Demonstration of quasi-real-time intrafractional motion in esophageal cancer radiotherapy provided by ExacTrac X-ray snap verification

Abstract

OBJECTIVE:

To investigate the following hypotheses: (1) ExacTrac X-ray Snap Verification (ET-SV) is an alternative to CBCT for positioning patients with esophageal carcinoma (EC), (2) ET-SV can detect displacement in EC patients during radiotherapy (RT) and (3) EC patients can be feasibly monitored in quasi-real-time with ET-SV during RT.

METHODS:

Anthropomorphic phantoms and 13 patients were included in this study. CBCT and ET-SV were both implemented before treatment delivery to detect displacement, and their correction results were compared. For the patient tests, positional correction in 3 translational directions and the yaw direction were applied using the ET-SV correction results. The residual error was detected immediately using ET-SV. Finally, to acquire the intrafractional motion, ET-SV was implemented when the gantry was at 0°, 90°, 180° and 270°, respectively.

RESULTS:

In phantom tests, the maximum value of the difference in displacement between the CBCT and ET systems was 1.16 mm for translation and 0.31° for yaw. According to Bland–Altman analysis of the patient test results, 5% (5/98), 5% (5/98), 5% (5/98), and 4% (4/98) of points were beyond the upper and lower limits of agreement in the AP, SI, LR and yaw directions, respectively. The mean residual error was –0.482 mm, 1.215 mm, 1.0 mm, –0.487°, 0.105°, and 0.003° in the AP, SI, LR, pitch, roll and yaw directions, respectively. The intrafractional displacement ranged from –0.21 mm to 0 mm for translation and from –0.63° to 0.21° for rotation. The mean total translational error for intrafractional motion increased from 0.47 mm to 1.14 mm during the treatment.

CONCLUSION:

The accuracy of ET-SV for EC RT positional correction is comparable to that of CBCT. Thus, Quasi-real-time intrafractional monitoring can be used to detect EC patient displacement during radiotherapy.

Keywords

Quasi-real-time monitoring esophageal cancer ExacTrac X-ray Snap

1 Introduction

Esophageal cancer (EC) ranks seventh in terms of incidence (572,000 new cases) and sixth in terms of overall mortality (509,000 deaths), and it is common in several Eastern and Southern African countries [1], while in China, EC is the fourth leading cause of cancer-related deaths [2]. Radiotherapy (RT) is a major part of the treatment strategy established by multidisciplinary teams (MDTs) for patients diagnosed with EC. However, the tumors are located within and near sensitive normal structures, and both day-to-day baseline shifts and respiration induce motion of the primary tumor and lymph nodes relative to the bony anatomy. Additionally, anatomical changes occur frequently, and involuntary patient movement is common. When the observed target motion exceeds a certain threshold, the treatment should be interrupted, and a couch shift should be performed to realign the target with the radiation beam. Therefore, the implementation of image guidance and real-time tracking during RT for EC is necessary.

There are several typical image-guided radiation therapy (IGRT) systems, including electronic portal imaging devices (EPIDs) and kilovoltage (kV) or megavoltage (MV) cone-beam computed tomography (CBCT), fan-beam CT, ultrasound, magnetic resonance imaging (MRI), electromagnetic tracking, optical surface imaging, optical imaging and 2D KV radiographic imaging combination systems. CBCT is the most commonly used image guidance technique [3 –8] because of the sufficient quality of its volumetric imaging [9]. Ultrasound and MRI provide good soft tissue visualization, but the geometric accuracy of ultrasound is lower than that of other IGRT systems. CBCT, EPID, and fan-beam CT systems are radiation-based systems, producing average doses per image of 30–50, 1–3, and 10–30 mGy, respectively [10]. Electromagnetic tracking systems and optical surface imaging systems are nonradiation based and capable of real-time intrafractional motion monitoring during RT. However, the implantation of transponders in electromagnetic tracking systems is invasive and unacceptable for many patients. Furthermore, the application of optical surface imaging systems is limited by the assumption that the external surface is a good surrogate for the internal position.

