Anatomy and Histology of the Lacrimal Fluid Drainage System

Transcription

1 Okajimas Folia Anat. Jpn., 77(5): , December Anatomy and Histology of the Lacrimal Fluid Drainage System By Rieko KOMINAMI, Satoru YASUTAKA, Yutaka TANIGUCHI and Harumichi SHINOHARA Department of Anatomy II, Kanazawa Medical University, Uchinada, Ishikawa , Japan -Received for Publication, August 1, Key Words: Lacrimal fluid, Canaliculus, Common canaliculus, Lacrimal sac Summary: Five human specimens of the lacrimal canaliculus and sac were examined by light and scanning electron microsopy. The superior and inferior lacrimal canaliculi are lined with stratified squamous epithelium that is nonkeratinized and non-mucin-producing. The common canaliculus is also lined with stratified squamous epithelium, but its lumen is much narrower than the lumen of the superior and inferior canaliculi. The common canaliculus opens into an ample space called the vestibule, where the epithelium changes to high pseudostratified columnar and then low pseudostratified columnar. The vestibule continues to the infundibulum of the lacrimal sac. The infundibulum is formed by several epithelial folds that radiate from the vestibular opening to the lacrimal sac. The vestibule and infundibulum are consistent transitional structures from the common canaliculus to the lacrimal sac. The connective tissue of the lamina propria from the common canaliculus to the lacrimal sac has two histological characteristics: numerous free cell aggregates (= lymphoid structure) and numerous venules and capillaries (= cavernous structure). Lacrimal fluid enters the punctum, passes through the lacrimal canaliculus and sac, and finally drains into the nasal cavity through the nasolacrimal duct. This duct system has been studied in terms of gross anatomy (Jones, 1961) and histology (Fernandez-Valencia and Pellico, 1990; Paulsen et al., 1998), and it has also been studied in terms of tear drainage function (Doane, 1981; Hurwitz, 1996) and immunologic self-defense (Paulsen et al., 1998). Earlier publications, however, are inadequate for understanding the morphology of the lacrimal drainage system. For example, it is known that the canaliculus is lined by stratified squamous epthelium and the lacrimal sac by pseudostratified epithelium (Ross and Romrell, 1985), but where and how the former changes into the latter is unknown. In the present study, we dissected the human adult lacrimal canaliculus, lacrimal sac, and part of the nasolacrimal duct. We also prepared histological sections and specimens for scanning electron microscopy and discovered the presence of junctional structures between the common canaliculus and lacrimal sac. Materials and Methods Five human specimens of the lacrimal canaliculi and sac were obtained from two males and three females, 68 to 92 years of age. One of the specimens was embedded in paraffin, serially sectioned in the sagittal planes, and stained with Meyer's hematoxylin and eosin. The remaining four specimens were dissected grossly or under a dissecting microscope, and samples of the lacrimal canaliculus and sac were collected for semithin sections and scanning electron microscopy (SEM). The specimens for semithin sections were fixed in 2.5% glutaraldehyde in 0.1 M phosphate buffer solution (PBS) at ph 7.4 for an hour, dehydrated in a grade series of ethanol, embedded in epoxy resin, and sliced 0.5 gm thick. The sections were then stained with toluidine blue. The specimens for SEM were fixed in 2.5% glutaraldehyde in 0.1 M phosphatebuffered saline (PBS) at ph 7.4 for an hour, postfixed in 1% osmium tetroxide in PBS, dehydrated in ethanol, critical-point-dried, gold-coated, and viewed with a scanning electron microscope (JSM- 840, JEOL).

