# Comparing CT and MR Properties of Artificial Thrombi According to Their Composition

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## Abstract

**:**

_{1}and T

_{2}NMR relaxation times and measurements of the apparent diffusion coefficient (ADC). In addition, the thrombus models were CT-scanned in a dual-energy mode (80 kV and 140 kV) and in a single-energy mode (80 kV) to measure their CT numbers. The results confirmed that RBC thrombi can be distinguished from platelet thrombi by using ADC and CT number measurements in all three settings, while they cannot be distinguished by using T

_{1}and T

_{2}measurements. All measured parameters allowed for the differentiation of RBC thrombi according to their HT values, but the best sensitivity to HT was obtained with ADC and single-energy CT measurements. The importance of this study also lies in the potential application of its results for the characterization of actual thrombi in vivo.

## 1. Introduction

## 2. Materials and Methods

#### 2.1. Artificial Thrombi

_{2}(320 mmol/L) was added to each sample and mixed thoroughly. To make the platelets stick to each other, thrombin 10 IU (Thrombin, Sigma-Aldrich, Burlington, MA, USA) was added to the sample. This was mixed manually until platelet aggregates were visibly seen sticking together and forming a thrombus. These thrombi had a maximum diameter of 2 mm, which is consistent with the platelet-rich thrombi found in clinical cases. These thrombus models were examined with the first measurements within an hour of their formation to prevent their drying. After the first set of measurements, the thrombi were left at room temperature until the second set of measurements 24 h after their formation. Prior to these measurements, the thrombi were examined visually, and the surrounding serum and RBCs extruded by clot retraction were removed from the sample. The weight of the extruded volume was measured.

#### 2.2. Nuclear Magnetic Resonance Measurements and Analysis

_{1}and T

_{2}, as well as the apparent diffusion coefficient (ADC), were measured from signals of the entire sample (in a non-imaging fashion). The measured NMR parameters thus corresponded to their sample average. The longitudinal (T

_{1}) relaxation time was measured using the inversion recovery (IR) pulse sequence with 14 different IR times in a range from 50 ms to 10 s logarithmically equidistant [19]. The transversal (T

_{2}) relaxation time was measured using the Carr–Purcell–Meiboom–Gill (CPMG) sequence with the inter-echo times of 6.1 ms (100 MHz system) and 2.1 ms (400 MHz system) [20]. ADC was measured using the pulsed-gradient spin-echo (PGSE) sequence in 11 different b-values in ranges from 0 to 826 s/mm

^{2}(100 MHz system) and from 0 to 893 s/mm

^{2}(400 MHz system) [21].

#### 2.3. Computer Tomography Imaging and Analysis

#### 2.4. Statistical Analysis

_{1}, T

_{2}, ADC) and the parameters measured using CT (CT number) of the RBC thrombus models were statistically analyzed using linear regression to verify the existence of a possible correlation between the measured parameters and HT and the dependence of this correlation on time from the formation of a thrombus. The linear regression analysis was also used to analyze the dependence of the extruded serum and RBC fraction on HT. The linear regression analysis was performed using Excel (Microsoft, Redmond, WA, USA).

## 3. Results

_{1}, T

_{2}and the ADC parameters and using CT for CT numbers, and, finally, the measured values were analyzed statistically using linear regression.

#### 3.1. Extruded Serum and RBC Fraction

^{2}= 0.33). Furthermore, no significant differences (p > 0.05) were found when comparing the measured fractions of the extruded serum and RBCs between the different HT groups. An analysis of the extruded serum and RBC fractions was performed only for the RBC thrombi, as the platelet thrombi were so small that their extruded volumes were negligible, and their weight could not be reliably measured with the available equipment.

#### 3.2. NMR Measurements

_{1}) and transversal (T

_{2}) relaxation times and measurements of the apparent diffusion coefficient (ADC) for the thrombus models measured 5 h and 24 h after their formation. These measurements were made using 100 MHz and 400 MHz NMR systems. All presented data were obtained as the average of six replicate experiments for each thrombus model. Experimental errors correspond to the standard deviations of the measurements within each thrombus model group. The table elements highlighted in red correspond to the RBC thrombus models that overlap in T

_{1}or T

_{2}values with the corresponding platelet thrombus model values.

