R E V I E W A R T I C L E
Twinkling artifact on color Doppler ultrasound: an advantage
or a pitfall?
Ebru Ozan1• Gokce Kaan Atac1•Sadi Gundogdu1
Received: 10 December 2015 / Accepted: 4 April 2016 / Published online: 28 April 2016 Ó The Japan Society of Ultrasonics in Medicine 2016
Abstract The twinkling artifact (TA) or color comet-tail artifact is characterized by a rapidly changing mixture of red and blue color Doppler signals. Even though many diseases and clinical conditions have been shown to pro-duce this artifact, its source is not clearly understood yet. The TA may provide additional information to gray-scale ultrasound findings in several clinical situations. However, there may be pitfalls to keep in mind. We must first be aware of the TA to benefit from the advantages and avoid the pitfalls. In this review, we aim to give practicing radiologists an overview of the mechanisms and clinical applications of the TA by illustrating sample cases we have encountered.
Keywords Ultrasound Color Doppler ultrasound Twinkling artifact Color comet-tail artifact
Introduction
The twinkling artifact (TA) appears as a rapidly alternating focus of red and blue color Doppler signals behind rough reflective surfaces, imitating turbulant flow. On spectral Doppler ultrasound (US), a broadband heterogenous signal representing noise is yielded, instead of a flow spectrum. Since it was first described in 1996 [1], various conditions have been shown to produce this artifact. Although several
mechanisms have been proposed regarding the cause of TA, its source is not clearly understood yet. It is helpful in several conditions where gray-scale US does not provide satisfactory information. Radiologists should be familiar with this artifact to benefit from the advantages and avoid the pitfalls. In this review, we aim to enhance the most useful clinical applications of TA and call attention to the pitfalls by illustrating sample cases we have encountered.
Mechanisms
Several hypotheses have been proposed to explain the mechanism of TA. Rahmouni et al. considered TA to be associated with individual reflectors of rough surfaces that split the US beam into a complex beam, resulting in random scattering [1]. Chelfouh et al. found an in vitro relationship between TA and the morphology and biochemical compo-sition of urinary stones [2]. In addition, the color Doppler system technology and several ultrasound machine settings, including focal depth, color filter, and gain settings, were conjectured to affect the intensity or shape of the artifact by other authors [3, 4]. Accordingly, decreasing gray-scale gain, increasing color-write priority, and placing the focal zone at or below the rough reflective surface may enhance TA (Figs.1,2). Gao et al. encouraged the use of a lower color Doppler carrier frequency in terms of pronouncing TA [5]. While Kamaya et al. postulated the ‘phase-jitter,’ a narrow band of intrinsic noise produced by the sonography scanner, as the source of TA [6], a more recent study related TA to the presence of stabilized bubbles in cracks on the stone surface [7]. On the other hand, Liu et al. found a relationship between the scatter lights of glass beads and the twinkling sign, and concluded that the US radiation force-driven micro oscilla-tion was the cause of the twinkling sign [8].
& Ebru Ozan
1 Department of Radiology, Ufuk University School of
Medicine, Dr. Ridvan Ege Training and Research Hospital, Mevlana Bulvarı (Konya Yolu) No: 86-88, 06520 Balgat, Ankara, Turkey
Gallbladder and biliary duct diseases
Although it is well known that gallbladder stones can produce TA [9], it has no diagnostic value, as they are easily diagnosed with gray-scale US (Fig.3). An in vitro study conducted to investigate the relationship between this artifact and the biochemical architecture of gallstones suggested that most of the gallstones producing prominent TAs were cholesterol stones, while black pigment stones produced weak or no TAs [10]. In addition, cholesterol stones with rough surfaces did not seem to produce stronger artifacts than those with smooth surfaces. This finding was discordant with other studies concluding that TA was associated with the rough surface of a strongly reflective structure [1,2,6]. It was attributed to the greater effect of the complicated internal structures causing mul-tiple reflections, rather than the surface itself, on the for-mation of this artifact.
Even if biliary sludge commonly produces strong TA (Fig.4), it has little or no diagnostic value, while recog-nizing the artifact and differentiating it from flow on spectral Doppler is helpful to exclude a gallbladder mass.
