First published online August 6, 2007
British Journal of Radiology (2007) 80, 625-630
© 2007 British Institute of Radiology
doi: 10.1259/bjr/69016171
Reference values for Doppler ultrasound parameters of the thyroid in a healthy iodine-non-deficient population
T A A Macedo, MD
1
M C Chammas, MD, PHD
1
P T Jorge, MD, PHD
2
L Pereira de Souza, MD
3
L Farage, MD
3
B L Pegoraro, MD
3
S U Pessa
1 and
G G Cerri, MD, PHD
1
1 Division of Ultrasound of the Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo – Instituto de Radiologia, Av. Dr. Enéas de Carvalho Aguiar, 255, 3° andar, São Paulo, SP, Brazil, CEP 0503-001, 2 Division of Endocrinology, 3 Division of Radiology of the Hospital de Clínicas da Universidade Federal de Uberlândia – Departamento de Clínica Médica, Av. Pará, 1720, Uberlândia, MG, Brazil, CEP 38405-320
Correspondence: Dr Tulio Macedo, R. Delmira C R Cunha 740, Uberlândia 38408-208, Brazil. E-mail: tamacedo{at}hotmail.com
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Abstract
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The aim of this study was to describe normal Doppler parameter values in the thyroid arteries in an iodine-replete region. 165 individuals were randomly selected in a community located in the south-east of Brazil. We obtained a clinical history on each subject and determined serum thyrotropin, antiperoxidase antibodies, thyrotropin receptor antibody (TRAb) and thyroid volumes through ultrasound. Subjects with thyroid disease and those under 20 years of age were excluded. 84 representative subjects (30 men and 54 women) remained. The systolic peak velocity (SPV), resistive index (RI) and pulsatility index (PI) in the superior and inferior thyroid arteries were measured using a 5–12 MHz linear probe. Except for the RI, the distribution of all Doppler parameters was non-gaussian. The median and mean references for the SPV, RI and PI were 24.80 cm s–1 and 25.85 cm s–1, 0.60 and 0.62, and 0.98 and 1.04, respectively, for superior thyroid arteries; these reference values for the inferior thyroid artery were 20.92 cm s–1 and 21.50 cm s–1, 0.57 and 0.57, and 0.84 and 0.88, respectively (p<0.001). Women had greater SPV values (p<0.01). We have determined reference thyroid Doppler parameter values in our iodine-non-deficient population and prepared tables by sex and age.
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Introduction
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Some authors have already shown the possibility of distinguishing thyroid diseases and predicting their prognosis based on duplex-colour Doppler ultrasonography [1, 2]. These distinctions are usefully functional, because the duplex-colour Doppler is a non-invasive method and does not involve ionizing radiation [3]. Therefore, in order to comprehend the pathophysiology of the diseases whose vascularization is modified, some normal reference parameter definition is essential. However, currently, few studies report the normal reference range values of Doppler objective parameters in the superior, inferior and intraparenchymal thyroid arteries [4, 5]. The aim of this study was to describe the normal duplex-colour Doppler parameter values of thyroid arteries in an iodine-non-deficient region of Brazil.
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Methods and materials
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Patient demographics
165 adults were randomly selected from a few religious communities located in the south-east region of Brazil. The inclusion criteria were normal 3,5,3'-triiodothyronine (T3), thyroxine (T4), free T4 (fT4), antiperoxidase, thyroglobulin and thyrotropin receptor antibody (TRAb) levels. The exclusion criteria were: (1) younger than 20 years of age, (2) pregnancy, (3) use of thyroid hormone, (4) total or partial thyroidectomy and (5) agenesis or hypoplasia of the thyroid gland. Agenesis was considered when the thyroid parenchyma was not identified, and hypoplasia was defined as volume 
3.0 cm3. Of the 165 volunteers studied, 84 individuals (54 women and 30 men) fitted the inclusion criteria. The age range was between 20 and 69 years of age (average age of 41.6±13.0 years).
Sonography examination
Equipment
The examinations were performed using a PhilipsTM HDI 5000 (Bothell, WA) device, manufactured in 2000, attached to a 5–12 MHz linear multifrequency probe.
Examination technique
The sonographic study was performed with the patient in dorsal decubitus with a cushion under the shoulders and the neck hyperextended. In order not to underestimate the vascularization intensity, the probe was lightly positioned on the skin without any compression (Figure 1
). The images were obtained on colour and pulsed Doppler. We did not use frequency shift-coded Doppler (so called conventional Doppler), but only amplitude-coded colour Doppler.
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Figure 1. Amplitude colour Doppler obtained correctly without compression(a) and improperly with compression (b), which underestimates the vascularization.
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Colour Doppler
A short apnoea was requested from the patients during the duplex-colour Doppler recordings. Colour Doppler parameters were standardized and, for all studies, the same presets were used for the acquisition. The equipment was set up to "thyroid", configured as follows: PRF (pulse repetition frequency) 700 Hz, colour map 1, WF (wall filter) medium and flow option medium velocity. These parameters allow the measurement of blood flow between a lower limit of –4.4 cm s–1 (away from the transducer) and an upper limit of 4.4 cm s–1 (towards the transducer), which we have found to be the appropriate range for the thyroid parenchyma of normal subjects. In addition, the gain settings (between 72 and 79) were adjusted to avoid background noise.