_{1}values at 40% HT and 5 h and at 80% HT and 24 h for the 100 MHz MR system, whereas there was no overlap in the measurements for the 400 MHz MR system. There was no overlap in the ADC values in the measurements on either the 100 MHz or 400 MHz MR system. For the T

_{2}values, there was some overlap at 5 h for both MR systems and at 24 h for the 100 MHz MR system.

_{1}, T

_{2}and ADC as a function of HT, which are shown in Figure 3. From these graphs, it can be seen that all three measured NMR parameters have a negative trend with increasing HT, i.e., negative slopes (k) of the trendlines (Table 2). The trends are approximately equally significant for both T

_{2}(Figure 3b) and ADC (Figure 3c), while they are less significant for T

_{1}(Figure 3a). This can be confirmed by the parameter 100 × k/(50 × k + n) being significantly higher for ADC and T

_{2}than for T

_{1}at both magnetic field strengths (Table 2). As expected, the T

_{1}values in Figure 3a are longer for measurements at 400 MHz than for measurements at 100 MHz (e.g., 2490 vs. 1950 ms for the trendline y-intercept (n) at 5 h), while the slopes of the corresponding trendlines are practically identical for both magnetic field strengths (k = −8.7 vs. −9.2 ms/% at 5 h). The T

_{2}measurements in Figure 3b show considerably higher T

_{2}values at a lower (100 MHz) than at a higher (400 MHz) magnetic field strength (n = 400 vs. 145 ms at 5 h); the slopes of the corresponding trendlines are accordingly steeper at 100 MHz than at 400 MHz (k = −2.7 vs. −1.1 ms/% at 5 h). In the ADC measurements in Figure 3c, the dependence on the magnetic field strength is almost negligible, while the measurements show lower ADC values in older thrombi (after 24 h) than in fresh thrombi (after 5 h). This difference is approximately 0.2 × 10

^{−9}m

^{2}/s (Table 2). Such a dependence on the age of the thrombus can also be observed in the T

_{1}and T

_{2}measurements in Figure 3a,b. According to the linear regression parameters in Table 2, these differences are 120 ms and 110 ms for the T

_{1}measurements and 25 ms and 15 ms for the T

_{2}measurements at 100 MHz and 400 MHz, respectively.

#### 3.3. CT Measurements

#### 3.4. Regression and Statistical Analyses of NMR and CT Measurements

^{2}and by the chi-squared χ

^{2}. The latter is defined as the weighted sum of squared deviations (the squared difference between the measured and modeled values divided by the variance). The regression parameters k and n correspond to the trendlines presented in Figure 3 and Figure 5. Table 2 also contains the values of the parameter 100 × k/(50 × k + n), which correspond to the ratio between the difference between the final (100% HT) and the initial (0% HT) values of the trendline and their average. Since this parameter is dimensionless, it can be used to compare the extent of the relative difference of the measured parameter (T

_{1}, T

_{2}, ADC and CT number) over the entire HT range. The parameter with the largest such difference, i.e., with the highest 100 × k/(50 × k + n), can be considered the most sensitive to changes in the RBC thrombus in HT. As can be seen in Table 2, this parameter is the highest for the NMR parameter ADC for the older thrombi and for the fresh thrombi at 400 MHz (highlighted in green), it is relatively high for the NMR parameter T

_{2}at 400 MHz and for the CT number measured in the SE mode (highlighted in gold), and it is the lowest for the NMR parameter T

_{1}at 400 MHz (highlighted in red). R

^{2}values close to one or low χ

^{2}values indicate a good fit of the trendline to the measurement. For these measurements, such fits can be considered to be all of those where R

^{2}> 0.9 or χ

^{2}< 10.

## 4. Discussion

_{1}, T

_{2}, ADC and CT number) on HT using linear regression. Furthermore, the range of HTs from 0% to 100% was higher than that physiologically found in normal blood, i.e., around 40%. The use of a larger HT range can be justified; firstly, it increases the accuracy of the linear regression analysis, and, secondly, contracted thrombi may have HTs that are much higher than normal.