Identifying common bile duct stones is often more dif-ficult than detecting gallbladder stones, as they are fre-quently obscured by bowel gas, even when the duct is dilated. Thus, the presence of TA facilitates stone detection [11].
Fig. 1 Effect of focal zone on intensity of twinkling artifact (Logiq 7, GE Healthcare, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, USA). a Color Doppler ultrasound image shows a weak artifact when the focal zone is located above the object causing the artifact (arrow). bTwinkling artifact is enhanced when the focal zone is located at the level of the object (arrow)
Fig. 2 Effect of color-write priority on intensity of twinkling artifact (Logiq 7, GE Healthcare, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, USA). a Color Doppler ultrasound image shows decreased intensity of the artifact when the color-write priority level is low (circle). b When the level is high (circle), the artifact is pronounced
Fig. 3 A 43-year-old woman with a gallbladder stone was examined by abdominal US (Logiq 7, GE Healthcare, curved transducer, 3.5C, 2–5 MHz, Milwaukee, WI, USA). Color Doppler ultrasound image shows the twinkling artifact produced behind the gallstone
Evaluation of gallbladder adenomyomatosis (GADM) is another clinical application where the presence of TA can be advantageous. GADM is a benign epithelial and smooth muscle proliferation of the gallbladder wall, with accompanying invaginations of the mucosa into the thickened muscular layer, referred to as Rokitansky– Aschoff sinuses. On gray-scale US, the imaging char-acteristics of GADM include focal or diffuse thickening of the gallbladder wall, small intramural cysts repre-senting Rokitansky–Aschoff sinuses, and multiple echo-genic intramural foci with or without a gray-scale comet-tail reverberation artifact, arising from cholesterol crys-tals within the Rokitansky–Aschoff sinuses [12]. These tiny echogenic foci can produce TA on color Doppler US (Fig.5). Recognizing this artifact and confirming that it is just noise rather than flow on spectral Doppler is of great value for excluding gallbladder carcinoma on the way to making a definitive diagnosis [13]. When the gray-scale comet-tail artifact is weak or absent, in par-ticular, the presence of TA can be useful to differentiate GADM from isolated polyps localized on the non-de-pendent wall of the gallbladder [14]. In addition, this artifact may aid identification of the fundal form of GADM, especially when the fundus is obscured by bowel gas or a reverberation artifact from the subcuta-neous tissue.
Bile duct hamartomas (BDHs) of the liver are comprised of cystic dilated bile ducts filled with variable amounts of collagenous stroma. Imaging is valuable in the diagnosis of BDHs, particularly to differentiate them from cirrhosis or metastasis. Multiple tiny echogenic foci spread along the liver, causing TAs on color Doppler US, and accompany-ing comet-tail artifacts on gray-scale US are valuable sonographic features for making a correct diagnosis of
BDHs and avoiding unnecessary imaging modalities or invasive procedures [11,15].
Genitourinary tract diseases
Urinary stones showing distinct echogenicity and discrete posterior acoustic shadowing can easily be detected on gray-scale US. However, there may be many equivocal cases in clinical practice, mostly due to the small size and indiscrete posterior shadowing of stones. The presence of TA may be useful in such cases (Fig.6). Aytac and Ozcan concluded that TA can help differentiate a small stone from other small echogenic structures [3]. In a retrospective study, the correlation of TA on color Doppler US with unenhanced computed tomography (CT) in the detection of nephrolithiasis was investigated. Although TA was asso-ciated with nephrolithiasis, a high false-positive rate was found when compared with 5-mm unenhanced CT images [16]. On the other hand, Korkmaz et al. evaluated the efficiency of TA in detecting stones smaller than 5 mm in diameter and concluded that satisfactory results can be achieved with the combined use of US and color Doppler US in comparison with CT [17]. Yavuz et al. conducted a prospective study to compare the effectiveness of TA versus unenhanced CT with diagnose millimetrical nephrolithiasis [18]. In this study, TA was considered to be sensitive, and it was concluded that color Doppler US might be preferred to unenhanced CT in the detection of stones smaller than 5 mm. Furthermore, Chelfouh et al. suggested that TA may help predict fragmentability, regarding the existence of an in vitro relationship between TA and the chemical composition of urinary stones [2].
