Should the Small Intestine Be Avoided in Pelvic Intensity-Modulated Radiation Therapy?

doi:10.21203/rs.3.rs-952492/v1

Objectives. This study aimed to evaluate changes in small intestine position during whole pelvic intensity-modulated radiation therapy (IMRT) for patients with gynecologic malignancies using computed tomographic images during treatment and to investigate whether the small intestine should be avoided for delineation of pelvic lymph nodes in IMRT.

Methods. Thirty-one patients with gynecologic malignancies were included for pelvic radiotherapy and divided into two groups: surgical (n=15) and non-surgical (n=16). The 10th, 15th, and 20th fractions of the computed tomographic images were reviewed and changes in the intersection volume of the small intestine in the hot-spot areas compared to the initial planning scan were recorded.

Results. During radiotherapy, the proportion of overlapping area of intersecting volume in the hot-spot area, which included the left common iliac nodes, right common iliac nodes, left internal iliac nodes, right internal iliac nodes, left external iliac nodes, right external iliac nodes, left obturator nodes, right obturator nodes, and presacral nodes, was 16.52%, 28.05%, 18.65%, 37.16%, 39.18%, 49.67%, 23.74%, 50.07%, and 42.65%, respectively, for the non-surgical group, and 39.57%, 34.41%, 18.45%, 31.21%, 44.21%, 43.39%, 31.32%, 49.67%, and 27.59%, respectively, for the surgical group.

Conclusion. The proportion of the overlapping area of the intersecting volume accounted for 50% or less in patients, regardless of whether they had been operated on. Therefore, it is recommended that the small intestine, regardless of whether they had been operated on or not, does not need to be avoided for delineation of pelvic lymph nodes for gynecological malignancies (Clinical trial registration number: ChiCTR2100043240).

Oncology

Nuclear Medicine & Medical Imaging

Gynecologic malignancies

Intensity-modulated radiotherapy

Clinical target volume

Pelvic lymph nodes

Small intestine.

External beam radiation therapy (EBRT) is a common treatment for gynecologic malignancies, such as cervical, vaginal, and endometrial cancer. Intensity-modulated radiotherapy (IMRT) has emerged as an effective approach for EBRT. IMRT delivers radiation while minimizing doses to nearby organs at risk (OARs), such as the small intestine, bladder, rectum, and pelvic bone marrow [1–4]. Previous studies have shown IMRT has similar or lower rates of locoregional recurrences compared to three-dimensional conformal radiotherapy (3D-CRT), suggesting that IMRT is both safe and effective [5–8]. The lymph nodes are included in the radiation target volume when the tumor stage and grade indicate a significant risk of microscopic nodal metastases or if overt node involvement is already present.

However, a barrier to widespread implementation of IMRT for patients with pelvic malignancies is the absence of an objective description of lymph node locations in a three-dimensional (3D) space that can be easily used for radiation treatment planning. Conventional computed tomography (CT) and magnetic resonance (MR) cannot reliably detect small pelvic lymph nodes, whether normal or abnormal, and have low sensitivity for identifying metastases [9, 10]. Anatomic and embryologic studies [11] have shown the close developmental and spatial relationships between the lymphatics and vasculature, providing a basis for resolving this issue. The pelvic lymph nodes lie adjacent to major blood vessels [12], and the pelvic vessels are readily detected using contrast-enhanced CT or MR [13]. Previous studies have demonstrated that blood vessels with a modified 7-mm margin to be a good surrogate target for pelvic lymph nodes [14]. By making appropriate adjustments and excluding anatomical barriers, coverage of specific nodal groups may be increased, while the volume of normal tissue irradiated is decreased. The anatomical barriers include the small intestine, muscle, sacrum, and other internal organs. The small intestine is an athletic organ in the abdominal cavity, with only 20% of the small intestine staying in its original position during fractionated radiotherapy [15]. Furthermore, since the small intestine is the most important dose-limiting organ in radiotherapy for gynecologic malignancies, there is debate over whether the small intestine should be excluded from the pelvic nodal clinical target volume (CTV) in IMRT for gynecologic malignancies. According to Takafumi [16], the small intestine should not be excluded from the nodal CTV in cervical cancer. However, the Radiation Therapy Oncology Group (RTOG) recommended that the small intestine should be excluded [17].

