Three-Dimensional Microscopic Characteristics of the Human Uterine Cervix Evaluated by Microtomography

Abstract

Objectives: To analyze the microscopic anatomy of the human uterine cervix in two-dimensional (2D) and three-dimensional (3D) images obtained by microtomography (microCT). Methods: Human uterine cervixes surgically removed for benign gynecologic conditions were immersed in formalin and iodine solution for more than 72 h and images were acquired by microtomography. Results: In total, 10 cervical specimens were evaluated. The images provided by microCT allowed the study of the vaginal squamous epithelium, demonstrated microscopic 3D images of the metaplastic process between the exo and endocervix, and demonstrated the effects of metaplastic transformation on the thickness of the endocervical epithelium. Also reconstructed in 3D the endocervical folds and the repercussions of the metaplastic process on the endocervix, the changes of the endocervical epithelium along the cervical lumen and the relationship between the endocervix epithelium from the internal os and endometrium. In addition, 2D images could demonstrate the difference in tissue orientation of the collagen on the cervical stroma in a large field of view. Conclusions: MicroCT could demonstrate the microscopic anatomy of the human uterine cervix in 2D and 3D images, including the different stages of metaplastic process of the endocervical epithelium and reconstructed the endocervical lumen in 3D, preserving its natural anatomy without any mechanical effect for its dilatation.

Keywords: microscopy; microtomography; three-dimensional image; two-dimensional image; uterine cervix.

Figure 1

The vaginal mucosa covering the uterine cervix. The vaginal mucosa and its stratum corneum are visible (arrow) in the conventional microscopic image (A) and in the X-ray microtomographic image (B). The ability of this epithelium to absorb iodine is demonstrated by the intense contrast caption, shown as a prominent white appearance (radiopaque) in the radiographic image (B). Also, note the difference of the imaging definition at the cellular level between the two techniques (lower images): despite the capacity of acquisition of images at a microscopic scale, the detailed morphology at cellular scale could not be achieved by microCT.

Figure 2

(A,B) Coronal and sagittal 2D images of the uterine cervix. The multiple cystic images correspond to Naboth cysts. In (B), the intracervical Naboth cyst distorts the cervical lumen with significant discontinuity between the cervical epithelium (asterisk). (C) shows 3D reconstruction of the same uterine cervix and the spatial relationship between the Naboth cysts and the cervical epithelium.

Figure 3

The “virtual colposcopy” of uterine cervix specimens generated by microCT images: the squamocolumnar junctions and their visibility at colposcopy. In (A), the squamocolumnar junction (arrow) is completely visible (type 1); in (B), the squamocolumnar junction (arrow) is partially visible (type 2); and in (C), the squamocolumnar junction is not visible (type 3).

Figure 4

The uterine cervix and the squamocolumnar junction from different perspectives. In (A), the fully visible squamocolumnar junction is shown in 3D and below in 2D images, demonstrating the area of metaplastic transformation (arrow). (B) shows the partially visible squamocolumnar junction (arrow) after virtual cervical sectioning. In (C), the squamocolumnar junction not visible in “virtual colposcopy” can be seen in a virtual section of the cervix, demonstrating the most caudal epithelium surrounded by Naboth cysts.

Figure 5

The endocervical epithelium and its relationship to the external os and cervical stroma. (A) shows the epithelial folds toward the vaginal cavity (arrowhead), presenting their extremity as a “bunch of grapes”. The epithelium is forced in a parallel direction, with its most external extremity of “small polypoid epithelium”, creating the appearance of a “bunch of grapes” visualized in colposcopic examinations (arrow). In (B), the epithelial folds still have a thick part of the external os (arrowhead). The pattern of parallel folds can be seen as the metaplasia progresses. However, there is a significant reduction in the number of endothelial folds and their thickness, with a more relevant sub-epithelial stroma. The shape of the crypts is similar to the plicae palmatae described in classic textbooks. In (C), the epithelium becomes scarce and simultaneously the cervical stroma occupies the external os of the uterine cervix covered by the squamous epithelium. (D) shows the metaplastic phenomena, the absence of visible cervical endocervical epithelium on colposcopic examination. The portio vaginalis is completely covered by metaplastic squamous epithelium. The columnar epithelium has lost its thickness and few folds, with a cobblestone appearance visible in 2D and 3D images.

Figure 6

The cervical epithelial folds (arrows) are preserved despite the presence of larger cysts in this specimen.

Figure 7

In (A,B); epithelial folds and crypts. The section of the 3D image of the endocervix shows the direction of the crypts, which are directed towards the external os. Their outer border can be seen in the direction of the center of the lumen and with the appearance of fusion in waves of folds.

Figure 8

The transition from the endocervix to the endometrium. The folds of the endocervical epithelium became sparse, predictable, and organized (arrow) to a thin, simple, and rudimentary endometrial tissue (arrowhead). The subtle change between tissues has no other anatomical marker on the uterine cervix.

Figure 9

Visualization of the stroma. The cervical fibers appear to be parallel to the luminal axis (arrow), but there is a change in direction in the internal os (arrowhead).

Figure 10

The crypts open into the cervical lumen. The arrows indicate the opening of the crypts, and the 2D image shows the large number of gland-like structures that will be opened in the lumen.