It can be difficult to evaluate ureteral stones due to obscuring effects of bowel gas, especially when they are located in the middle or distal ureter. Small stones in the ureterovesical junction can be missed when hydronephrosis is mild or absent and ureteral jet is present (Fig.7). The presence of TA strongly supports the diagnosis of ureteral stone. Ripolle´s et al. concluded that TA was sensitive and specific for the diagnosis of ureteral stones in patients with renal colic in an emergency setting [19]. The authors also emphasized the usefulness of TA to detect ureteral stones, especially those located in the middle ureter, with this location being the most difficult portion for sonographic examination. A more recent study investigated the correlation of TA in ureteral stones with clinical parameters [20]. The absence of TA was found to be associated with considerable pain, more recent colic, and difficult passage of a guidewire across the stone. Accordingly, the authors concluded that the absence of TA was a valuable sign, indicating the presence of a significant obstruction requiring intervention.
Fig. 4 A 58-year-old woman with right upper quadrant pain was examined by abdominal US (Logiq 7, GE Healthcare, curved transducer, 3.5C, 2–5 MHz, Milwaukee, WI, US). Color Doppler ultrasound image shows the twinkling artifact from sludge. It is important to recognize this artifact to exclude flow in a gallbladder mass
Breast
While macrocalcifications (e.g., large, coarse, and popcorn calcifications) may produce TA (Fig.8), this finding does not represent clinical significance as they are considered benign and are readily seen on mammography (MG) or gray-scale US.
Punctate echogenic foci may be present in both benign and malign breast lesions and may produce TA on color Doppler US (Figs.9,10). The ability to detect calcifications
on US has improved with the recent advances in US tech-nology and the use of higher frequency transducers. Although US is not yet as sensitive as MG for detecting calcifications in cases of DCIS, it may serve as an useful adjunct to increase the mammographic specificity [21]. In addition, US can guide potential biopsy in cases of micro-calcifications. Furthermore, Hashimoto et al. suggested that detection of microcalcifications on US may present clinical significance in invasive breast carcinoma cases to predict the degree of malignancy and to decide adjuvant chemotherapy Fig. 5 A 55-year-old woman with gallbladder adenomyomatosis was
examined by abdominal US (Logiq 7, GE Healthcare, curved transducer; 3.5C, 2–5 MHz, linear transducer; 12L, 4.5–13 MHz, Milwaukee, WI, USA). a Gray-scale ultrasound image shows focal thickening of the gallbladder wall in the fundus (arrows). b Color Doppler ultrasound image shows twinkling artifacts thought to arise from cholesterol crystals on the fundus wall, which helped establish
the diagnosis of the fundal form of adenomyomatosis. c Spectral Doppler ultrasound image showing a broadband heterogenous signal representing noise is yielded, instead of a flow spectrum. d When the gallbladder fundus was examined with a linear transducer, cholesterol crystals that initially were not identified with a convex transducer were better appreciated
[22]. Recently, Tsujimoto reported a new clinical application of TA in non-mass image-forming lesions with microcalci-fications in the breast [23]. The author reported two cases of gathering microcalcifications in which TA was observed and
regarded the ‘difference in path length (DL)’ as the cause of the TA. Accordingly, he concluded that, in the cases of scattered calcifications, no TA is generally detected due to the lack of DL. In addition, the author emphasized future Fig. 6 A 38-year-old man with a right renal stone was examined by
abdominal US (Logiq 7, GE Healthcare, curved transducer, 3.5C, 2–5 MHz, Milwaukee, WI, US). Gray-scale ultrasound image (left) shows a mild echogenic focus without discrete posterior acoustic
shadowing (calipers) in the lower pole of the right kidney. The corresponding color Doppler image (right) shows the twinkling artifact that proves that the echogenic focus is a small renal stone
Fig. 7 A 35-year-old man with renal colic and hematuria was examined by abdominal US (Logiq 7, GE Healthcare, curved transducer, 3.5C, 2–5 MHz, Milwaukee, WI, USA). Gray-scale ultrasound image (left) shows a small echogenic focus without discrete posterior acoustic shadowing (calipers) in the left
ureterovesical junction. The corresponding color Doppler image (right) shows the prominent twinkling artifact representing the stone. Ureteric jet is also evident on the same side (arrow), indicating the presence of a partial obstruction
Fig. 8 A 43-year-old woman was examined with mammography and ultrasound (Logiq 7, GE Healthcare, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, USA) for breast screening. Left CC mammogram (left) shows round macrocalcifications in the breast.