In view of this, this study aimed to evaluate the changes in small intestine position during whole pelvic IMRT using CT images during treatment for patients with gynecologic malignancies, and investigate whether the small intestine should be avoided for delineation of pelvic lymph nodes in pelvic IMRT.

2.1 Patients

This study was approved by the ethics committee of Affiliated Hospital of Southwest Medical University. A total of 31 patients diagnosed with gynecologic malignancies who underwent IMRT concurrent with cisplatin chemotherapy were recruited from January to March 2021. Written informed consent was obtained from all patients.

2.2 Radiotherapy and imaging

Each patient underwent a CT scan with oral and intravenous contrast on an empty stomach before radiotherapy. The same device was attached to the same body position of all patients. Contiguous 5-mm slices were made from the 10th thoracic vertebra to 5 cm below the obturator. Patients were instructed to drink 1 L of water 30 minutes before the time of simulation and to empty their rectum. The baseline CT image before radiotherapy was defined as PLAN. Each patient underwent the same CT imaging method except for the oral and intravenous contrast at the 10th, 15th, and 20th fractions (patients were excluded if the treatment center was displaced >3 mm in any of the six directions: inferior, superior, left, right, anterior, or posterior). The follow-up CT images during radiotherapy were defined as N1, N2, and N3. In accordance with our treatment protocol, the patients were treated with IMRT, 45 Gy in 25 fractions of 1.8 Gy, irradiating the primary planning target volume (PTV), as well as the (elective) lymph nodes (PTV lymph nodes). All patients received concomitant weekly chemotherapy (40 mg/m² cisplatin intravenously).

2.3 Delineation

The PLAN, N1, N2, and N3 CT images were transmitted to the Pinnacle treatment planning system to contour the small intestine. The contouring method was generated based on the RTOG 2012 pelvic normal tissue contouring guidelines [18]. The bowel bag may provide a simpler and faster way of contouring the bowel, especially in the absence of small intestine contrast. A correctly contoured bowel bag will encompass all the small intestine and colon contours. A lymph node CTV was contoured on the PLAN CT image by creating a 7-mm expansion in the common, internal, or external iliac artery. The obturator and presacral lymph nodes CTV were contoured according to the RTOG guidelines [19]. Delineation of the small intestine and pelvic lymph nodes CTV was performed and verified by the same experienced physician. A lymph node CTV on the PLAN CT image was marked as a hot-spot area. There were nine hot-spot areas for each patient: left common iliac nodes, right common iliac nodes, left internal iliac nodes, right internal iliac nodes,left external iliac nodes, right external iliac nodes, left obturator nodes, right obturator nodes, and presacral nodes. To compare the locations of the small intestine, follow-up CT images taken during IMRT were fused with the baseline CT image by matching the fiducial markers, which were attached to the patient's skin surface in the central plan image. Automatic image registration was performed between baseline CT and follow-up CT using a method based on mutual information in the Pinnacle planning system. The automatically registered image was checked by an experienced radiologist. The volume changes of the small intestine in hot-spot areas during whole pelvic IMRT treatment were observed using CT images (Fig. 1).

2.4 Data Collection

2.4.1 The daily changes in shape and position of the small intestine can be quite complex. As a result, describing changes in the small intestine position is not straightforward. This study aimed to evaluate changes in small intestine position and investigate whether the small intestine should be avoided for delineation of pelvic lymph nodes during treatment. Therefore, a relatively simple and pragmatic approach was selected to analyze the changes. In the hot-spot area during radiotherapy, p∩n represents the overlapping area of the small intestine intersecting, while (p∩n)/p represents the proportion of the overlapping area of the small intestine intersecting volume (Fig. 2).

2.4.2 In order to observe the volume change of the small intestine and intestinal motion amplitude in the irradiation field, it was necessary to determine the small intestine volume change rate (volume change rate ΔV = (V1 -V2)/V1) and the spatial repetition volume ratio which can be expressed as (V1∩V2)/V1, where V1 and V2 were the volume of the small intestine on baseline CT and follow-up CT, respectively. The acute gastrointestinal toxicities of patients during radiotherapy were evaluated according to the RTOG criteria.

