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Gastrointestinal Imaging
February 2004

High-Resolution MRI of the Anatomy Important in Total Mesorectal Excision of the Rectum

Abstract

OBJECTIVE. The surgical removal of a rectal carcinoma and the adjacent lymph nodes in an en bloc package lessens the risk of local recurrence due to residual tumor. Heightened awareness of good surgical techniques has created much interest in the anatomy involved in total mesorectal excision surgery, with particular focus on the fascial planes and nerve plexuses and their relationship to the surgical planes of excision. Clear preoperative depiction of these relationships is of value in determining tumor resectability. The aim of this study was to describe the radiologic appearance of these anatomic structures.
SUBJECTS AND METHODS. High-spatial-resolution T2-weighted MRI was performed using a 1.5-T system in cadaveric sections and in patients before they underwent total mesorectal excision surgery. Anatomic dissections of sagitally sectioned hemipelves were compared with MRIs obtained in vivo to establish criteria for visualization of the structures relevant to anterior resection of the rectum.
RESULTS. High-spatial-resolution MRI depicted a number of structures of importance in total mesorectal excision surgery. The mesorectal fascia, which forms the boundary of the surgical excision plane in total mesorectal excision, was identified, and the presacral fascia, peritoneal reflection, and Denonvilliers' fascia were also shown. Structures 1–2 mm in diameter were visualized because the contrast resolution afforded by T2-weighted fast spin-echo imaging permitted depiction of the inferior hypogastric nerve plexus and the fascial planes within the posterior pelvis.
CONCLUSION. Anatomic landmarks important to the performance of rectal cancer surgery, in particular the mesorectal fascia, may be defined on MRI and are of potential importance in the staging of tumors, assessing resectability, planning surgery, and selecting patients for preoperative neoadjuvant therapy.

Introduction

Over the past 20 years, the anatomy of the pelvis has been reevaluated as evidence has grown for the benefits of careful anatomic dissection in rectal cancer surgery. Emphasis is now placed on excising the rectum and mesorectum within its enveloping fascia as a completely intact “monobloc.” This complete removal of the tumor-containing rectum and its draining lymph nodes as a distinct anatomic package is the essence of total mesorectal excision [1] and has resulted in reduced local recurrence rates [2], leading to the widespread acceptance of total mesorectal excision in the management of rectal cancer.
The proximal dissection involves dividing the inferior mesenteric artery close to its origin and mobilizing the vascular pedicle of the sigmoid mesocolon, while carefully preserving the superior hypogastric nerve plexus. The dissection then continues in the relatively avascular areolar tissue plane posterior to the mesorectum, thereby separating the visceral fascia on the surface of the mesorectum from the presacral parietal fascia. As the dissection proceeds inferiorly, the variable rectosacral fascia is divided at the level of the fourth sacral vertebra. The lateral surfaces of the mesorectum are then dissected, separating the mesorectal fascia from the parietal fascia of the pelvic sidewall while preserving the hypogastric nerves and the inferior hypogastric plexus. Further lateral dissection separates the mesorectum from the neurovascular bundles that run forward and medially toward the urogenital structures. The anterior dissection divides the peritoneum anteriorly relative to the rectovesical (in males) or rectovaginal (in females) pouches. The dissection continues in front of Denonvilliers' fascia, posteriorly relative to the seminal vesicles and the prostate gland in the male. In the female, there is a corresponding, but thinner, rectovaginal septum. Thus, the total mesorectal excision specimen comprises the rectum surrounded by a complete mesorectum containing draining lymph nodes within an intact mesorectal fascial envelope with a smooth glistening surface and including Denonvilliers' fascia anteriorly. Preservation of the intact superior and inferior hypogastric plexuses and hypogastric nerves safeguards sexual and bladder function.
Preoperative knowledge of the precise extent of tumor spread in relation to anatomic structures is of critical importance in planning surgery. Furthermore, because this information is used to determine the use of preoperative therapy, surgical planning itself may be altered. The aim of our study, therefore, was to compare axial MRIs of the cadaveric pelvis with axial histologic sections of the same cadaver and to compare MRIs of selected patients obtained before they underwent total mesorectal excision surgery with whole-mount histologic sections obtained after surgery. In addition, anatomic dissections of sagittally sectioned hemipelves were compared with MRIs obtained in vivo to establish criteria for visualization of the structures relevant to anterior resection of the rectum.