_{1}values show a significant negative linear dependence on HT for both MR systems and for all thrombi. This is due to the increasing content of paramagnetic iron ions in the RBC thrombi and the associated increased effect of T

_{1}NMR relaxation. Paramagnetic iron was present in hemoglobin in the blood, as we used deoxygenated blood (venous blood), where each hemoglobin group contains four or five unpaired electrons, making hemoglobin paramagnetic. Because of the unpaired electrons, paramagnetic hemoglobin has a magnetic moment, which, due to the thermal motion of the molecules, creates local oscillating fields that shorten the T

_{1}NMR relaxation time. The shortening of the T

_{1}relaxation time increases with increasing HTs due to the associated increased concentration of paramagnetic iron [23,24]. In addition to the effect of paramagnetic hemoglobin concertation, there is also an effect of the magnetic field strength on the T

_{1}NMR relaxation rate; namely, T

_{1}is longer in a stronger magnetic field than in a weaker one. In our measurements, the difference between the corresponding T

_{1}relaxation times on the 400 MHz MR system and on the 100 MHz system is in the range of 550 milliseconds (Table 1 and Table 2, and Figure 3a), which is consistent with the literature [25].

_{2}measurements have a relatively strong negative linear dependence on HT. This dependency occurs due to an increase in the surface-to-volume ratio with increasing HT, which results in increased surface-induced relaxation and, thus, a decrease in T

_{2}[26]. This decrease in T

_{2}occurs because, for a molecule near the surface compared to a molecule in the bulk, the surface molecule is under the influence of paramagnetic centers in the cell or differences in magnetic susceptibility between the cell wall and the plasma-filled extracellular space making the relaxation time faster. Our results show that the T

_{2}relaxation times measured on the 400 MHz MR system are on average four times shorter than those measured on the 100 MHz MR system (Table 1 and Table 2). This is because the effect of magnetic susceptibility is proportional to the strength of the magnetic field.

_{max}= 826 s/mm

^{2}, Δ = 20 ms and δ = 4 ms compared to b

_{max}= 893 s/mm

^{2}, Δ = 12 ms and δ = 2 ms for the 100 MHz and 400 MHz MR systems. The temporal parameter Δ, also known as the diffusion time, can have a great influence on the diffusion measurement of a porous system. For a porous system with pore diameter $a$, the measured diffusion coefficient would be equal to the unrestricted diffusion coefficient ${D}_{0}$ when Δ $\ll {a}^{2}/6{D}_{0}$, and it would decrease and level off to ${D}_{\infty}$ when Δ $\gg {a}^{2}/6{D}_{0}$, where the ratio ${D}_{0}/{D}_{\infty}$ is equal to the tortuosity of the porous medium [28,29]. For Δ values between these two extremes, the measured diffusion coefficient is between ${D}_{\infty}$ and ${D}_{0}$, and its value depends on the ratio of Δ to ${a}^{2}/6{D}_{0}$.

_{1}and T

_{2}values mostly at HTs above 50%. This result can be explained by the high lipid content of platelets and the fact that the T

_{1}and T

_{2}NMR relaxation times of lipid tissues are shorter than those of water-dominated tissues [30]. Negative HU values of platelet thrombi on CT measurements are again probably related to their high lipid content; namely, adipose tissues in humans have a HU between −205 and −51 [31]. While the HU values of our platelet thrombus models are in the negative range, their values are more negative than the minimal adipose tissue value in the literature. This may be due to a partial volume effect in the CT images because the samples were relatively small (2 mm in diameter). This result is promising, as we have demonstrated that CT can clearly differentiate between platelet and RBC thrombi and thrombi with high and low RBC contents. Among the NMR parameters, ADC is without such an overlap of values between RBC and platelet thrombi. In addition, it also has the best sensitivity among the NMR parameters to HT changes in RBC thrombi (parameter 100 × k/(50 × k + n) in Table 2). This result also agrees with our previous findings in a study where ADC and T

_{2}were used to monitor the progression of thrombolysis [32].