2.5 Statistical Analysis

The SPSS v.25.0 software package was used for statistical analysis. Descriptive statistical analysis was used to determine the proportion of the overlapping area of intersecting volume. The Wilcoxon test was applied to compare the volume change rate, spatial repetition volume ratio, and gastrointestinal toxicities between the two groups.

3.1 Basic characteristics of patients

The staging was performed according to the International Federation of Gynecology and Obstetrics (FIGO) classification. A total of 31 patients were enrolled: twenty-seven with cervical squamous carcinoma (stage IB1∼IVB), two with endometrial adenocarcinoma (stage II∼IIIC), one with vulvar squamous carcinoma (stage IB), and one with vaginal squamous carcinoma (stage II). The patients had a median age of 52 years (range 29-79 years). The basic characteristics are shown in Table 1.

Table 1

Basic characteristics of patients enrolled in the group
Disease	Cases	Hysterectomy	Non-hysterectomy
Cervical cancer	27	13	14
Endometrial cancer	2	2	0
Vulvar cancer	1	0	1
Vaginal cancer	1	0	1
Total	31	15	16

3.2 The proportion of the overlapping area of the small intestine intersecting volume in the hot-spot area during radiotherapy.

During radiotherapy, the volume of the small intestine entering the irradiation field ranged from 727.87 to 903.71 cc. The results showed that there was no significant difference in the proportion of the overlapping area of intersecting volume in each hot spot area between the surgical and non-surgical groups (Table 2). The median of the proportion of overlapping area of intersecting volume in the hot-spot area, which included the left common iliac nodes, right common iliac nodes, left internal iliac nodes, right internal iliac nodes, left external iliac nodes, right external iliac nodes, left obturator nodes, right obturator nodes, and presacral nodes, was 16.52%, 28.05%, 18.65%, 37.16%, 39.18%, 49.67%, 23.74%, 50.07%, and 42.65%, respectively, for the non-surgical group, and 39.57%, 34.41%, 18.45%, 31.21%, 44.21%, 43.39%, 31.32%, 49.67%, and 27.59%, respectively, for the surgical group (Fig. 3). In the surgical group, there was a significant difference in the proportion of the overlapping area of the small intestine intersecting volume between the internal and external iliac hot-spot areas (P=0.022). However, in the non-surgical group, there was a significant difference in the proportion of the overlapping area of the small intestine intersecting volume between the common and external iliac hot-spot areas (P=0.006).

Table 2

The proportion of the overlapping area of the small intestine intersecting volume
Hot-spot areas	Surgical group (%)	Non-surgical group (%)	P-value
Left common lliac artery	39.57(0.88-60.43)	16.52(0-40.00)	0.075
Right common lliac artery	34.41(11.08-45.64)	28.05(3.50-54.09)	0.51
Left internal lliac artery	18.45(2.81-45.15)	18.65(0-51.91)	0.68
Right internal lliac artery	31.21(10.31-56.01)	37.16(14.74-68.52)	0.58
Left external lliac artery	44.21(20.00-60.40)	39.18(11.27-58.47)	0.44
Right external lliac artery	43.39(24.99-66.39)	49.67(27.61-66.54)	0.72
Left obturator	31.32(1.79-60.31)	23.74(9.63--60.50)	0.85
Right obturator	49.67(27.15-65.17)	50.07(8.34-100.00)	0.59
Presacral	27.59(9.59-49.08)	42.65(12.00-66.98)	0.11
Note: data are median (range).

3.3 The volume change rate in the small intestine

The rate of volume change in the small intestine is displayed in Table 3. The volume change rate in the operated group was not significantly different from the non-operated group. In addition, there was no significant difference in the volume change rate in the small intestine at the 10th, 15th, and 20th fractions in both the operated and non-operated groups.

Table 3

The volume change rate in the small intestine during radiotherapy
Fractions	Surgical group (%)	Non-surgical group (%)
10th	11.99(3.07-27.09)	18.92(5.45-37.93)
15th	18.40(5.65-24.42)	17.17(7.96-23.25)
20th	26.56(8.63-33.02)	8.31(5.52-21.33)
Note: data are median (range).

