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British Journal of Radiology (2006) 79, 766-773
© 2006 British Institute of Radiology
doi: 10.1259/bjr/98024704
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full paper

Breast movement during normal and deep breathing, respiratory training and set up errors: implications for external beam partial breast irradiation

S Chopra, MD, DNB1, K A Dinshaw, DMRT, FRCR1, R Kamble, MSc1 and R Sarin, MD, FRCR2

1 Radiation Oncology, Tata Memorial Hospital, Mumbai, Maharashtra, 2 ACTREC, Kharghar, NaviMumbai, Maharashtra, India

Correspondence: Prof. Rajiv Sarin, Director, ACTREC, Tata Memorial Centre, Kharghar, NaviMumbai, Maharashtra, India


   Abstract
Top
 Abstract
Introduction
 Methods and materials
 Observations and results
 Discussion
 Conclusions
 References
 
This study was designed to evaluate interfraction and intrafraction breast movement and to study the effect of respiratory training on respiratory indices. Five patients were immobilized in supine position in a vacuum bag and three-dimensional set up errors, respiratory movement of the breast during normal and deep breathing, tidal volume and breath hold time were recorded. All patients underwent respiratory training and all the respiratory indices were re-evaluated at the end of training. Cumulative maximum movement error (CMME) was calculated by adding directional maximum set up error and maximum post training movement during normal breathing. The mean set up deviation was 1.3 mm (SD ± 0.5 mm), 1.3 mm (SD ± 0.3 mm) and 4.4 mm (SD ± 2.6 mm) in the mediolateral, superoinferior and anteroposterior dimensions. Pre-training mean of the maximum marker movement during normal breathing was 1.07 mm, 1.94 mm and 1.86 mm in the mediolateral, superoinferior and anteroposterior dimensions. During deep breathing these values were 2 mm, 5.5 mm and 4.8 mm. While respiratory training had negligible effect on breast movement during normal breathing, it resulted in a modest reduction during deep breathing (p = 0.2). The mean CMME recorded for these patients was 3.4 mm, 4.5 mm and 7.1 mm in the mediolateral, superoinferior and anteroposterior dimension. Respiratory training also resulted in an increase in breath hold time from a mean of 31 s to 44 s (p = 0.04) and tidal volume from a mean of 560 cm3 to 1160 cm3 (p = 0.04). With patients immobilized in the vacuum bag the CMMEs are relatively less. Individualized directional margins may aid in reduction of planning target volume (PTV).


   Introduction
Top
 Abstract
 Introduction
Methods and materials
 Observations and results
 Discussion
 Conclusions
 References
 
Accelerated partial breast irradiation (APBI) is presently the focus of research in radiotherapy for early breast cancer (EBC) [1]. In addition to interstitial brachytherapy, three-dimensional conformal radiation therapy (3DCRT) and intensity-modulated radiation therapy (IMRT) are currently being evaluated for APBI in this group of patients [1–5]. For successful implementation of these high precision techniques both intrafraction and interfraction movements of the breast have to be considered. Efforts have been made to decrease respiratory movement by the use of active breathing control (ABC), respiration correlated cone beam CT (RC-CBCT), real time tumour tracking and helical tomotherapy while implementing 3DCRT for APBI [6–10].

While efforts are being made to incorporate image guidance for precise localization of planning target volume (PTV) for APBI, there is a paucity of data regarding cumulative positional uncertainties due to intrafraction respiratory movement and interfraction-re-positioning errors with different positioning devices in patients with breast cancer. This study was designed with the aim:

  1. To ascertain intrafraction respiratory movement of the breast.
  2. To evaluate interfraction movement of breast clinical target volume (CTV) by studying the re-positioning set up errors with individualized vacuum cast immobilization.
  3. To evaluate the possible efficacy of respiratory training in reducing breast movement for the purpose of external beam APBI with 3DCRT and IMRT.
  4. To devise guidelines for CTV to PTV margins based on cumulative maximum movement error (CMME) combining intrafraction or interfraction maximum respiratory motion during normal breathing and maximum re-positioning set up errors.