Subjects and Methods

This study was performed according to a protocol approved by the relevant ethics committees, and informed consent was obtained from each patient. In addition, the institutional ethics committee approved the protocol for imaging and correlation using MRI and histopathology of two human cadaveric subjects. Thin-section MRI was performed using a 1.5-T system (Horizon Advantage, software version 5.62, General Electric Medical Systems, Milwaukee, WI). For cadaveric sections, T2-weighted fast spin-echo images were obtained with the following parameters: TR/TE, 4,000/85; 24-cm field of view; 3-mm slice thickness; no interslice gap; 512 × 384 matrix; echo-train length, 8; no fat saturation; 32-kHz bandwidth; and six acquisitions. For the in vivo imaging, we used the same parameters with the exception of field of view (16 cm), matrix (256 × 256), and number of acquisitions (four).
Axial whole-mount histologic sections were obtained from a cadaveric pelvis. Thin axial slices were fixed in formalin and decalcified in 5% hydrochloric acid solution for 6 weeks. Histologic sections were cut and stained with H and E, so that the whole of the mesorectum and surrounding structures could be mounted onto large glass slides. These were then compared with corresponding high-resolution MRIs obtained in the cadaver. Anatomic landmarks visualized on total mesorectal excision whole-mount sections were compared with in vivo MRIs. In addition, cadaveric pelvic hemisections dissected in the parasagittal plane to show the nerve plexuses were compared with in vivo sagittal high-resolution MRIs of the pelvis.

Results

The Parietal Fascia

The muscles of the pelvic walls (piriformis, levator ani, coccygeus, and obturator internus) are covered by the parietal fascia that fuses with the sacral periosteum toward the midline. Anteriorly, the fascia attaches to the back of the body of the pubis. On the sidewall of the pelvis, the parietal fascia is thickened on the surface of the obturator internus muscle where it forms the obturator fascia. On MRI, the parietal fascia appears isointense relative to signal intensity of muscle and is not seen as a separate structure except anterolaterally, where it appears as a separate layer overlying the obturator internus muscle (Fig. 1).
Fig. 1. In vivo axial T2-weighted image shows parietal fascia in 78-year-old man with adenocarcinoma. Anterolaterally, fascia (arrows) is seen as separate low-signal-intensity layer overlying obturator internus muscle.

The Retrorectal Space

When the rectum in the sagittally hemisected cadaveric pelvis is pulled forward, the retrorectal space is clearly visible (Fig. 2A). This space is limited posteriorly by the presacral parietal fascia and anteriorly by the mesorectal fascia. The presacral fascia is shown on sagittal MRI as a low-signal-intensity linear structure overlying the presacral vessels (Fig. 2B). The mesorectal fascia is seen immediately anterior to this structure, and the potential space between these two fascial layers forms the retrorectal space. In two patients, abnormal collections of fluid had accumulated in the retrorectal space as a result of the perforation of the rectum (Fig. 3).
Fig. 2A. Pelvis and retrorectal space. Photograph of hemisected cadaveric pelvis shows retrorectal space (arrowhead), which is limited anteriorly by mesorectal fascia (arrow).
Fig. 2B. Pelvis and retrorectal space. Sagittal T2-weighted fast spin-echo image obtained in 68-year-old man with recrtal adenocarcinoma shows posterior fascial layers of pelvis. Visceral mesorectal fascia (long solid arrow) is lying anterior to presacral fascia (short solid arrow). High signal deep relative to presacral fascia (arrowhead) represents fat, and signal void of median sacral vessel (open arrow) lies in retrorectal space.
Fig. 3. Sagittal T2-weighted fast spin-echo image obtained in 55-year-old woman with rectal carcinoma shows perforation of rectal tumor. High-signal-intensity fluid is seen in retrorectal space (white arrow). Presacral fascia (black arrow) forms posterior wall of fluid collection.