_{1}, T

_{2}and ADC, which are all sensitive to molecular changes, while CT is only sensitive to the density of imaged tissue. While this is true for in vitro measurements using high-resolution NMR/MRI systems, for in vivo measurements using clinical MRI scanners, current MR technology does not yet provide this precision. Therefore, currently, modern (dual-energy) CT scanners can still serve as a potentially useful tool in the analysis of thrombus structures if the protocol used allows for a sufficient spatial resolution and contrast.

## 5. Conclusions

## Author Contributions

## Funding

## Institutional Review Board Statement

## Informed Consent Statement

## Data Availability Statement

## Acknowledgments

## Conflicts of Interest

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**Figure 1.**Experiment workflow depicts collected blood sample processing, nuclear magnetic resonance (NMR) measurements and computed tomography (CT) imaging, processing of NMR and CT measurements and statistical analysis. Note that the first set of measurements for red blood cell (RBC) and pure plasma thrombus samples were carried out 5 h after the addition of thrombin, while the first set of measurements for pure platelet thrombus samples were carried out 30 min after they were formed to prevent the samples from drying out.

**Figure 2.**Graph depicts extruded serum and red blood cell (RBC) fraction as a function of hematocrit level (HT), along with a linear regression line showing a weak negative correlation between the two.

**Figure 3.**The graphs in panels (

**a**–

**c**) depict the dependence of measured nuclear magnetic resonance (NMR) T

_{1}, T

_{2}and apparent diffusion coefficient (ADC) parameters on thrombus type (red blood cell (RBC) vs. platelet) and on hematocrit level (HT) (for RBC thrombi only). Measured values for graphs shown with circles are taken from Table 1, while dashed trendlines are calculated using linear regression analysis. For each of the seven thrombus models (six RBC and one platelet), measurements were carried out for two time points (5 h and 24 h) and with two different NMR systems (100 MHz and 400 MHz).

**Figure 4.**Computed tomography (CT) images in dual-energy (80 kV) mode of all seven different thrombus models taken five hours after initiation of their clotting: platelet thrombus (

**a**), pure plasma thrombus (

**b**), 20% red blood cell (RBC) thrombus (

**c**), 40% RBC thrombus (

**d**), 60% RBC thrombus (

**e**), 80% RBC thrombus (

**f**) and 100% RBC thrombus (

**g**). In images (

**b**–

**g**), presented in the same Window Width (WW) and Window Center (WC), it is clearly seen how the image brightness increases with increasing HT. The platelet thrombus in image (

**a**) is displayed with different WW and WC, which is optimal for its presentation.

**Figure 5.**The graph depicts the dependence of computed tomography (CT) numbers on thrombus type (red blood cell (RBC) vs. platelet) and on hematocrit level (HT) (for RBC thrombi only). Measured values for graphs shown with circles are taken from Table 3, while dashed trendlines are calculated using linear regression analysis. For each of seven thrombus models (six RBC and one platelet), measurements were performed for two time points (5 h and 24 h) and with three different CT modes (DE 80 kV, DE 140 kV and SE 80 kV).

**Table 1.**Average values and standard deviations of T

_{1}, T

_{2}and apparent diffusion coefficient (ADC) measurements on both magnetic resonance (MR) systems (100 MHz and 400 MHz) for all thrombus models at both time points (5 h and 24 h). Overlaps in T

_{1}and T

_{2}values between platelet thrombi and red blood cell (RBC) thrombi are indicated in red.