The probe was positioned in the longitudinal direction, with its centre at the middle third of the thyroid lobes. The isthmus vascularization was not taken.
In order to quantify the vascularity of the parenchyma, the colour pixel density (CPD) was calculated as follows:
- The digital images containing the longitudinal middle third of the thyroid lobes were stored on optical disks in the "Data Exchange File Format – DEFF" (.CRI) format. The colour Doppler images were stored when the vessels were more prominent (i.e. maximum filling of the systolic phase).
- These files were uploaded to an external workstation equipped with software that easily calculates the CPD (SysArea© version 1.1). This software was set up as follows: filter 15, amplitude colour mode and black background. CPD was defined as the percentage of the area of interest occupied by colour velocity signals, calculated as the colour pixel area divided by the total area of the region of interest (ROI) x 100 (dimensionless).
- Later, a polygonal ROI was drawn around the thyroid surface by the researcher (TAM). If necessary, the ROI was altered point by point to exactly conform to the shape of the lobe cross-section (Figure 2). The maximum area of the ROI was limited by the colour Doppler area box and the probe field of view (approximately 35 mm).
- After the selection, the computer promptly displayed the CPD value. The gland CPD value was equal to the average between the two lobes.
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Figure 2. Software interface used to measure the thyroid colour pixel density(CPD). The area of interest was delimited (green solid trace) by the user.
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The sample volume was adjusted to 2 mm. The PRF was set according to the speed of the flow and to obtain the best graphic representation. The evaluation of the superior thyroid artery was achieved with the probe positioned in the oblique sagittal plane, close to the superior thyroid pole, as demonstrated in Figure 3.
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Figure 3. Duplex-colour Doppler of the superior thyroid artery with the probe positioned in the oblique sagittal plane.
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The inferior thyroid artery was examined in the oblique transversal plane, close to the transition between the medium and the inferior third of the thyroid (Figure 4).
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Figure 4. Duplex-colour Doppler of the inferior thyroid artery with the probe positioned in the oblique transversal plane.
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The cursor for evaluation of the inferior thyroid artery was set close to the trachea in order to avoid artefacts coming from the common carotid artery and the internal jugular vein.
The systolic peak velocity (SPV) and resistive and pulsatility index (RI and PI) values in the superior and inferior thyroid arteries were obtained. The Doppler angle was corrected to values under or equal to 60°.
The mean value found in the right and left lobes was used as a representative parameter.
Laboratory evaluation
All the patients were submitted to thyrotropin, T3, T4, fT4, thyroglobulin, antiperoxidase (AutoDELFIATM kits, PerkinElmerTM Wallac Oy, Turku, Finland) and TRAb (TR-AB, CIS bio International, Gif-sur-Yvette Cedex, France) serological dosage. The normal value ranges for these tests at our laboratory are thyrotropin (0.3–4.2 mU l–1), T3 (1.3–2.5 nmol l–1), T4 (69–141 nmol l–1), fT4 (10.2–17.0 pmol l–1), thyroglobulin (<45 pmol l–1), antiperoxidase (<30 mU l–1) and TRAb (<12 %).
Statistical analysis
The Student t-test and Mann–Whitney U-(Wilcoxon) test were used for comparison between two independent samples for variables with gaussian and non-gaussian distribution, respectively.
The Cochran–Armitage 
2 statistic for trend was used in the nominal analyses. The statistical package NCSS (Kaysville, UT), "August 4 2005 Release 1" version, was used to make the statistical analysis. It was considered significant when p<0.05.
Ethics
This study was approved by our institution's Committee of Ethics in Research. All subjects signed the term of consent with no restriction.
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Results
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It was possible to obtain the values from all individuals. Except for the RI, all other continuous variables were non-gaussian. The examinations lasted approximately 23 min. The time spent on the CPD analysis was 2 min for each subject.
The average CPD was 3.67±5.63%. There was no significant difference in the CPD for gender (p = 0.085) (Table 1). The CPD was higher in older individuals (p<0.02) (Table 2).
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Table 1. Means and standard deviations of systolic peak velocity(SPV) and resistive (RI) and pulsatility indices (PI) of the superior and inferior thyroid arteries in 84 healthy individuals, according to gender
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Table 2. Means and standard deviations of systolic peak velocity(SPV) and resistive (RI) and pulsatility indices (PI) of the superior and inferior thyroid arteries in 84 healthy individuals, according to age group
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The SPV in the superior thyroid artery was higher than in the inferior one (p<0.001) (Table 3). The SPV averages in the superior and inferior thyroid arteries were 25.84±8.76 cm s–1 and 21.50±7.72 cm s–1, respectively (Table 3).