The Rectosacral Fascia

At examination of cadaveric specimens, we found the rectosacral fascia (Fig. 4A) to be a fascial band of variable thickness running from the sacrum to the mesorectal fascia at the level of the fourth sacral vertebra that could be visualized on MRI (Fig. 4B).
Fig. 4A. Rectosacral fascia. Photograph of sagittal cadaveric hemisected pelvis shows rectosacral fascia (arrow) running obliquely from sacrum to posterior wall of rectum.
Fig. 4B. Rectosacral fascia. In vivo T2-weighted fast spin-echo image of pelvis in 67-year-old man with rectal adenocarcinoma reveals oblique low-signal-intensity band (arrows) extending from junction of S3 and S4 vertebrae to posterior wall of rectum that represents rectosacral fascia.

The Peritoneal Reflection

From the uppermost part of the posterior surface of the bladder, the peritoneum extends posteriorly to the junction of the upper two thirds and lower one third of the rectum in males (Fig. 5A, 5B). In females, the site of attachment in the lower third of the rectum is more varied. The peritoneum-lined recess between the rectum and the posterior aspect of the bladder is the rectovesical pouch. On sagittal MRI of histologic sections obtained after surgery, the peritoneal reflection appears as a low-signal-intensity linear structure that extends over the surface of the bladder and can be traced posteriorly to its point of attachment onto the rectum (Fig. 6). The peritoneum attaches in a V-shaped manner onto the anterior aspect of the rectum, an appearance we characterized as the “seagull” sign (Fig. 7A, 7B).
Fig. 5A. Peritoneal reflection. In photograph of sagittal cadaveric hemisection, arrow indicates peritoneum as it is reflected from bladder onto rectum.
Fig. 5B. Peritoneal reflection. In vivo sagittal T2-weighted fast spin-echo image obtained in 78-year-old man with rectal adenocarcinoma shows peritoneal reflection (arrows) that, in this plane, can be followed to its point of attachment (lower arrow) over anterior surface of rectum.
Fig. 6. In vivo sagittal T2-weighted fast spin-echo image of pelvis in 56-year-old man with rectal adenocarcinoma shows peritoneal reflection as line (arrow) of low signal intensity extending over surface of bladder posteriorly to point of attachment on anterior surface of rectum. Below this point, peritoneum fuses to form Denonvilliers' fascia (arrowheads).
Fig. 7A. Peritoneal reflection in 74-year-old man with rectal adenocarcinoma. In vivo axial thin-slice T2-weighted fast spin-echo image shows peritoneal reflection as low-signal-intensity layer that attaches to rectum with characteristic V-shaped configuration anteriorly in midline (arrow).
Fig. 7B. Peritoneal reflection in 74-year-old man with rectal adenocarcinoma. Photograph of histologic section shows point of attachment (arrow) of peritoneal reflection to anterior portion of rectum. (H and E)

Denonvilliers' Fascia and the Urogenital Neurovascular Bundle

This well-developed fascia forms a distinctive shiny anterior surface of the mesorectum. It is visible on MRI as a low-signal layer that can be traced up to the peritoneum superiorly (Fig. 8A, 8B).
Fig. 8A. Denonvilliers' fascia. Photograph of cadaveric whole-mount histologic section (A, H and E) and corresponding cadaveric MRI (B) show Denonvilliers' fascia as localized thickening of fascia overlying mesorectum in midline (straight arrows). Neurovascular bundle is seen posterolaterally relative to prostate (curved arrows). Vessels in bundle are depicted as tiny signal void structures.
Fig. 8B. Denonvilliers' fascia. Photograph of cadaveric whole-mount histologic section (A, H and E) and corresponding cadaveric MRI (B) show Denonvilliers' fascia as localized thickening of fascia overlying mesorectum in midline (straight arrows). Neurovascular bundle is seen posterolaterally relative to prostate (curved arrows). Vessels in bundle are depicted as tiny signal void structures.