3.4 The spatial repetition volume ratio in the small intestine

Table 4 displays the spatial repetition volume ratio in the small intestine of the two groups. The spatial repetition volume ratio during radiotherapy was significantly larger in the operated group than the non-operated group (P=0.001). There was no significant difference in the spatial repetition volume ratio in the small intestine at the 10th, 15th, and 20th fractions in both the operated and non-operated groups.

Table 4

The spatial repetition volume ratio of the small intestine during radiotherapy
Fractions	Surgical group (%)	Non-surgical group (%)
10th	73.16(57.54-77.69)	57.51(55.69-74.11)
15th	62.86(56.86-73.27)	58.49(48.32-67.41)
20th	66.46(58.03-76.27)	52.83(48.98-56.52)
Note: data are median (range).

3.5 Acute gastrointestinal toxicities

The most common acute gastrointestinal toxicities in patients include nausea, vomiting, and diarrhea. There was no acute grade ≥III gastrointestinal toxicity in the non-operated and operated groups, and no patients discontinued treatment due to intolerable toxicity effects (Table 5). There was no significant difference in the occurrence of acute gastrointestinal toxicities between the two groups.

Table 5

Acute gastrointestinal toxicities during radiotherapy
Group	RTOG scoring of gastrointestinal toxicities(N/%)
Group	Grade I	Grade II	Grade III	Grade IV
Surgical group	6(37.50)	6(37.50)	0	0
Non-surgical group	6(40.00)	6(40.00)	0	0

Over the last two decades, radiation therapy for gynecologic malignancies has evolved with the advent of IMRT. Therefore, it is important to define and standardize radiation therapy target volumes accurately. Furthermore, improving the accuracy of IMRT is required to account for the effect of organ motion during radiotherapy. Although all guidelines recommend excluding bone and muscle from the pelvic nodal CTV [20], there has been debate on whether the pelvic nodal CTV in IMRT for gynecologic malignancies should avoid the small intestine. The small intestine is not generally excluded from any gynecologic malignancies guidelines, except for the RTOG guidelines [17]. This is because the RTOG guidelines are for postoperative cases of cervical and endometrial cancers, where the small intestine falls into the pelvis postoperatively and its location is relatively fixed. Therefore, the small intestine is excluded from the pelvic nodal CTV to reduce normal tissue toxicity.

All other guidelines for delineation of pelvic lymph nodes for gynecologic malignancies do not exclude the small intestine because the daily changes in shape and position of the small intestine can be quite complex [15], making it very difficult to predict specific organ motion in patients [21]. In addition, when delineating pelvic lymph nodes for rectal cancer [22], it is not recommended to avoid the small intestine when the small intestine is in the pelvic nodal CTV. The main reason is to account for changes in the position of the small intestine during fractionated radiotherapy. However, the consensus is that the pelvic nodal CTV is required to routinely avoid the small intestine in prostate cancer [23]. Those guidelines that do not recommend avoiding the small intestine for the pelvic nodal CTV in IMRT simply state that the small intestine is prone to motility without providing any evidence.

In this study, the volume change rate of the small intestine during radiotherapy was not significantly different between the surgical and non-surgical groups, based on the motion study of the small intestine during radiotherapy. However, the spatial repetition volume ratio of the small intestine in the non-surgical group was smaller than the surgical group (P=0.001). This indicated that the small intestine fell into the pelvic cavity after hysterectomy, as well as postoperative interbowel adhesions, led to a certain degree of reduced intestinal motility. This study aimed to determine whether the small intestine needs to be avoided for delineation of pelvic lymph nodes in IMRT for gynecologic malignancies.

Firstly, the changes in the intersection volume of the small intestine in hot-spot areas were compared to the initial planning scan. The results showed that there was no significant difference in the proportion of the overlapping area of intersecting volume in each hot spot area between the surgical and non-surgical groups. This indicated that intestinal motility was not differentially diminished in the surgical group compared to the non-surgical group within the pelvic nodal CTV. In addition, the results revealed that the internal iliac hot-spot area had greater intestinal motility than the external iliac hot-spot area in the surgical group (P=0.022). However, in the non-surgical group, the external iliac hot-spot area had greater intestinal motility than the common iliac hot-spot area (P=0.006). Finally, the median of the proportion of the overlapping area of intersecting volume in each hot-spot area was calculated. If (p ∩ n)/p ≤ 50%, we recommend that avoiding the small intestine is unnecessary due to the increased intestinal motility in this case. When there is a large small intestine motion, excluding it from the pelvic nodal CTV may sacrifice too much of the target volumes. In the non-surgical group, the proportion of the overlapping area of the intersecting volume was 50.07% in the right obturator hot-spot area, which was around 50%. Thus, it is suggested that the small intestine should not be avoided in this case.

