosis Mycobacterium Commonly located in the junction of distal aortic and Commonly arch A fibroinflammatory condition involving many organs including organs many involving A fibroinflammatory condition cause true aortitis,May confusion with creating LVV Inflammatory vascular disease Inflammatory plus inflammation contribute risk factors Traditional cause aortic aneurysmsMay in aortic and lumen narrowing Pathologies which should be considered in the differential diagnosis of giant cell arteritis and/or Takayasu arteritis in the should be considered diagnosis of giant cell arteritis differential Takayasu which Pathologies and/or 7 Table Ehlers–Danlos Syndrome Type IV (EDS) [ 86 , 122 ] Type Ehlers–Danlos Syndrome Marfan syndrome (MFS) [ 86 , 121 ] syndrome Marfan Syphilis (Sy) [ 84 – 86 ] HIV (human immunodeficiency virus) infection [ 88 ] HIV (human immunodeficiency virus) infection Middle aortic [ 119 , 120 ] syndrome Mimicker Mycotic aneurysm [ 84 , 85 87 89 ] Mycotic Tuberculosis (TB) [ 84 – 86 ] Tuberculosis Congenital aorticCongenital coarctation [ 117 , 118 ] Immunoglobulin G4-related disease (IgG4-RD) [ 103 ] G4-related Immunoglobulin Atherosclerosis [ 108 – 116 ] Atherosclerosis

1 3 180 Rheumatology International (2019) 39:169–185 - ​ GCA arteries most commonly affected; aortic involvement rare arteries affected; aortic commonly involvement most stenosis with and diffuse tubular angiography angiography resonance foamy histiocytes surroundedfibrosis histiocytes by foamy tomatous Lisch nodules in the iris, café au lait macules and learn nodules in the iris,- Lisch tomatous café diagnosis be helpful in differential ing disabilities may ischemia with or without bleeding ischemia intraabdominal bicuspid aortic valve helpful in diagnosis bicuspid aortic valve Presence of organomegaly and isolated proteinuria not expected in expected and isolated proteinuria not of organomegaly Presence deposition staining Congo red with biopsy confirms amyloid No systemic inflammation systemic No Middle and distal portions internal of renal, and vertebral carotid, concentric narrowing Classic “string-of-beads” or focal appearance, on magnetic uptake edema, or contrast arterialNo thickening, wall Absence of systemic inflammation of systemic Absence hamar gliomas, tumors, optic tumors, plexiform Neurocutaneous Histological features include xanthogranulomatous of infiltration features Histological Cortical and associated pain of long bones typical osteosclerosis Presence of postprandial abdominal pain caused by intestinal intestinal abdominal pain caused by of postprandial Presence location anatomic a single limited to lesions generally Vascular or heritable diseases infectious, of other inflammatory, Absence History of previous malignancy and radiotherapy History of previous Comments for differential diagnosis differential Comments for No systemic inflammation systemic No needed testing Genetic of hypertelorism, presence Additional bifid uvula, cleft palate, and - ies including renal, internalies including renal, arteries and vertebral carotid, heterogeneous presentation heterogeneous artery coarctation of aorta, stenosis, or segmental of narrowing abdominal or distal descending thoracic aorta rial dissecting aneurysms,and to media, predisposing stenosis vessels occlusions in medium-sized and large irregularity, plus focal fibrosis and necrosis fibrosis plus focal irregularity, abdominal aortaç Amyloid deposition in temporal artery​ deposition in temporal mimic GCA Amyloid may May lead to aneurysm,occlusion, and dissection lead to stenosis, May hypertension is frequent Renovascular or TAK mimic GCA and limb claudication may Headache Non-inflammatory vasculopathy of small and medium-sized artervasculopathy Non-inflammatory Non-Langerhans histiocytosis affecting multiple organs, with affecting multiple organs, histiocytosis Non-Langerhans mimic LVV may involvement Vascular May cause vascular aneurysms/arteriovenous malformations, renal renal aneurysms/arteriovenous malformations, cause vascular May Frequently involves abdominal visceral arteries abdominal visceral involves Frequently of smooth muscle cells in the arte degeneration - Causes vacuolar Injury to vascular endothelial cells causes intimal thickening and endothelial cells causes intimal thickening Injury vascular to Definition Another genetic disorder of the connective tissue matrix of the disorder connective Another genetic mutations from in the gene TGF-β receptor Results aneurysms, and dissections in thoracic and cause tortuosity, May disease) [ 124 , 125 ] Primary [ 127 , 128 ] amyloidosis Fibromuscular dysplasia [ 86 , 126 ] dysplasia Fibromuscular Erdheim–Chester disease (ECD) [ 129 ] Erdheim–Chester Segmental arterial mediolysis (SAM) [ 130 ] Segmental arterial (SAM) mediolysis Post-radiation lesions [ 131 ] Post-radiation 7 Table (continued) Mimicker Neurofibromatosis type 1 (NF1) (von Recklinghausen Recklinghausen type 1 (NF1) (von Neurofibromatosis Loeys–Dietz syndrome (LDS) [ 86 , 123 ] syndrome Loeys–Dietz

1 3 Rheumatology International (2019) 39:169–185 181 atherosclerosis from vasculitis, as summarized in Table 7 differential diagnosis of aortitis is completed, other pathol- [111–116]. ogies which may mimic LVV, including atherosclerosis, Other pathologies which may mimic LVV include con- congenital aortic problems, and hereditary collagen tissue genital causes of aortic coarctation and middle aortic syn- disorders, should be excluded before diagnosing LVV. drome [117–120], hereditary disorders (Marfan syndrome [121], Ehler–Danlos syndrome [122], Loeys–Dietz syn- Acknowledgements The authors wish to thank Professor Dr. Suha Sureyya Ozbek, Head of Ege University Department of Radiology, for drome [123], neurofibromatosis [124, 125], fibromuscular providing the ultrasound image. dysplasia [126]), primary amyloidosis [127, 128], Erd- heim–Chester disease [129], segmental arterial mediolysis Compliance with ethical standards (SAM) [130], and post-radiation vascular lesions [131]. Practical points for differentiating those mimickers from Conflict of interest The authors declare that they have no actual or po- LVV were also given in Table 7. tential conflict of interest in relation to this article.

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