Gray-scale ultrasound image (upper right) shows one of the macrocalcifications with posterior acoustic shadowing. The corre-sponding color Doppler image (lower right) shows the presence of the twinkling artifact
Fig. 9 A 26-year-old woman with a painful mass in her right breast was examined with ultrasound (Logiq 7, GE Healthcare, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, USA). Gray-scale ultrasound image (left) shows an oval-shaped hypoechoic mass with ill-defined punctate echogenic foci, and the corresponding color
Doppler image (right) shows evidence of the twinkling artifact from the echogenic foci detected in the mass. Ultrasound-guided Tru-Cut biopsy was performed and pathological examination revealed a fibroadenoma
applications of a new US modality called multidetector ultrasonography (MD-US) to detect TA in microcalcifica-tions of the breast.
Thyroid gland and cervical lymph nodes
Egg-shell or coarse calcifications in the thyroid gland may cause TA. In addition, some punctate echogenic foci may give rise to TA (Fig.11). Tchelepi and Ralls concluded that TA observed in punctate echogenic foci should not be used to differentiate colloid material from microcalcifica-tion, pointing out the limited experience in this area [14]. Nevertheless, considering the statement that the presence of microcalcifications within a nodule raises the likelihood of malignancy [24], as is the case with microcalcifications of the breast, it seems that this area represents another potential future application of TA, requiring further investigations.
Cervical lymph nodes should be evaluated for lymph node metastases prior to thyroidectomy in patients with thyroid cancer. The presence of microcalcifications within the lymph node suggests involvement with papillary thy-roid cancer and is also one of the US features associated with the highest risk of malignancy [25]. In addition, there may be cases of abnormal lymph nodes representing metastatic thyroid cancer adjoining a normal gland in cases where the primary tumor is too small size to be visible on US [24]. Microcalcifications in metastatic cervical lymph nodes may be a source of TA (Fig.12), and this can be advantageous, especially in cases with microcalcifications exhibiting subtle echogenicity on gray-scale US.
Soft tissue lesions
Gray-scale and color Doppler US play an important role in the diagnosis of soft tissue tumors. Despite the fact that no specific finding is present to differentiate between benign and malignant lesions, color Doppler US may be useful for evaluating the internal vascularity of the lesion [26,27].
We experienced a case with an epidermal inclusion cyst in which TA was detected on color Doppler US. The subcutaneous lesion demonstrated well-defined margins and a heterogenous echo pattern with scattered punctate echogenic foci causing TAs (Fig. 13). Well-defined margins, ovoid contour, internal echoes due to the presence of keratinous debris, and avascularity on color Doppler US are typical US findings of epidermoid cysts [26]. In this instance, keratinous debris may be considered to be the source of TA in our case of epi-dermal inclusion cyst. Consequently, when a superficial soft tissue lesion with internal echoes exhibiting TA on color Doppler US is encountered, epidermal inclusion cyst should be kept in mind when making the differential diagnosis. In addition, the pitfall of using TA as a diagnostic sign in soft tissue lesions is to be aware of this artifact and recognize it is just ‘noise’ rather than flow on spectral Doppler US to differentiate it from internal vascularity of the lesion.