The Lateral Ligaments

Contralateral rectal traction, or cadaveric dissection (Fig. 9A, 9B), of the fascia around the neurovascular branches as they run medially to the rectum creates the lateral ligaments of the rectum. Although not shown as ligamentous structures on MRI, the lateral ligaments may be indicated by middle rectal vessels when these are present (Fig. 10A, 10B).
Fig. 9A. Lateral ligament. Photograph of dissected cadaveric pelvis (A) and diagram (B) show lateral ligament, which is constituted by fascia around rectal nerve supply derived from inferior hypogastric plexus. S2–S4 = sacral vertebrae 2–4.
Fig. 9B. Lateral ligament. Photograph of dissected cadaveric pelvis (A) and diagram (B) show lateral ligament, which is constituted by fascia around rectal nerve supply derived from inferior hypogastric plexus. S2–S4 = sacral vertebrae 2–4.
Fig. 10A. Lateral ligament. In vivo axial T2-weighted fast spin-echo image obtained in 65-year-old man with rectal adenocarcinoma shows middle rectal vessels as tubular signal-void structures (arrow) forming lateral ligament.
Fig. 10B. Lateral ligament. Photograph of corresponding whole-mount histologic section reveals lateral ligament visualized as fascia around middle rectal vessels, which are indicated by arrow. (H and E)

The Pelvic Nerve Plexuses

In cadaveric sections, the superior hypogastric plexus is seen as bifurcating like a wishbone into a pair of hypogastric nerves that descend to join the inferior hypogastric plexuses. Each inferior hypogastric plexus lies in a parasagittal plane on the sidewall of the pelvis. In males, the inferior hypogastric plexus lies posterolaterally relative to the seminal vesicle; and in females, its anterior half lies against the upper third of the vagina. Thus, the inferior hypogastric plexus is shown on MRI in a plane inside and medial to the vessels on the pelvic sidewall. The inferior hypogastric plexus is a rectangular, fenestrated structure that is 3–4 cm in its anteroposterior length (Fig. 11A, 11B) in the parasagittal plane and is easily identified on MRI. The dissected inferior hypogastric plexus in a cadaveric hemipelvis can be correlated with sagittal T2-weighted MRIs (Fig. 11B), on which it is depicted as a high-signal-intensity meshlike structure. We found that the inferior hypogastric plexuses consistently appear on axial (Fig. 12) and coronal oblique (Fig. 13) MRIs as linear, somewhat beaded structures. On coronal oblique images, these structures could be traced to their sacral nerve origins.
Fig. 11A. Inferior hypogastric plexus. In photograph of sagittal dissection of cadaveric pelvis, inferior hypogastric plexus (arrow) is shown as rectangular, fenestrated structure, 3–4 cm in anteroposterior length.
Fig. 11B. Inferior hypogastric plexus. In vivo sagittal T2-weighted fast spin-echo image obtained in 68-year-old woman with rectal adenocarcinoma depicts inferior hypogastric plexus (arrow) as distinctive high-signal lattice.
Fig. 12. Oblique axial T2-weighted image obtained at level of seminal vesicles in 66-year-old man with rectal adenocarcinoma shows inferior hypogastric plexus (arrow) lateral to mesorectal fascia as high-signal-intensity slightly beaded bundles, distinguishable from vessels by lack of flow void.
Fig. 13. Oblique coronal T2-weighted fast spin-echo image obtained in 68-year-old man with rectal adenocarcinoma shows beaded appearance of inferior hypogastric plexus (arrow), which can be traced back to sacral nerves.

The Mesorectal Fascia and Mesorectum

We found that the mesorectal fascia seen on axial MRIs of the cadaveric sections and correlated with the corresponding whole-mount histologic sections to be a distinct thin layer encompassing the mesorectum and surrounded by loose areolar tissue (Fig. 14A, 14B, 14C). The mesorectal fascia is best seen on axial images and appears as a low-signal-intensity linear structure surrounding the mesorectum. It was consistently visualized on thin-slice MRI.
Fig. 14A. Mesorectal fascia in cadaveric pelvis. Photograph of axial whole-mount histologic section (A, H and E), corresponding axial T2-weighted image (B), and decalcified histologic section (C, H and E) show mesorectal fascia surrounding mesorectum (arrows).
Fig. 14B. Mesorectal fascia in cadaveric pelvis. Photograph of axial whole-mount histologic section (A, H and E), corresponding axial T2-weighted image (B), and decalcified histologic section (C, H and E) show mesorectal fascia surrounding mesorectum (arrows).
Fig. 14C. Mesorectal fascia in cadaveric pelvis. Photograph of axial whole-mount histologic section (A, H and E), corresponding axial T2-weighted image (B), and decalcified histologic section (C, H and E) show mesorectal fascia surrounding mesorectum (arrows).
The mesorectum is shown on axial MRIs of the cadaveric sections as a high-signal-intensity (similar to the signal intensity of fat) package surrounding the rectum, containing vessels and lymphatic tissue (Fig. 15A, 15B). Lymph nodes within the mesorectum are shown as high-signal-intensity ovoid structures.
Fig. 15A. Mesorectal fascia. Axial T2-weighted fast spin-echo image obtained in 68-year-old man with rectal adenocarcinoma shows mesorectal fascia as low-signal layer (arrows) surrounding high-signal-intensity mesorectum.
Fig. 15B. Mesorectal fascia. Photograph of corresponding whole-mount histologic section shows mesorectal fascia (arrows) encasing mesorectum. Blood vessels and lymphatic tissue are seen within mesorectum. (H and E)