MR System and Measurement Time | |||||
---|---|---|---|---|---|

100 MHz | 400 MHz | ||||

HT (%) | 5 h | 24 h | 5 h | 24 h | |

T_{1} (ms) | 0 | 2020 ± 100 | 2070 ± 80 | 2550 ± 70 | 2570 ± 100 |

20 | 1700 ± 180 | 1490 ± 110 | 2240 ± 200 | 2060 ± 80 | |

40 | 1560 ± 180 | 1310 ± 110 | 2070 ± 140 | 1880 ± 110 | |

60 | 1420 ± 130 | 1260 ± 190 | 1930 ± 170 | 1790 ± 180 | |

80 | 1350 ± 80 | 1250 ± 60 | 1850 ± 100 | 1780 ± 70 | |

100 | 1040 ± 70 | 1010 ± 60 | 1530 ± 110 | 1500 ± 140 | |

Platelet | 1570 ± 230 | 1210 ± 150 | 1780 ± 390 | 1390 ± 460 | |

T_{2} (ms) | 0 | 447 ± 31 | 442 ± 28 | 152 ± 8 | 149 ± 16 |

20 | 295 ± 58 | 264 ± 47 | 111 ± 32 | 92 ± 18 | |

40 | 254 ± 42 | 222 ± 43 | 100 ± 22 | 78 ± 18 | |

60 | 250 ± 29 | 202 ± 75 | 90 ± 15 | 77 ± 40 | |

80 | 229 ± 63 | 216 ± 67 | 75 ± 15 | 78 ± 34 | |

100 | 111 ± 13 | 105 ± 25 | 26 ± 5 | 27 ± 9 | |

Platelet | 232 ± 91 | 115 ± 38 | 89 ± 24 | 47 ± 16 | |

ADC (10^{−9} m^{2}/s) | 0 | 2.18 ± 0.32 | 2.07 ± 0.07 | 1.95 ± 0.04 | 1.98 ± 0.07 |

20 | 1.61 ± 0.24 | 1.47 ± 0.18 | 1.5 ± 0.21 | 1.27 ± 0.16 | |

40 | 1.51 ± 0.21 | 1.12 ± 0.21 | 1.42 ± 0.13 | 1.04 ± 0.2 | |

60 | 1.26 ± 0.11 | 1.02 ± 0.29 | 1.35 ± 0.11 | 0.97 ± 0.34 | |

80 | 1.19 ± 0.1 | 1.17 ± 0.25 | 1.17 ± 0.19 | 1.05 ± 0.17 | |

100 | 0.83 ± 0.13 | 0.87 ± 0.24 | 0.58 ± 0.1 | 0.49 ± 0.11 | |

Platelet | 0.22 ± 0.05 | 0.15 ± 0.04 | 1.24 ± 0.37 | 0.69 ± 0.4 |

**Table 2.**Linear regression analysis parameters of nuclear magnetic resonance (NMR) and computed tomography (CT) data for red blood cell (RBC) thrombi in Table 1 and Table 3, shown by slopes (k) and y-intercept (n) values. The goodness of fit between the trendline and the data is given by the coefficient of determination R

^{2}and the chi-squared χ

^{2}. In addition, the 100 × k/(50 × k + n) parameter corresponding to the sensitivity of the measured NMR or CT to HT is also shown for each trendline. Cells with high and higher sensitivity parameters are marked in green and gold, and those with low sensitivity are in red.

NMR | CT | |||||||||
---|---|---|---|---|---|---|---|---|---|---|

T_{1} | T_{2} | ADC | DE | SE | ||||||

100 MHz | 400 MHz | 100 MHz | 400 MHz | 100 MHz | 400 MHz | 80 kV | 140 kV | 80 kV | ||

5 h | Slope (k) | −8.7 $\frac{\mathrm{ms}}{\%}$ | −9.2 $\frac{\mathrm{ms}}{\%}$ | −2.7 $\frac{\mathrm{ms}}{\%}$ | −1.1 $\frac{\mathrm{ms}}{\%}$ | −0.012 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}\%}$ | −0.011 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}\%}$ | 0.44 $\frac{\mathrm{HU}}{\%}$ | 0.40 $\frac{\mathrm{HU}}{\%}$ | 0.61 $\frac{\mathrm{HU}}{\%}$ |

Intercept (n) | 1950 ms | 2490 ms | 400 ms | 145 ms | 2.0 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}}$ | 1.9 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}}$ | 37 HU | 30 HU | 28 HU | |