Pediatric applications
Predicting the chemical composition of stones to guide management options and detection of tiny calculi, partic-ularly after lithotripsy, are regarded as potential uses of TA in pediatric US [28]. Regarding the mounting concerns Fig. 10 A 44-year-old woman with a palpable mass in her left breast
was examined with ultrasound (Logiq 7, GE Healthcare, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, US). Gray-scale ultrasound image (left) shows a hypoechoic mass with microlobulated margins. Color Doppler image (right) shows the twinkling artifact from the indistinct echogenic foci in the breast parenchyma close to the mass that was not clearly defined initially on gray-scale ultrasound imaging. Tru-Cut biopsy was performed and the pathological diagnosis of an infiltrating ductal carcinoma was achieved
about radiation exposure from CT, one must consider that TA may provide additional information for the diagnosis of urinary stones by US, reducing the frequency of the use of CT in the pediatric population (Fig.14). Information about pediatric applications of TA in disorders other than urinary stones seems to be limited in the literature, necessitating further investigation of this issue.
Other conditions
There are several other diseases or conditions displaying TA that have been reported in the literature in which the presence of TA may be advantageous to guide the diag-nosis. Diagnosis of chronic pancreatitis on US may be problematic in cases with discrete parenchymal calcifica-tions. TA displayed on color Doppler US can help establish
the diagnosis by enhancing the visualization of subtle calcifications [14]. TA may also be useful for detecting intestinal pneumatosis and aiding the initial diagnosis on US, reducing the requirement for further imaging studies, such as radiography and CT [29].
Conclusions
Although the most common and useful application of TA seems to be evaluation of urinary stones, many other conditions may be encountered in sonographic practice. In addition, detection of breast microcalcifications seems to represent a potential future application of TA. Subtle abnormalities on gray-scale US may be enhanced and better appreciated when TA is present on color Doppler US. The leading drawback of TA is the possibility of Fig. 11 A 47-year-old man with a nodule in the right lobe of the
thyroid gland was examined with ultrasound (Logiq 7, GE Healthcare, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, USA). Gray-scale ultrasound image (upper left) shows a cystic nodule with internal punctate echogenic foci thought to represent colloid material.
Some of these foci caused twinkling artifacts on color Doppler ultrasound (upper right, lower left). Spectral Doppler image shows (lower right) a heterogenous broadband signal representing noise. Fine needle aspiration biopsy yielded cytopathologic findings repre-senting benign cyst content
Fig. 12 A 30-year-old woman with a history of Hashimoto thyroidi-tis was examined with ultrasound (Logiq 7, GE Healthcare, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, USA). Gray-scale ultrasound image (upper left) shows the hypoechoic thyroid gland with a heterogeneous echotexture and echogenic septations. No distinct nodule is identified. Gray-scale ultrasound image (upper right) shows one of the cervical lymph nodes with subtle echogenic
foci. Color Doppler ultrasound images (lower left and lower right) show twinkling artifacts from echogenic foci thought to represent microcalcifications within the lymph nodes. Ultrasound-guided aspi-ration of the suspicious nodes was performed, and the sample sent for thyroglobulin assay yielded a diagnosis of metastatic papillary thyroid carcinoma
Fig. 13 A 28-year-old man with a mass growing in size in his left gluteal region was examined with ultrasound (Logiq 7, GE Health-care, linear transducer, 12L, 4.5–13 MHz, Milwaukee, WI, USA). Gray-scale ultrasound image (left) shows a subcutaneous soft tissue mass with a heterogenous echo pattern and well-defined margins. On
color and spectral Doppler ultrasound (right), ill-defined punctate echogenic foci causing twinkling artifacts and corresponding noise are demonstrated, and no internal vascularity of the mass is detected. Excisional biopsy was performed and the pathological examination revealed a diagnosis of epidermal inclusion cyst
confusing it with vascular flow; however, spectral Doppler yields noise rather than flow. Under the circumstances, being familiar with TA is essential for avoiding the pitfalls and benefiting from the advantages.
Compliance with ethical standards
Conflict of interest The authors declare that they have nothing to disclose and they have no conflict of interest.
Ethical standards All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1964 and later versions. Informed consent was obtained from all patients for being included in the study.
Informed consent Additional informed consent was obtained from all patients for which identifying information is included in this article.
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