   Methods and materials
Top
 Abstract
 Introduction
 Methods and materials
Observations and results
 Discussion
 Conclusions
 References
 
Five patients with EBC who had undergone breast conservative surgery at our institution and were potentially eligible for APBI as per standard eligibility criteria for APBI [1] were included in this study. Patients with restricted arm movements after surgery and pre-existing respiratory problems were excluded. Written informed consent was obtained from all the patients. While these women participated in this investigational study for respiratory movements and set up errors during positioning for APBI, they were treated with the standard radiotherapy protocol of our department. The standard treatment included 5 weeks of daily whole breast radiotherapy with bitangential portals with 6 MV photons on an inclined breast board followed by an en face electron boost. For the purpose of this study, the women underwent a separate process of evaluation of set up errors for which they were immobilized in an individualized body cast (vacuum bag). Baseline movements during normal and deep breathing, breath hold time and tidal volume were evaluated for all the women. Breath hold time and tidal volume were measured on a daily basis during the course of respiratory training. After a short course of 8–10 days of respiratory training, breast movement during normal and deep breathing was re-evaluated.

Immobilization and surface markers
Patients were immobilized in individualized body casts made of a polyurethane bag filled with tiny polystyrene pellets, which sets according to the body shape upon application of vacuum. Patients were positioned in the body cast in supine position with arms above the head without using the breast board. The lumpectomy cavity was localized and outlined on the breast surface using the information from pre-operative clinical description, mammography films, intraoperative findings and lumpectomy scar. With an additional margin of 1.5 cm in the x and y dimensions the CTV was delineated on the patient's surface. Lead markers (2 mm diameter) were placed at the centre of each of the four borders of the outlined CTV and at the centre of the CTV (Figure 1Go). For the purpose of the study it was assumed that the movement of these five markers on the anterior surface of the CTV would represent the movement of the entire CTV.


Figure 1
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  		Figure 1. Localization of clinical target volume(CTV) on the breast surface with lead markers.

 
Interfraction movement: re-positioning set up errors
After carefully positioning a patient in the customized body cast on the simulator (Ximavision 2.1®; Varian Medical Systems, Palo Alto, CA), a field size of 10 cm x 10 cm was centred on the CTV at a target to skin distance of 95 cm. Using an isocentric technique, orthogonal anterior and lateral images were acquired. Patients were instructed to hold their breath after deep inspiration during image acquisition. This served as a baseline image against which set up reproducibility was evaluated. After the baseline image acquisition patients were then taken off the couch and re-positioned four times at different time intervals on the same day and orthogonal images were repeated. For each patient, four pairs of orthogonal films were compared against the baseline orthogonal pair of films. On each of these films, the perpendicular distance between the centre of each spherical marker and the nearest delineator wire or the central crosswire of the simulator was measured using an inbuilt measuring scale with an accuracy of 0.1 mm. The differences between the measurements in the baseline and subsequent films were recorded for each of these markers in the mediolateral, superoinferior and anteroposterior dimensions. Internal surgical titanium clips demarcating the tumour bed were present in one patient. However, the visualization of these titanium clips was poor in orthogonal films and not suitable for evaluation of tumour bed movement.

Systematic error ({sum}), defined as the variation between the planned position and average position on re-positioning, was calculated as the average value of the mean deviation of each patient. Random errors ({sigma}) defined as fraction to fraction variations around the mean deviation were calculated as the average of the standard deviation around the mean [11].

Intrafraction movement: respiratory movement of breast
Baseline evaluation of respiratory movements was carried out in normal as well as deep breathing, using the cine-acquisition mode of Ximavision®. Orthogonal cine-fluoroscopic images were acquired at the rate of two images per second with the gantry at 0° and 90° (or 270°). At the end of image acquisition, cine recordings were available for each patient and the orthogonal image sets could be used for evaluation of movement in mediolateral, superoinferior and anteroposterior dimensions. A total of 80 images (40 orthogonal images in normal breathing and 40 orthogonal images in deep breathing) were available per patient. For the purpose of measurement or tracking of movements of breast markers during respiration, the projection of the field delineator and the central cross wires were considered as a stationary structure against which the position of individual markers was measured in serial cine images acquired during the respiratory cycle. On each of these images, the perpendicular distance between the marker and the nearest delineator wire or central crosswire of the simulator was measured as for set-up errors. Differences between the measurements in the baseline and subsequent images were recorded for each of these markers for ascertaining the breast movement in the mediolateral, superoinferior and anteroposterior direction during a few respiratory cycles.

Respiratory training
After baseline assessment of respiratory movement, all patients were given a short course of respiratory training for a period of 8–10 days. Patients were trained by an occupational therapist (RK). Deep breathing exercises, including inspiratory and expiratory manoeuvres and forced abdominal expiration technique, were taught to all the patients. A spirometer was used on a daily basis for training. Patients carried out all these exercises for 15–20 min once daily under the supervision of the occupational therapist and repeated them at least twice daily without the instructor. Breath holding time and tidal volume were recorded before starting respiratory training. While patients received respiratory training daily breath hold time and tidal volume were noted. Detailed cine-fluoroscopic evaluation of breast movement as described above was done before starting the respiratory training and repeated once after completion of respiratory training. Any reduction in the movement of the skin markers during respiration, increase in the tidal volume or breath holding time was used as an end point to evaluate the efficacy of short course respiratory training. The Wilcoxon Sign rank test was used to evaluate the statistical significance of observed differences.