The Rectal Wall

In cross-section, the rectal wall comprises the mucosal layer, muscularis mucosae, submucosa, and muscularis propria (Fig. 16A, 16B). On MRIs obtained in cadavers and in vivo, the mucosal layer of the bowel wall appears as a fine, low-signal-intensity line with the thicker, higher-signal-intensity submucosal layer beneath. The muscularis propria is sometimes depicted on MRI as two distinct layers—the inner circular layer and the outer longitudinal layer. The outer layer has an irregular corrugated appearance and numerous surface interruptions caused by vessels entering the rectal wall. The perirectal fat displays high signal intensity and is surrounded by the low signal intensity of the muscularis propria.
Fig. 16A. Rectal wall. In vivo axial T2-weighted fast spin-echo image of rectum in 42-year-old woman with rectal adenocarcinoma (A) and photograph of corresponding histologic section (B, H and E) show layers of rectal wall. Mucosa (short straight arrow) displays low signal intensity, and submucosa (long straight arrow) displays high signal intensity. Muscularis propria (curved arrows), comprising inner circular and outer longitudinal muscle, has low signal intensity.
Fig. 16B. Rectal wall. In vivo axial T2-weighted fast spin-echo image of rectum in 42-year-old woman with rectal adenocarcinoma (A) and photograph of corresponding histologic section (B, H and E) show layers of rectal wall. Mucosa (short straight arrow) displays low signal intensity, and submucosa (long straight arrow) displays high signal intensity. Muscularis propria (curved arrows), comprising inner circular and outer longitudinal muscle, has low signal intensity.