Takayuki et al. [11] found that respiratory motion is the main source of esophageal motion. Cardiac motion was also detected in the frequency analysis, but its magnitude was much smaller than that of respiratory motion [11]. In some situations, patients experienced pain or fatigue or coughed at the end of treatment, probably because of the long radiation fractions [12]. This can lead to a reduction in the accuracy of RT to different degrees.

The ExacTrac Snap Verification (ET-SV) System (BrainLab, Germany) is a tool that offers easy setup control and quasi-real-time monitoring of patient position during radiation. This combination system is composed of an infrared-based optical positioning system and a kV X-ray imaging system, enabling precise imaging and verification of patient intrafractional motion [13]. ET-SV has a short image acquisition and registration time and a low radiation dose, ranging from 0.33–0.55 mGy [10]. Given the high-quality images it produces at low X-ray doses, previous studies have found that the ET-SV tool provides precise verification not only for patients with brain [13], head and neck [14], or lung cancer [12, 15] or spinal metastasis [16] but also of the target from the beginning to the end of each fraction. However, no studies have yet examined IGRT in EC using ET-SV.

In this prospective study, we investigated the following hypotheses: I, ET-SV is an alternative to CBCT for positioning patients with EC; II, it can detect displacement in EC patients during RT; and III, it allows the feasible, quasi-real-time monitoring of EC patients during RT. To the best of our knowledge, this is the first experimental study to evaluate the quasi-real-time monitoring ability of ET-SV for the esophagus. This study may provide new evidence for implementing quasi-real-time monitoring during RT for EC using ET-SV.

2 Methods and Materials

2.1 Image-guided systems

All experiments were performed at the Varian Clinac iX Linear Accelerator (Varian Medical Systems, Inc., Palo Alto, CA) using anthropomorphic phantoms and patient datasets. In this research, an OBI system and BrainLab ET-SV equipped on a linear accelerator were used to implement IGRT. The OBI system is composed of a kV X-ray source and an amorphous silicon detector. After registration of the CBCT images and the planning CT images, 4-degree-of-freedom (DOF) deviations of patient position, including 3 translational directions and 1 rotational direction, can be obtained.

BrainLab ET enables the monitoring of a patient’s position after the patient has been positioned for treatment. The system is separate from the linear accelerator, so the verification image can be obtained at any time during the treatment. The ET system, using the 2D X-ray system, includes 2 in-room-mounted oblique X-ray tubes and 2 detectors. When correcting the patient’s position, two exposure images need to be captured using a snap verification operation. However, at some specific angles, the X-ray system is blocked by the linear accelerator gantry, and so only one verification image is visible at this time; in such cases, IGRT is not available for the ET system. To obtain 2 images for judging the positional error more accurately, we positioned the linear accelerator gantry at approximately 0°, 90°, 180° and 270° to obtain verification images with the ET-SV. Finally, two oblique, high-quality X-ray images were acquired for the patient and fused to the digitally reconstructed radiographs (DRRs) obtained from the corresponding planning CT. Six-dimensional (6D) offsets, including 3 translational and 3 rotational offsets, were generated after determining the best match [17].

2.2 Phantom tests

To simulate a real radiotherapy environment for esophageal cancer, two different sets of markers were pasted into the anthropomorphic phantom (Alderson Rando phantom, Alderson Research Laboratories, Inc.) to simulate the isocenters of different plans for EC patients (Fig. 1). CT scans of the anthropomorphic phantom were acquired using a Philips CT scanner (Holland, CT Lightspeed 16) with a voltage of 120 kV, tube current of 200 mA, and slice thickness of 3 mm. The CT images were exported to the Eclipse clinical treatment planning system (TPS, version 13.6, Varian Medical Systems, Inc., Palo Alto, CA). Two clinical EC plans for two different isocenters were superimposed on the phantom images.