   Observations and results
Top
 Abstract
 Introduction
 Methods and materials
 Observations and results
Discussion
 Conclusions
 References
 
Re-positioning errors using the customized vacuum bag were evaluated in the mediolateral, superoinferior and anteroposterior dimensions for all patients. Cranial, anterior and right sided deviations were recorded in the positive direction whereas caudal, posterior and left sided deviations were recorded in the negative direction. The details of the set up errors on re-positioning are shown in Table 1Go. The mean deviations for all markers from their baseline positions were 1.3 mm (SD ± 0.5 mm) in the mediolateral; 1.3 mm (SD ± 0.3 mm) in the superoinferior and 4.4 mm (SD ± 2.6 mm) in the anteroposterior dimension. Rotational errors were not calculated.


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  		Table 1. Set up variation and cumulative set up errors in mediolateral, superoinferior and anteroposterior dimensions with the use of individualized body cast

 
Breast movement, as judged by five surface markers, was minimal during normal breathing with pre-training mean marker movement of 1.07 mm (0.6–1.4 mm); 1.94 mm (0.7–4.5 mm) and 1.86 mm (0.6–1.9 mm) in the mediolateral, superoinferior and anteroposterior directions, respectively, during normal breathing. The breast movements during normal breathing were not affected by respiratory training (Table 2Go).


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  		Table 2. Maximum movement during normal breathing in anteroposterior, mediolateral and superoinferior dimension before and after respiratory training

 
As expected, the marker movement was more pronounced during deep breathing with mean values of 2 mm (1–3.4 mm), 5.5 mm (1.4–8.2 mm) and 4.8 mm (1.7–9 mm) in the mediolateral, superoinferior and anteroposterior directions, respectively (Table 3Go). Respiratory training produced a non-significant reduction of movement of marker in mediolateral, superoinferior and anteroposterior directions during deep breathing.


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  		Table 3. Maximum movement of breast in anteroposterior, mediolateral and superoinferior dimension during deep breathing before and after respiratory training

 
After training the breath hold time increased from a pre-training mean of 31 s to a mean of 44 s (p = 0.04). The tidal volume increased in all the patients from an average of 560 cm3 in the pre-training phase to 1160 cm3 in the post-training phase (p = 0.04) (Table 4Go, Figures 2Go and 3Go).


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  		Table 4. Pre- and post-respiratory training breath hold time and tidal volume

 

Figure 2
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  		Figure 2. Box whisker plot showing variation of breath hold time during respiratory training over 1 week(BH 1–7 = breath hold time day 1–7). y-axis: breath hold time in seconds; x-axis: breath hold time over 1 week of respiratory training; N = number of patients.

 

Figure 3
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  		Figure 3. Box whisker plot showing the variation in tidal volume during respiratory training over 1 week.(Tidal 1–7 = tidal volume from day 1–7). y-axis: tidal volume in millilitres; x-axis: tidal volume over 1 week of respiratory training; N = number of patients.

 
CTV to PTV margins based on cumulative maximum movement error
For determining the CTV to PTV margin for each study patient, we derived the CMME by combining the maximum intrafraction movement as judged by cine-fluoroscopic assessment of breast respiratory motion during normal breathing and maximum interfraction re-positioning set up errors obtained in these test conditions (Table 5Go). The CMME did not exceed 10 mm for any of these patients in any of the axes. The mean of the CMME recorded for these 5 patients was 3.4 mm (range 2.3–4.3 mm), 4.5 mm (range 2.5–7.8 mm) and 7.1 mm (range 3.9–9.9 mm) in the mediolateral, superoinferior and anteroposterior dimensions, respectively.


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  		Table 5. Measured cumulative maximum movement error(CMME in mm) combining maximum respiratory motion in normal breathing after respiratory training and maximum set up errors

 

   Discussion
Top
 Abstract
 Introduction
 Methods and materials
 Observations and results
 Discussion
Conclusions
 References
 
While several studies have previously evaluated set up errors in women undergoing daily breast radiotherapy [12–17], this is probably the first study in which both the interfraction (re-positioning set up errors) and intrafraction (respiratory) components of variability in CTV localization have been ascertained individually for each study patient. Our findings confirm that re-positioning set up errors and respiratory movements both contribute to the total uncertainty. The maximum interfraction and intrafraction movement readings have been combined to derive the cumulative maximum movement error for each patient. In our opinion, this represents a simple and perhaps more accurate and safe method of deriving the CTV to PTV margin for individual patients.