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Table 3. Means, standard deviations and percentiles of systolic peak velocity(SPV) and resistive (RI) and pulsatility indices (PI) for the superior and inferior thyroid arteries in 84 healthy individuals
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The impedance indices were higher in the superior thyroid artery than in the inferior one (p<0.001) (Table 3
). The averages of the RI and PI values in the superior thyroid artery were 0.62±0.07 and 1.04±0.24, while in the inferior thyroid artery, they were 0.57±0.07 and 0.88±0.18, respectively (Table 3).
SPV values in the superior and inferior thyroid arteries were higher in women than in men (p = 0.011 for the superior thyroid artery and p = 0.017 for the inferior thyroid artery) (Table 1). There was no significant difference in the impedance indices (RI and PI) between men and women in both arteries (p>0.05) (Table 1). In addition, the SPV in the thyroid arteries increased with age (p<0.001).
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Discussion
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The colour Doppler-based thyroid vascularization evaluation has been used for the differential diagnosis of diffuse and neoplastic diseases. This method is widely available, fast, relatively cheap, non-invasive, does not involve ionizing radiation, is capable of measuring the blood flow and calculates the impedance indices [3, 6–9]. Although the normal reference duplex Doppler parameters are very important to compare and contrast abnormal values found in some thyroid diseases, this is the first study, to our knowledge, that describes the normal duplex Doppler parameters at the thyroid arteries.
The SPV in intraparenchymal arteries was not used in our study because of the small diameter and the difficulty in correcting the Doppler angle. As this imprecision can lead to mistakes in the calculation of the blood flow speed, we preferred not to use it.
However, this does not happen in larger vessels, such as the superior and inferior thyroid arteries, because a larger diameter enables the proper Doppler angle correction. We observed that the SPV was higher in the superior thyroid artery than in the inferior one. The mechanism for this is uncertain, but the afferent vessels could be essential, because the superior thyroid artery is supplied by the external carotid artery, larger than the thyrocervical trunk, which is a vessel afferent to the inferior thyroid artery.
Previous studies on SPV have not compared the differences between superior and inferior thyroid arteries. Castagnone et al [2] and Vitti et al [1] only studied the inferior thyroid artery and did not consider gender and age variables. Moreover, Chan et al [4] and Arntzenius et al [10] only studied the superior thyroid artery of young patients. Contrasting these previous reports, our study was able to demonstrate the distribution curves, averages and percentiles of variables obtained from duplex-colour Doppler in a representative sample of our population. Nevertheless, despite the limitations of those studies, the values found by those authors for SPV in the thyroid arteries were similar to our results (Table 4).
In our research, the patients in the higher age group presented higher SPVs. This could be explained by: (1) higher blood pressure levels associated with lesser compliance and/or vessel atherosclerotic stenosis, which could increase the systolic blood flow in the thyroid arteries; (2) larger thyroid volume, which would demand additional arterial supply and elevation in the blood flow speed; (3) the highest prevalence of nodules and hyperplasia could determine a larger blood load to the thyroid.
In relation to gender variables, the SPV values are higher in females. This result was already found in a previous study performed by Chan et al [4]. This author suggests that this is due to estrogens. These hormones would act on (1) the thyroid metabolism, increasing it and determining an increment in the blood load to the thyroid and/or (2) the cardiovascular system, through an increase in the arterial blood pressure.
A few articles have been published on impedance indices in thyroid arteries. Chan et al [4], studying the PI in the superior thyroid artery, described results very similar to (1.19±0.16 for men and 1.15±0.32 for women in the ovulatory period) those found in our research. Castagnone et al [2] evaluated the RI in the inferior thyroid artery and also found values very close (0.55±0.02) to the values in our study (0.57±0.07). Neither of these studies compared the impedance indices between the superior and inferior thyroid arteries as we have done. In this study, we have demonstrated that the impedance indices are higher in the superior thyroid artery than in the inferior one. This could be explained by differences in compliances and/or outlying resistance of the vessels [11, 12] being higher in the superior thyroid artery. Perhaps it may be explained by the fact that the efferent vessels from the superior thyroid artery do not only supply the thyroid parenchyma, but also the cervical structures with high impedance indices, such as muscles and the larynx [13] (Figure 5).
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Figure 5. Colour Doppler of the thyroid superior third demonstrating a superior thyroid artery branch(arrow) to muscular structures and the larynx.
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In this study, we found CPD values higher (3.67±5.63%) than those described before by Hiromatsu et al [14] (0.73±0.94%). This is probably a result of the equipment used by these authors, older and less sensitive than that used in our study. This difference exemplifies a disadvantage of the CPD analysis, which depends on the equipment and the Doppler gain level [15]. Besides, the CPDs obtained were calculated by different software, which could result in diverse values.
In conclusion, we have determined reference thyroid Doppler parameter values in our iodine-non-deficient population. All these reference values constitute a basis for understanding the pathophysiology of the diseases whose vascularization is modified.
This work has been presented partially at the 2006 European Congress of Radiology.
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Acknowledgments
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We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for their financial support.
Received for publication July 16, 2006.
Revision received October 18, 2006.
Accepted for publication November 7, 2006.
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References
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Abstract
Introduction