Fig. 1

Phantom with two sets of markers. Each set of markers was used to generate a plan to approximately simulate the isocenters of different plans for patients with EC.

The phantom was scanned using CBCT in half-fan mode, and the 4-DOF calibration deviations were obtained after image registration. Then, two oblique X-ray snap verification images were acquired using the ET system. To obtain the 6D shift, these two images were registered with the planning DRRs. We introduced different levels of known positional error (1 mm, 4 mm, 6 mm, and 20 mm for translation and 2° for yaw) from the isocenter to simulate the patient positioning procedure and repeated these scanning procedures four times.

2.3 Patient tests

Thirteen patients who underwent RT for EC at our hospital were randomly selected. All patients were undergoing their first RT session and had no history of RT. The patients signed informed consent forms, and the study was approved by the ethics committee of our institution. The CT scan parameters for the patients were identical to those for the above phantom. The patients were positioned supine on the CT table and immobilized with a thermoplastic mask extended to the shoulders. A 6- to 7-field intensity-modulated radiotherapy (IMRT) plan was generated for each patient on the Varian Eclipse TPS. The planning isocenters for 5 and 8 patients were set at the locations of marker 1 and marker 2 on the phantom, respectively.

The patient setup and IGRT workflow are shown in Fig. 2. The CBCT correction results were considered the ‘gold standard’ and compared with ET-SV correction results were. First, patients were scanned with CBCT in the half-fan mode. Then, ET-SV was performed for each patient followed by CBCT scanning. Bone registration was used for both CBCT and ET to determine the displacement. Subsequently, we evaluated the consistency of the displacement determined by the CBCT and ET systems. The positions were corrected in the 3 translational directions and the yaw direction using the ET-SV correction results. The residual error was immediately detected using ET-SV and denoted ET1. Finally, to acquire the intrafractional motion, ET-SV was implemented when the gantry was positioned at 0°, 90°, 180° and 270°, and the error was denoted ET2, ET3, ET4, and ET5, respectively. As bone registration is feasible and currently widely used for esophageal RT setups [18], it was applied here for both CBCT and ET-SV.

Fig. 2

Patient setup and IGRT workflow.

2.4 Data analysis

In this work, the displacement measured by CBCT and ET was calculated using the mean, standard deviation (SD), and root mean square (RMS). The Bland–Altman method was used to assess the agreement between CBCT and ET. Box plots were used to show the intrafractional displacement distribution, in which displacement is depicted as a vector with a direction. The total translational setup error was obtained by using $D (t) = \sqrt{x {(t)}^{2} + y {(t)}^{2} + z {(t)}^{2}}$ for the intrafractional setup error, where D(t) is the magnitude of displacement, and x(t), y(t), and z(t) are the displacements in each of the 3 orthogonal directions.

Then, the paired Student’s t tests were used to compare the differences between the CBCT and ET correction results. All analyses were performed using SPSS version 22.0 (SPSS, Chicago, IL, USA). P < 0.05 was considered significant.

3 Results

3.1 Phantom test results

A total of 8 pairs of CBCT and ET scans were acquired. The differences in the correctional displacement between the two systems shown in Table 1. The maximum difference in displacement between the CBCT and ET systems was 1.16 mm for translation and 0.31° for yaw. The RMS of the difference in the correction displacement between the CBCT and ET systems was less than 1 mm for translation and less than 0.5° for yaw.

