ARTICLE
Almost all organs and tissues, in many species, have been explored by
magnetic resonance imaging (MRI) since its inception. However, to our
knowledge, there is no published matter specifically regarding magnetic
resonance (MR) images of lips. The size of the different tissues lying
in the thickness of the lips requires successful high resolution MR images.
This is the same requirement as for skin MRI [1, 2]. To this end, we use
a low-field (0.1 T) dedicated MRI system. 0.1 T is an uncommon field value
for MR imaging near a microscopic scale although it has already been used
for skin imaging [3]. We show the MR images obtained, one being correlated
with a histological section, and discuss the different contrasts obtained.
Materials and methods
We used a dedicated low-field MRI system, based on a water-cooled variable
electromagnet (Drusch, Poissy, France) creating a main magnetic field
of 0.1 T [4]. Maximum gradient strength is 20 mT/m (rising time of 0.5
ms). The orientation of B0, perpendicular with respect to the
sample access, allows the use of solenoidal transmit-receive radio-frequency
(rf) coils. In order to achieve a good filling factor with respect to
the sample, an rf coil of 2.3 cm diameter, 1.7 cm length and 6 turns made
with 2 mm diameter copper wire was built. The rf coil was tuned at 4.32
MHz with 3 fixed non-magnetic capacitors (American Technical Ceramics,
New York, USA) in parallel (total capacitance of 1,890 pF). The imaging
software running on a PC-based spectrometer (MR 3030, SMIS, Guilford,
Great-Britain) has already been developed in our laboratory [5].
A portion (between the midline and the angle of the mouth) of the inferior
lip of a male cadaver was set apart. The cadaver was embalmed by femoral
cannulation using a solution containing phenic acid, formol, alcohol,
glycerin, chloral hydrate and conserved in alcohol solution. After MR
imaging, it was processed to 5 µm thick paraffin sections, stained
with trichrome technique or hematoxylin and eosine. Digitized photographs
of the histological sections were obtained for further comparison with
MR images.
All MR images were acquired with 3D-FLASH sequences, T1 and
T2* weighted (see details of the sequences in figure legends).
Asymmetric acquisition matrix was used due to the shape of the sample
and to reach a good compromise between signal to noise ratio and resolution.
Both histological and MR images were processed on a Macintosh Centris
650 (Apple, Cupertino, USA) using the public domain NIH Image program
(developed at the US National Institutes of Health and available on the
Internet at http://rsb.info.nih.gov/nih-image/). In particular, scaling
of the histological sections was done. This allowed us to take the exact
measurement of structures and to compare them with measurements made on
MR images. In the following, no indication means that the values given
were measured on histological sections and were identical with values
found on corresponding MR slices.
Results
Both skin, red lip and oral mucosa are classically described by their
3 constituent layers [6]. The superficial and thin layer is a stratified
squamous epithelium. The epidermis disappears on the red lip and the oral
mucosa [7]. The dermis is divided into the papillary layer, close to the
epithelium, and the deeper reticular layer. The dermis of the red lip
is characterized by a typical micro circulation [8]. Below the epithelium
of the oral mucosa, a thick lamina propria, in continuity with the dermis,
contains labial glands in a loose connective tissue. The last layer is
the hypodermis, or the deeper part of the lamina propria. In the skin,
minimal fat between the musculus orbicularis oris and dermal planes is
characteristic of the structure of the lip, although there are close attachments
between the skin and perioral muscles [9]. The vermilion border is a particular
kind of tissue joining the skin and mucosa, outside and inside. At the
limit between the epidermis and red lip (a transitional zone), the epithelium
becomes thicker and progressively less keratinized [7], the orbicular
muscle arises in the deep surface of dermis.
In Figure 1, we present
an histological section compared with the corresponding MR image (T2*
weighted) made at the same location. The epidermis is too thin (about
40 µm) to be visible on the MR image. Dermis (1 mm thick) along with
epithelium and the superficial layer of lamina propria of oral mucosa
(2 mm thick) both gave high signal intensity relative to the other structures.
This is also the case of the vermilion border. The classic distinction
between papillary and reticular dermis is not quite evident in the lip.
Deep parts of lamina propria of oral mucosa and hypodermis have similar
appearances of irregular structures at low signal intensity. Most muscular
fibres could be found in the hypodermis, marked by lines of high intensity,
and labial glands are present in the lamina propria. Musculus orbicularis
oris (about 2.5 mm thick on histological section vs 2 mm on MR
images) gives a high, uniform signal.
In Figure 2, more T1
weighted yield almost an absence of contrast between structures easily
visible in Figure 1. However
this allows the clear delineation of the inferior arteria labialis (internal
diameter about 550 µm) and particularly of a perilabial gland vascular
network (diameter about 450 µm, measured on MR image) which could
be followed on 4 contiguous slices.
Discussion
We show that high resolution images of lips are able to fit histological
sections made at the same location even at a low field of 0.1 T. The relative
obliquity between MR slices and histological ones, and the thickness of
MR images could lead to difficulty in finding exactly the same location
for the same structure. This is particularly the case of labial glands,
which are hard to identify on MR image (only one is clearly identifiable
out of 3) in Figure 1.
The outer layer of mucosa gives a high signal
similar to the second skin layer (dermis). Likewise hypodermis and deep
parts of lamina propria are of similar low signal intensity. These appearances
may be explained by similar tissular composition, but also by similar
mechanical function (gliding zones). When following the periphery of the
MR image, the continuous white layer corresponds successively to the dense
connective tissue of the dermis in the cutaneous part of the lip, to the
red lip and finally to the epithelium and superficial part of the lamina
propria of oral mucosa.
These results are different from previous studies regarding the MR appearance
of skin: notably the lip dermis appears like a high signal intensity layer
when compared with skin dermis studies made at a higher field (1.5 T)
[1, 2]. Due to the high collagen content of these layers, a very short
T2 is expected, but the chemical content of skin, notably collagen
content, may also vary with location; and vascular structures [8, 10]
are different between calf, heel (location of skin images in [1, 2]) and
lips. In particular, the hypodermis has less fat content than in other
locations [9].
Measurements on histological sections accord well with those on MR images
except for the musculus orbicularis oris. The thinner appearance on MR
images may be related to partial volume effect at the boundary of the
muscle bundles.
Lips, explored by ultrasound, are a subject of interest for fetal malformation
diagnosis [11] or dental investigation [12], for example. Their exploration
could take place in decisions in reconstructive surgery [9], or in dermatology.
The ability to make precise measurements on MR images acquired with variable
obliquity could lead to potential surgical applications, for facial rejuvenation
or reanimation.
CONCLUSION
Acknowledgements
The authors thank Mr. VETTER for his technical assistance and Apple
Computer France for its grant.
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