2 156 R. Kominami et al. Results The distance from the base of the inferior lacrimal papilla to the lacrimal sac ranged from 12 to 16 mm in these adult specimens. The superior lacrimal punctum was situated approximately 3 mm medial to the inferior lacrimal punctum. The lacrimal canaliculus is divided into two portions: vertical and horizontal. The vertical portion was about 2 mm in length and contained a few longitudinal folds (Fig. 1). Horner's muscle surrounded the vertical portion. Although the orientation of the individual muscle fibers were unclear, some muscle fibers circled around the vertical portion, while others coursed parallel to it (Figs. 1 and 2). The muscle also surrounded the entire circumference of the horizontal portion near the vertical portion. Horner's muscle covered only the anterior surface in the horizontal portion near the common canaliculus. The common canaliculus was approximately 3 mm long when measured from the lacrimal sac in its thick connective tissue sheath. The lacrimal sac formed a small flat cistern medio-lateral diameter of about 1 mm and a large antero-posterior diameter of about 2.5 mm. When the lacrimal sac was viewed from inside, the lateral wall was seen to contain a star-shaped slit approximately 2 mm from the cranial end of the sac, and several epithelial folds radiated from the center of the star. The slit corresponds to the infundibulum of the lacrimal sac (see the next paragraph). The canaliculus near the lacrimal punctum was lined with non-keratinized and non-mucin-producing stratified squamous epithelium. It was clearly discriminated from the anteriorly-situated keratinized epithelium of the palpebral epidermis (Figs. 3A and 3B) and from the posteriorly-situated mucin-producing epithelium of the conjunctiva (Figs. 3A and 3C). The canalicular epithelium was gm in thickness and consisted of a few layers of squamous cells, several layers of polyhedral cells, and a layer of basal cells. The canalicular lumen was varied in diameter from 100 to 250 micrometers, possibly due to the planes of sectioning. The superior and inferior canaliculi did not join as equal partners, instead the superior canaliculus emptied into the inferior canaliculus like a small branch emptying into the main stream. Consequently, the common canaliculus was more of a continuation of the inferior canaliculus. The common canaliculus was usually lined with stratified squamous epithelium, but occasionally with pseudostratified columnar epithelium (Fig. 5). Its lumen was less than 100 p,m in diameter, and narrower than the canalicular lumen. The common canaliculus continued to the vestibule, whose lumen was several times the diameter of the common canalicular lumen. It was initially lined with high pseudostratified columnar epithelium but converted to low pseudostratified columnar epithelium (Figs. 4A and 4B). The vestibule continued to the infundibulum of the lacrimal sac. The lining of the lacrimal sac is low pseudostratified columnar epithelium (Fig. 6), and the cells were approximately 30 gm in height. The basement membrane was thick for most part. There were numerous mucin-producing cells in the lacrimal sac epithelium, and they often formed clusters of secretory cells. Brown-pigment cells, probably melanocytes, were also numerous in the lacrimal sac epithelium (Fig. 4A, arrowheads) and subepithelial connective tissue. There were two distinctive features in the subepithelial connective tissue from the common canaliculus to the lacrimal sac: the presence of free cell aggregates and numerous venules and capillaries (Figs. 4A and 5). The cell aggregates were predominantly composed of lymphocytes, but mast cells and plasma cells were common. Several capillaries gm in diameter were usually present in the aggregates, and the area had appearance of lymphoid tissue. Capillaries were not entirely absent in the superior and inferior canaliculi, but were far less in number than in the common canaliculus and lacrimal sac. Numerous small veins and capil- Explanation Plate of Figures I Fig. 1. Scanning electron microscopy view of the vertical portion of the inferior canaliculus. The lumen (L) is surrounded by the stratified squamous epithelium (SE). Cut-ends of circular muscle bundles are visible (arrows) between the longitudinal muscle bundles (M) and connective tissue (CT) of the lamina propria. Fig. 2. Semithin section stained with toluidine blue. Fig. 3. Paraffin section through the inferior lacrimal punctum. The epithelium of the canaliculus (C) is nonkeratinized and nonmucin-producing. Note the clear transition from the keratinized palpebral epidermis (arrowheads) and from the mucinproducing epithelium of the conjunctiva (arrows). Squares B and C correspond to insets. The arrows in the insets indicate the borders of the epithelia. PA; Palpebral aperture.