Table 1
Differences in correction setup between CBCT and ET for two different positions determined by two sets of phantom markers

Displacement direction Differences between ET and CBCT (n = 8)

Marker 1 Marker 2

Mean SD RMS Mean SD RMS

Translation (mm)

AP –0.018 0.583 0.505 –0.403 0.260 0.461

SI 0.228 0.385 0.403 0.755 0.398 0.830

LR –0.748 0.331 0.801 –0.79 0.316 0.836

Rotation (degree)

Yaw –0.108 0.167 0.180 0.073 0.178 0.171

Displacement direction	Differences between ET and CBCT (n = 8)
Translation (mm)
AP	–0.018	0.583	0.505	–0.403	0.260	0.461
SI	0.228	0.385	0.403	0.755	0.398	0.830
LR	–0.748	0.331	0.801	–0.79	0.316	0.836
Rotation (degree)
Yaw	–0.108	0.167	0.180	0.073	0.178	0.171

3.2 Patient test results

From July 2019 through November 2019, a total of 13 EC patients from our hospital were enrolled in this study. The baseline characteristics of the patients are shown in Table 2. A total of 9 were male and 4 were female, ranging in age from 46 to 81 years (median: 67 years; mean±SD: 66.2±9.2 years) and in weight from 39 to 70 kg (median: 56 kg; mean±SD: 55.1±8.6 kg). All plans were designed by the multifield IMRT technique. The plan isocenters were selected at marker 1 or marker 2, in line with the phantom as the target location.

Table 2
Baseline patient characteristics

Patient Number Sex Age (years) Weight (kg) KPS score PTV volume (cm³) TNM Stage Dose (Gy)/fractions Radiotherapy technology Isocenter position

1 Male 56 45 80 370 T3N2M1 1.8/33 8-field IMRT Marker 1

2 Male 75 70 90 289 T3N0M0 1.8/28 5-field IMRT Marker 2

3 Female 68 53 90 462 T3N1M1 2.0/31 7-fields IMRT Marker 2

4 Male 77 56 90 219 T3N0M1 2.0/30 7-field IMRT Marker 2

5 Male 81 61 80 84 T3N0M0 1.8/33 6-field IMRT Marker 2

6 Male 62 49 60 326 T3N1M1 1.8/33 8-field IMRT Marker 1

7 Female 46 47 90 428 T3N2M0 2.0/29 7-field IMRT Marker 1

8 Male 64 63 90 105 T3N2M0 2.0/29 5-field IMRT Marker 1

9 Male 71 60 80 216 T3N0M0 2.2/28 5-field IMRT Marker 2

10 Female 67 39 90 260 T3N0M0 1.8/28 7-field IMRT Marker 1

11 Female 70 61 90 348 T1N1M0 1.8/33 7-field IMRT Marker 1

12 Male 62 52 80 302 T3N2M1 2.0/30 10-fields IMRT Marker 2

13 Male 62 60 80 272 T2N1M0 1.8/23 5-field IMRT Marker 2

Patient Number	Sex	Age (years)	Weight (kg)	KPS score	PTV volume (cm³)	TNM Stage	Dose (Gy)/fractions	Radiotherapy technology	Isocenter position
1	Male	56	45	80	370	T3N2M1	1.8/33	8-field IMRT	Marker 1
2	Male	75	70	90	289	T3N0M0	1.8/28	5-field IMRT	Marker 2
3	Female	68	53	90	462	T3N1M1	2.0/31	7-fields IMRT	Marker 2
4	Male	77	56	90	219	T3N0M1	2.0/30	7-field IMRT	Marker 2
5	Male	81	61	80	84	T3N0M0	1.8/33	6-field IMRT	Marker 2
6	Male	62	49	60	326	T3N1M1	1.8/33	8-field IMRT	Marker 1
7	Female	46	47	90	428	T3N2M0	2.0/29	7-field IMRT	Marker 1
8	Male	64	63	90	105	T3N2M0	2.0/29	5-field IMRT	Marker 1
9	Male	71	60	80	216	T3N0M0	2.2/28	5-field IMRT	Marker 2
10	Female	67	39	90	260	T3N0M0	1.8/28	7-field IMRT	Marker 1
11	Female	70	61	90	348	T1N1M0	1.8/33	7-field IMRT	Marker 1
12	Male	62	52	80	302	T3N2M1	2.0/30	10-fields IMRT	Marker 2
13	Male	62	60	80	272	T2N1M0	1.8/23	5-field IMRT	Marker 2

Figure 3 shows the planning CT, CBCT, DRR and ET images for one patient. The ET system provided a clear image of the bony structure. By performing bone registration, we achieved better alignment whether we compared the planning CT to the CBCT images or the DRR to the ET images.