In this study instead of relying on the surgical clips, which are usually placed on the posterior surface of the lumpectomy cavity, we have evaluated respiratory movements by skin surface markers representing the anterior surface of the CTV. We feel that it is reasonable to assume that the movement of the breast surface represents movement of the CTV, except in patients with large pendulous breasts where surface markers may not be so reliable for representing the underlying CTV. As we observed in one patient, titanium surgical clips are not visualized well in all projections that are required for assessing set up errors and respiratory movements, especially in the true lateral projection. Moreover, it has been reported that the surgical clips may be displaced by up to 3 mm (range 0–11 mm) [18] especially if they are not anchored to the muscle. Other authors have described using bony or soft tissue reference points for measuring set up errors or respiratory movements [15–17]. In our opinion, none of the soft tissue or bony reference points in this region are so well defined that they can be reliably and accurately localized in all projections in serial imaging.

Interfraction movement: re-positioning set up errors
Previous studies have measured re-positioning set up errors using bony or soft tissue reference points [12–17] during a 5–6 week course of daily radiotherapy. In contrast, we have ascertained the set up errors by re-positioning the patients five times during the same day and by using skin markers. While our approach of re-positioning assessments over 1 day may not reflect time trends in set up variation over 5 weeks [19–21] it has certain other advantages. Most importantly, it removes the confounding variability in the placement of markers or problems in precisely localizing the same reference point in the thoracic bony cage or soft tissues in serial orthogonal films. For abbreviated treatment like APBI which is delivered over 5 days, time trends if any, are likely to be much less than that observed over a treatment course of 35 days [21]. Assessment over 1 day allows the use of individualized decision regarding CTV to PTV margins, the benefits of which are discussed later.

The set up errors with this individualized body cast immobilization were quite small under these test conditions, except in the anteroposterior direction (Table 1Go). However, we have not compared the re-positioning set up errors without body cast. Similar findings have been reported by other groups using various immobilization devices [12–15]. Nalder [12] et al evaluated set up reproducibility for breast radiotherapy using a breast board with and without a Vacfix device (PAR Scientific A/S, Denmark). They noted reduction in set up errors in the superoinferior direction using the Vacfix device. Giraud et al [22] have demonstrated that a personalized body cast leads to a significant reduction in lung apex movements along with reduction in lateral displacement of the thoracic cage.

Vicini et al [4] have used vacuum bags for immobilization for APBI and 5 mm margin has been incorporated for re-positioning errors.

Intrafraction movement: respiratory movement of breast
Ideally the entire treatment period should be continuously monitored and orthogonal images should be acquired simultaneously for assessing intrafraction motions. However, for reasons of logistics and in order to minimize radiation exposure to the opposite breast with lateral beams, we used cine-fluoroscopic assessment of breast motion for only 10 s. Since the beam on time for each radiation field of APBI using 3DCRT is usually in the range of 20–30 s, this 10 s assessment may therefore be a reasonable representation of intrafraction movement.

The findings of our study confirm that respiratory movements during normal breathing are negligible (<2 mm) and may be ignored for conventional whole breast treatment, whereas deep breathing could cause significant intrafraction error. However, respiratory motion even during normal breathing merits special consideration when planning external beam APBI using 3DCRT or IMRT and even for tangential whole breast treatment if using IMRT. With IMRT, not only the CTV is moving with respiration but the lack of synchrony between respiratory motion and the dynamic sliding multileaf collimator could result in perturbation in radiation dose delivery [23].

Hence for IMRT, respiratory movements are a matter of concern even for whole breast irradiation. Other authors have evaluated movements of the breast in various dimensions with varying respiratory patterns ranging from no breathing to deep breathing and reported 2–16 mm, 2–6 mm and 2–16 mm movement in the mediolateral, superoinferior and anteroposterior dimensions, respectively, and documented that the best reproducibility was achieved when patients were asked to hold their breath [23, 24]. In our study we recorded baseline average movement of less than 2 mm in mediolateral, superoinferior and anteroposterior dimensions during normal breathing. At the William Beaumont Hospital, ABC was used in the initial few patients undergoing external beam APBI [3, 6]. However, ABC is not used currently for APBI and a generic margin of 10 mm is being incorporated (5 mm for set up errors and 5 mm for breathing movements) for CTV to PTV generation. Formenti et al [2, 5] have treated patients with APBI in prone position with the aim of reducing breathing movements. However, up to 1 cm allowance has to be incorporated for enhanced set up errors in this position. Improved accuracy, both in re-positioning and minimizing target motion, has recently been reported with the incorporation of video based surface registration, optoelectronic surface registration and RC-CBCT [8–10]. This may further aid in reducing CTV to PTV expansion, but limited access to these devices may limit its wider applicability.