Discussion

The MRI appearances of the many structures relevant to total mesorectal excision of the rectum have not been previously described, to our knowledge. Yet careful correlation of anatomy with findings on high-resolution images facilitates the identification of key anatomic landmarks on preoperative in vivo imaging.
The detailed anatomy of the mesorectal fascia (fascia propria of the rectum) and MRI depiction of this structure have been described [3, 4]. Bissett et al. [4] dissected the mesorectal fascia from the mesorectum and showed that this fascia is a continuous structure that encircles the rectum and mesorectum, fusing with the peritoneum at its reflection off the rectum. At the level of the anorectal junction, the mesorectum thins out. The mesorectal fascia is clearly shown on MRI and thus permits an assessment of the distance between the tumor and the potential circumferential margin of total mesorectal excision. Depiction of tumor extending to this margin could influence the type of surgical procedure chosen and alter the plane of surgical excision; it could also result in having the patients undergo preoperative therapy in an attempt to induce the tumor to regress from the margin of the mesorectum.
Van Ophoven and Roth [5] reviewed the conflicting theories concerning the anatomy and embryologic derivation of Denonvilliers' fascia since its first description in 1836 [6]. The consensus is that this fascia represents the fusion of the walls of the peritoneal cul-de-sac that extends down to the pelvic floor in the fetus [7]. This fascia forms the glistening white surface of the anterior aspect of the mesorectum and is removed as an integral component of the resected package in total mesorectal excision. Denonvilliers' fascia is seen on MRI as a low-signal layer, and its visualization in relation to an anterior tumor of the rectum provides valuable preoperative information.
The rectosacral fascia, often referred to as Waldeyer's fascia (although Waldeyer did not describe it as such in his anatomic report published in 1899), was characterized by Crapp and Cuthbertson [8]. The thickness of this fascia varies from a thin transparent membrane to a thick, tough, opaque fascia. In the latter instance, unless the rectosacral fascia is deliberately divided, the surgical plane of dissection may erroneously extend anteriorly into the mesorectum, resulting in its incomplete excision, or stray posteriorly through the presacral fascia with consequent troublesome bleeding from presacral veins. We do not believe that the depiction of this ligament on MRI has been previously described.
The anatomy of the autonomic nerves that must be safeguarded during total mesorectal excision have been described in detail by Havenga et al. [9] and Kirkham et al. [10]. The preservation of these nerves is crucial to the maintenance of urologic and sexual function, and clear depiction of these structures in relation to tumor is of value in surgical planning. To our knowledge, the depiction of the inferior hypogastric plexus on MRI has not previously been described. As reported in MRI studies of the brachial plexus, the high spatial and contrast resolution of MRI enables neural structures to be separately defined from surrounding muscle and vascular structures. High-resolution T2-weighted images show the inferior hypogastric plexuses as high-signal structures that can be distinguished from vessels by their lack of blood-flow-related signal void. Our observations concur with findings of Liu et al. [11] that T2-weighted pulse sequences are the most useful for anatomic definition of nerve plexuses.
The inferior hypogastric plexus also provides branches to the rectum, which may be accompanied by a middle rectal artery, but this artery is often absent or very small. Traction on this neurovascular bundle produces the so-called lateral ligament, the size of which depends on the presence or absence of the middle rectal vessels. Previous studies have shown that the middle rectal vessels are not consistently shown either in cadaveric dissections or on angiography [12, 13].
Although our study defined a number of anatomic structures on high-spatial-resolution MRI, a potential limitation is that we were unable to document the frequency and variation in appearances of these structures because correlation of imaging appearances with anatomic structures had been performed in selected patients. Therefore, a future study evaluating frequency and variation of the structures seen on MRI as well as the usefulness of this information in the clinical setting in a large population would be of value.
The MRI appearances of the peritoneal cavity and the peritoneal folds that subdivide the cavity have been well described in the abdomen [14, 15]. However, the MRI appearances of the attachment of the peritoneum to the anterior rectal wall and the subperitoneal pelvic compartments have not been described, to our knowledge. We have reported the MRI appearance of the pelvic peritoneum and the site of its reflection off the anterior aspect of the rectum. The rectosacral space has also been imaged, and the presacral fascia that limits it has been visualized posteriorly. The preoperative imaging of perirectal structures and compartments and the elucidation of their relation to location and extent of tumor provide valuable information for the overall planning and delivery of best-practices surgery and neoadjuvant therapy.

Footnote

Address correspondence to G. Brown ([email protected]).

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 431 - 439
PubMed: 14736677

History

Submitted: March 6, 2003
Accepted: August 19, 2003

Authors

Affiliations

Gina Brown
Department of Radiology, Cardiff and the Vale NHS Trust, University of Wales College of Medicine, Heath Park, Cardiff CF14 4XW, Wales.
Present address: Department of Radiology, The Royal Marsden NHS Trust, Downs Rd., Sutton, Surrey SM2 5PT, England.
Alex Kirkham
Department of Imaging, The Middlesex Hospital, Mortimer St., London W1T 3AA, England.
Geraint T. Williams
Department of Radiology, Cardiff and the Vale NHS Trust, University of Wales College of Medicine, Heath Park, Cardiff CF14 4XW, Wales.
Michael Bourne
Department of Radiology, Cardiff and the Vale NHS Trust, University of Wales College of Medicine, Heath Park, Cardiff CF14 4XW, Wales.
Andrew G. Radcliffe
Department of Radiology, Cardiff and the Vale NHS Trust, University of Wales College of Medicine, Heath Park, Cardiff CF14 4XW, Wales.
Joanne Sayman
Department of Radiology, Cardiff and the Vale NHS Trust, University of Wales College of Medicine, Heath Park, Cardiff CF14 4XW, Wales.
Richard Newell
Cardiff School of Biosciences, Biomedical Bldg., Cardiff University, Cardiff CF10 3US, Wales.
Chummy Sinnatamby
Department of Anatomy, The Royal College of Surgeons of England, 35/43 Lincoln's Inn Fields, London WC2A 3PE, England.
Richard J. Heald
Department of Colorectal Surgery, The Pelican Centre, North Hampshire Hospital, Aldermaston Rd., Basingstoke, Hampshire RG24 9NA, England.

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