Fig. 3

Representative image registration steps for a single patient: (a) planning CT, CBCT and matched images; (b) digitally reconstructed radiographs (DRRs), ET-SV and matched images.

A total of 98 pairs of setup error values measured by CBCT and ET were acquired from the 13 EC patients. Table 3 shows the displacement between CBCT and ET for the patients in the 3 translational and 3 rotational directions, and Fig. 4 shows the consistency between the CBCT and ET correction results. The percentage of points beyond the upper and lower limits of agreement (LOA) was 5% (5/98), 5% (5/98), 5% (5/98), and 4% (4/98) in the anterior-posterior (AP), superior-inferior (SI), and left-right (LR) directions and around the AP direction (yaw), respectively. The differences between the two groups were not statistically significant.

Table 3

Setup errors and differences between CBCT and ET for the patients (N = 13, n = 98)

Displacement direction	Setup errors for CBCT(ET)
	Range	Mean	SD	RMS
Translation(mm)
AP	–8.00∼8.00 (–8.79∼8.66)	0.172(–0.339)	3.482(3.547)	3.469(3.545)
SI	–12.00∼23.00 (–11.47∼24.00)	1.031(1.349)	4.828(4.802)	4.913(4.964)
LR	–6.00∼18.00 (–6.86∼20.21)	1.459(0.985)	3.582(3.667)	3.851(3.779)
Rotation(degree)
Pitch	N/A (–2.96∼1.24)	N/A (–0.556)	N/A (0.907)	N/A (1.060)
Roll	N/A (–2.24∼2.21)	N/A (0.107)	N/A (0.925)	N/A (0.926)
Yaw	–2.70∼2.40 (–2.78∼2.32)	–0.191(–0.009)	0.857(0.958)	0.874(0.954)

Fig. 4

Consistency in the displacement between CBCT and ET: (a) translation in the anterior-posterior (AP) direction, (b) translation in the superior-inferior (SI) direction, (c) translation in the left-right (LR) direction, and (d) rotation in the AP direction (yaw).

A total of 115 pairs of ET and ET1 (to show the residual error) images were obtained in this study for patient testing. Table 4 shows the range, mean, SD, and RMS of the ET and ET1 displacements. The residual errors were very small after performing the ET-SV operation.

Table 4

Range, Mean, SD, and RMS of the setup errors of ET and ET1.

Displacement direction	Setup errors (mm) ET (ET1)
	Range	Mean	SD	RMS
Translation (mm)
AP	–8.79∼8.66 (–0.86∼0.54)	–0.482 (–0.075)	3.356 (0.220)	3.376 (0.232)
SI	–11.47∼24.00 (–0.58∼1.09)	1.215 (0.008)	4.580 (0.250)	4.719 (0.249)
LR	–6.86∼12.95 (–1.83∼1.48)	1.000 (–0.104)	3.378 (0.466)	3.508 (0.476)
Rotation (degree)
Pitch	–2.96∼1.68 (–2.79∼2.06)	–0.487 (–0.525)	0.872 (0.883)	0.996 (1.024)
Roll	–2.24∼2.21 (–1.85∼2.42)	0.105 (0.165)	0.872 (0.893)	0.874 (0.905)
Yaw	(–3.47∼2.32) (–1.27∼1.02)	0.003 (0.006)	1.005 (0.314)	1.001 (0.312)

We acquired 102 sets of intrafractional motion data measured by ET, which are plotted in Fig. 5. The mean error ranged from –0.21 mm to 0 mm in translation and from –0.63° to 0.21° in rotation.