Although there was only minimal impact of the short course of respiratory training in reducing breast movements, the tidal volume and breath hold time increased appreciably in all the patients. The post-training mean breath hold time was 44 s as compared with 12–16 s in untrained patients as reported by other studies [25]. This paradox of increased tidal volume with similar or reduced thoracic movement may be explained by an increase in the diaphragmatic component of breathing. However, this was not specifically measured in the present study. Increasing the diaphragmatic component of respiration and increased breath hold time may have two implications in thoracic radiotherapy. First, respiratory training imparted in this fashion has the possibility of exacerbating lung movements, especially of the lower lobe. Hence, the impact of respiratory exercises, which are sometimes imparted to patients with lung cancer in order to improve their pulmonary functions, should be studied with special reference to their impact on respiratory lung movement during shallow or normal breathing. Movements during deep breathing are irrelevant since it is unlikely that any clinical context would require delivering radiotherapy during continuous deep breathing. Second, such short course respiratory training could help deep inspiration breath hold (DIBH) assisted treatment of thoracic or abdominal tumours by increasing the breath hold time, thereby shortening the treatment delivery time and possibly improving accuracy in treatment delivery.

CTV to PTV margins
In the literature, there are several recommendations for deriving the CTV to PTV margins [11, 26]. Using a mathematical notation and assuming that the distribution of set up errors is gaussian, Stroom et al have recommended that a safety margin of 2.0{sum} + 0.7{sigma} should be incorporated where {Sigma} and {sigma} are as previously defined [11]. The criteria for this recommendation are based on an assumption that 99% of the CTV would be covered by 95% of the prescribed dose. While this recommendation has been favoured by other investigators [27] we feel that there are two caveats with this recommendation. First, set up errors may not always have a normal or gaussian distribution as seen in our data as well as in other studies [28, 29]. Second, such values of systematic and random errors and the CTV to PTV margins based on these formulae are derived for a particular study population and then recommended to be used for generating the CTV to PTV margin for individual patients. The present study as well as other investigators [30] have shown that there could be significant patient to patient variation both in the magnitude and vector of the mean or maximum set up error. For highly conformal radiation plans that are delivered in very abbreviated schedules, such as APBI over 5 days or highly hypofractionated schedules such as extracranial body frame stereotaxy [31, 32] use of generic values of CTV to PTV margins may result in under coverage or an inappropriately large margin for a substantial part of the treatment. For such highly abbreviated or hypofractionated schedules, the maximum re-positioning set up error measured over repeated re-positioning on a single day along with the measured respiratory movements can be incorporated in the initial individualized CTV to PTV generation algorithm. This would ensure the use of minimum yet safe CTV to PTV margins and in patients where the margins thus obtained are unacceptably large, the process of immobilization may be repeated or changed or the patient may be given special instruction. Finally, the appropriateness of these margins could be further validated with online portal imaging and if necessary online or offline correction [7].


   Conclusions
Top
 Abstract
 Introduction
 Methods and materials
 Observations and results
 Discussion
 Conclusions
References
 
Interfraction re-positioning set up errors and intrafraction respiratory movement of the breast contribute to total uncertainty in irradiating the intended CTV. Moreover, there are significant interindividual differences in the maximum values of interfraction and intrafraction movement errors. With the use of individualized vacuum bag fixation and individually ascertained values for set up errors and respiratory movements on a single day it is possible to use tight CTV to PTV margins for external beam APBI delivered during normal breathing. It is unlikely that more advanced techniques such as ABC, real time tumour tracking and image guided radiotherapy would result in "clinically significant" reduction in the CTV to PTV margin for APBI over and above what is achieved by the technique described here. Although not of much use for APBI, by increasing the breath hold time, a short course of respiratory training may be useful for patients undergoing DIBH for intrathoracic or abdominal tumours.

Received for publication January 11, 2006. Revision received March 25, 2006. Accepted for publication March 27, 2006.


   References
Top
 Abstract
 Introduction
 Methods and materials
 Observations and results
 Discussion
 Conclusions
 References
 

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