R^{2} | 0.96 | 0.96 | 0.85 | 0.92 | 0.93 | 0.89 | 0.86 | 0.90 | 0.97 | |

χ^{2} | 2.7 | 2.2 | 2.3 | 8.4 | 6.8 | 7.5 | 2.8 | 1.6 | 1.6 | |

100k/(50k + n) | −58% | −45% | −83% | −85% | −101% | −116% | 75% | 80% | 103% | |

24 h | Slope (k) | −8.7 $\frac{\mathrm{ms}}{\%}$ | −9.0 $\frac{\mathrm{ms}}{\%}$ | −2.6 $\frac{\mathrm{ms}}{\%}$ | −0.94 $\frac{\mathrm{ms}}{\%}$ | −0.010 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}\%}$ | −0.012 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}\%}$ | 0.38 $\frac{\mathrm{HU}}{\%}$ | 0.35 $\frac{\mathrm{HU}}{\%}$ | 0.56 $\frac{\mathrm{HU}}{\%}$ |

Intercept (n) | 1830 ms | 2380 ms | 375 ms | 130 ms | 1.8 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}}$ | 1.7 $\frac{{\mathsf{\mu}\mathrm{m}}^{2}}{\mathrm{ms}}$ | 48 HU | 40 HU | 37 HU | |

R^{2} | 0.80 | 0.86 | 0.79 | 0.79 | 0.75 | 0.80 | 0.62 | 0.65 | 0.72 | |

χ^{2} | 18.0 | 11.2 | 19.4 | 19.7 | 9.4 | 5.2 | 8.3 | 7.4 | 13.1 | |

100k/(50k + n) | −62% | −47% | −78% | −103% | −109% | −112% | 56% | 61% | 86% |

**Table 3.**Average values and standard deviations of computed tomography (CT) numbers in Hounsfield units (HUs) measured in dual energy (DE) (80 kV and 140 kV) and single energy (SE) (80 kV) modes of CT operation for all thrombus models at both time points (5 h and 24 h).

CT Mode and Measurement Time | ||||||
---|---|---|---|---|---|---|

DE | SE | |||||

80 kV (HU) | 140 kV (HU) | 80 kV (HU) | ||||

HT (%) | 5 h | 24 h | 5 h | 24 h | 5 h | 24 h |

0 | 32 ± 10 | 35 ± 7 | 25 ± 10 | 29 ± 7 | 24 ± 5 | 25 ± 4 |

20 | 48 ± 4 | 59 ± 9 | 42 ± 7 | 49 ± 6 | 43 ± 7 | 49 ± 10 |

40 | 51 ± 9 | 72 ± 14 | 44 ± 9 | 63 ± 16 | 54 ± 17 | 77 ± 21 |

60 | 74 ± 14 | 86 ± 11 | 61 ± 11 | 74 ± 9 | 71 ± 10 | 85 ± 18 |

80 | 73 ± 9 | 68 ± 13 | 63 ± 11 | 61 ± 9 | 74 ± 15 | 69 ± 13 |

100 | 74 ± 6 | 80 ± 4 | 66 ± 6 | 68 ± 4 | 87 ± 4 | 89 ± 7 |

Platelet | −197 ± 44 | −216 ± 117 | −238 ± 51 | −294 ± 172 | −260 ± 111 | −283 ± 116 |

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## Share and Cite

**MDPI and ACS Style**

Viltužnik, R.; Kaučič, A.; Blinc, A.; Vidmar, J.; Serša, I.
Comparing CT and MR Properties of Artificial Thrombi According to Their Composition. *Diagnostics* **2023**, *13*, 1802.
https://doi.org/10.3390/diagnostics13101802

**AMA Style**

Viltužnik R, Kaučič A, Blinc A, Vidmar J, Serša I.
Comparing CT and MR Properties of Artificial Thrombi According to Their Composition. *Diagnostics*. 2023; 13(10):1802.
https://doi.org/10.3390/diagnostics13101802

**Chicago/Turabian Style**

Viltužnik, Rebeka, Aleš Kaučič, Aleš Blinc, Jernej Vidmar, and Igor Serša.
2023. "Comparing CT and MR Properties of Artificial Thrombi According to Their Composition" *Diagnostics* 13, no. 10: 1802.
https://doi.org/10.3390/diagnostics13101802