Fig. 5

Intrafractional quasi-real-time displacement monitoring using ET.

Figure 6 shows the total translational error for intrafractional motion. The mean displacement increased from 0.47 mm to 1.14 mm throughout the treatment, while the interquartile range (IQR) increased from 0.38 mm to 1.12 mm.

Fig. 6

Box plots of the modulus of the vector for intrafractional displacement.

4 Discussion

RT for EC involves large geometric uncertainties due to setup error, positional variation in the esophageal target volume, and organ motion. In addition, as the dose per fraction increases, the duration of treatment may be prolonged, so the probability of intrafractional esophageal motion is greater than with conventional treatment. To overcome these shortcomings, IGRT was created to reduce these geometric uncertainties by acquiring anatomical images of the patient before or during treatment and comparing them with the planning images. Upon detecting target motion exceeding the threshold, the treatment should be interrupted, and a couch shift should be performed to realign the target with the radiation beam.

Unlike other IGRT methods, the ET system enables the quasi-real-time monitoring of changes in the patient’s body position and serves as a convenient method for measuring residual shifts. ET involves a low radiation dose, approximately one percent of the radiation dose of CBCT. Another advantage of ET-SV is that it measures and processes the target position using only the information available at the time of interrogation, with a time delay of less than 0.5 seconds, for monitoring organ movement. Therefore, the positional errors can be corrected in a timely manner.

The ET system has been applied for position verification in head and neck, brain, and lung cancers, especially for patients undergoing stereotactic treatment. However, few studies on EC patients have been reported. In this study, we first report the feasibility and accuracy of quasi-real-time intrafractional verification in RT for EC with ET-SV. We first compared the positional error of ET and CBCT using a phantom. Then, we tested the agreement between ET and CBCT in 13 EC patients. Finally, we successfully implemented quasi-real-time intrafractional monitoring for these patients. The phantom experimental data showed that the RMS of the difference between ET and CBCT was less than 1 mm in the linear direction and less than 1° in the rotational direction, as was the case for the patient validation results. The error after using ET correction was significantly smaller than that before ET correction, and the RMS of the pendulum error was reduced by 3 to 4.5 mm in the linear direction and by 0.7° in the rotational direction. The total intrafractional error indicates that the patient’s displacement increased over time, although the changes in the individual directions were not significant. In summary, we found that ET and CBCT demonstrate consistent positional correction capabilities. Encouragingly, we also found that the ET system has a strong ability to correct residual error in EC.

There are other aspects of value in this study. For example, pain, cough, and increasing doses per fraction may reduce the precision of RT for EC. Our research may address inaccurate dose delivery due to the above problems. On the other hand, reducing the target margin depends on the imaging frequency to some extent. The implementation of quasi-real-time monitoring with ET-SV in RT for EC could potentially reduce the outer boundaries of the target and reduce toxicity to normal organs. This assumption should be confirmed in future studies.

This study also has some limitations. First, the patient dataset of this study is limited. To address this issue, we first examined the phantom data and then increased the number of times that ET-SV was implemented for each patient as much as possible. Second, although 6D error can be detected using ET-SV, only 4D correction was performed, as this is the maximum supported by the CBCT system.

5 Conclusion

The accuracy of ET-SV for positional correction in RT for EC is comparable to that of CBCT. ET-SV can be used to safely and reliably monitor displacement in EC patients in clinical practice. Quasi-real-time intrafractional monitoring can detect EC patient displacement during RT.

Footnotes

Acknowledgments

The authors have no relevant conflicts of interest to disclose.

This research was partly supported by the National Nature Science Foundation of China (No. 81901743, No. 82001902 and No. 82172072), the Natural Science Foundation of Shandong Province (No. ZR2020QH198 and ZR2020LZL001).

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