In conclusion, the proportion of the overlapping area of intersecting volume accounts for 50% or less in patients, regardless of whether they were operated on or not. Therefore, it is recommended that the small intestine should not be avoided for delineation of pelvic lymph nodes for gynecological malignancies. In this study, although radiotherapists did not exclude the small intestine from the pelvic nodal CTV in both the operated and non-operated groups, there was no significant difference in acute gastrointestinal toxicity during radiotherapy between the two groups and was well tolerated by the patients.

Previous studies have described intestinal motion during radiation; however, ours is the first to analyze changes in small intestine volume in the pelvic nodal CTV for gynecologic malignancies throughout a treatment. There are several limitations to the present study. First, although patients were repeatedly instructed to fill their bladders and empty their rectum before simulation and treatment, it was all based on the patients' subjective degree of perceptions. Organ motion due to bladder fill has been extensively studied [24, 25]. However, there were no objective instruments used to assess bladder and rectal volumes, which may not have achieved the same state as during positioning and may have affected intestinal motility. Furthermore, the patients in the surgical group referred to cases that underwent a hysterectomy, but their surgical procedures differed, which may have affected the accuracy of grouping. Finally, this study had a small sample size that prevented more precise grouping, which could be examined further in the future by increasing the sample size and controlling more factors that affect intestinal motility.

In order to address the question of whether the small intestine should be avoided for delineation of pelvic lymph nodes in pelvic IMRT for patients with gynecologic malignancies, it was discovered that the proportion of the overlapping area of intersecting volume accounted for 50% or less in patients, regardless of whether they were operated or not. Therefore, it is recommended that the small intestine does not need to be avoided for the delineation of pelvic lymph nodes for gynecological malignancies, regardless of whether they were operated on or not.

IMRT

Intensity-modulated radiation therapy

EBRT

External beam radiation therapy

OARs

Organs at risk

3D-CRT

Three-dimensional conformal radiotherapy

3D

Three-dimensional

CT

Computed tomography

MR

Magnetic resonance

CTV

Clinical target volume

RTOG

Radiation Therapy Oncology Group

PTV

Planning target volume

FIGO

International Federation of Gynecology and Obstetrics.

Acknowledgements

None.

Author contributions

Study concept and design: Rong Huang, Dan Li, Qinglian Wen, Jingbo Wu.

Provision of materials or patients: Qinglian Wen, Rong Huang, Dan Li, Tian Liu.

Acquisition of data: Tian Liu, Haowen Pang, Zhenhua Zhang, Xiuju Du

Analysis and interpretation of data: Rong Huang, Qinglian Wen, Dan Li.

Manuscript writing: Rong Huang, Dan Li, Qinglian Wen, Tian Liu.

Critical review of the manuscript: All authors.

Final approval of manuscript: All authors.

Funding

None.

Availability of data and materials

Not applicable.

Ethics approval and consent to participate

This study was approved by the ethics committee of Affiliated Hospital of Southwest Medical University. Written informed consent was obtained from all patients.

Consent for publication

All authors gave consent for the publication.

Competing interests

The authors declare that they have no competing interest

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Should the Small Intestine Be Avoided in Pelvic Intensity-Modulated Radiation Therapy?

Status:

Version 1

Abstract

Figures

1 Introduction

2 Methods

2.1 Patients

2.2 Radiotherapy and imaging

2.3 Delineation

2.4 Data Collection

2.5 Statistical Analysis

3 Results

3.1 Basic characteristics of patients

3.3 The volume change rate in the small intestine

3.4 The spatial repetition volume ratio in the small intestine

3.5 Acute gastrointestinal toxicities

4 Discussion

Abbreviations

Declarations

References

Status:

Version 1