3 Lacrimal Canaliculus and sac 157 Plate I

4 158 R. Kominami et al. lanes in the common canaliculus and lacrimal sac formed a cavernous structure. Some of the capillanes were adjacent to the basement membrane. The common canaliculus was consistently accompanied by a vein the diameter of which was nearly 1 mm. Discussion The results are schematically illustrated in Figure 7. The non-keratinized and non-mucinproducing stratified squamous epithelium lined the whole length of the lacrimal canaliculi and the common canaliculus. The epithelium changed to high pseudostratified columnar and then to low pseudostratified columnar in the vestibule. The vestibule was an ample space that connected the narrow lumen of the common canaliculus to the infundibulum of the lacrimal sac. There were two structures that characterized the subepithelial connective tissue from the common canaliculus to the lacrimal sac: lymphoid structures and cavernous structures. Aubaret (1905) drew illustrations of the valves in the lacrimal fluid drainage system. He called a fold extending from the superior wall of the junction between the common canaliculus and lacrimal sac Rosenmuller's valve, and a fold from the inferior wall Huschke's valve. Scheaffer (1912) threedimensionally reconstructed the lacrimal canaliculus and sac but did not confirm the presence of such valves. Tucker et al (1996) injected a plastic compound through the lacrimal punctum and prepared plastic casts of the lacrimal fluid drainage system. They also failed to find Rosenmuller's and Huschke's valves in the canaliculus-sac junction, but instead found an acute kinking of the common canaliculus at its junction with the lacrimal sac and conjectured that enlargement of the lacrimal sac might cause collapse of the common canaliculus at the kink. Thus, reflux from the lacrimal sac toward the common canaliculus is blocked as though there were a valve at the junction. According to Hurwitz (1996), there is a sphincter muscle around the opening of the common canaliculus into the lacrimal sac, and the sphincter prevents reflux. We did not find any valvular folds or a sphincter muscle at the common canaliculus-sac juction. However, we did find that the common canaliculus and lacrimal sac were not connected directly but via transitional structures, the vestibule and infundibulum. The lumen increases suddenly from the common canaliculus to the vestibule, and the common canalicular end protrudes into the lumen of the vestibule. Tucker et al. (1996) attributed difficulty in cannulating to the sac to kinking of the canaliculus-sac junction. Our results suggest that the difficulty in cannulation may be primarily due to the small diameter of the lumen of the common canaliculus and the gap in luminal ampleness between the common canaliculus and the vestibule. Maurice (1973) introduced 1% Evans blue into his eye and examined the color of a nasal swab. Evans blue was consistently detected for six hours after introduction of a 20 mm3, whereas no color was detected for six hours after introduction of 1 mm3. He therefore concluded that lacrimal flow is of the order of 0.6 mm3 per minute, and that lacrimal fluid is absorbed in the lacrimal drainage pathway. Doane (1981) and Hurtiwitz (1996) found evidence suppoting the possibility of lacrimal fluid absorption in the passage from the lacrimal canaliculus through the nasolacrimal duct. As shown in the present study, the vestibule and the more distal portion of the lacrimal drainage system is lined with pseudostratified columnar epithelium. SEM examination of the lacrimal sac epithelium revealed the presence of numerous cytoplasmic extrusions of different shapes and sizes, and we confirmed this Plate II Fig. 4. Paraffin section through the common canaliculus, vestibule, and infundibulum of the lacrimal sac. Note the narrow lumen of the common canaliculus (CC) compared with that of the inferior canaliculus (IC) and vestibule (Vb). The vestibule (Vb) is continuous with the infundibulum (I) of the lacrimal sac. The epithelium at the opening of the common canaliculus is stratified squamous (SE) but changes to high pseudostratified columnar (open arrow), and then into low pseudostratified columnar (closed arrow) in the vestibule. These changes are indicated by the bidirectional arrows in inset 4B. The subepithelial connective tissue contains free cell aggregations (= lymphoid structure, asterisks) and numerous venules (V) and capillaries (= cavernous structure). The arrowheads point cells containing brown pigments. S; Lacrimal sac, SC; Superior canaliculus. Fig. 5. Semithin section of the common canaliculus. Note that the epithelium is low pseudostratified columnar. There were numerous free cells consisting of lymphocytes, mast cells, plasma cells, and cells of unknown origin, in the connective tissue of the lamina propria (asterisk). There are numerous venules (V) and capillaries forming a cavernous structure. Fig. 6. Scanning electron microscopy view of the lacrimal sac epithelium. Columnar cells (PE) approximately 30 jim in height stand on the basal lamina (BM), and thus the epithelium is pseudostratified columnar. There are spherical cytoplasmic extensions on the apical surface but no micirovilli.

5 Lacrimal Canaliculus and sac 159

6 160 R. Kominami et al. Plate III observation in histological sections. This means that the lacrimal sac epithelium may excrete mucin and membrane-bound particles into the lumen. The osmolarity values of freshly secreted lacrimal fluid have varied with the investigator and are thought to be equivalent to % NaC1 (Adler, 1950). However, investigators unanimously agree that lacrimal fluid loses water by evaporation and that the lacrimal fluid that reaches to the lacrimal sac is far more concentrated than freshly secreted lacrimal fluid, and thus, that its osmolarity is greater than 0.9% NaCl. This means that connective tissue fluid in the wall of the lacrimal sac may pass into the luminal surface by simple diffusion. There were numerous venules and capillaries from the common canaliculus to the lacrimal sac and they may supply water to dilute the lacrimal fluid in the lumen. The current of water from the subepithelial connective tissue toward the lumen may facilitate the migration of free cells in the lamina propria of the lacrimal sac into the sac lumen. References 1) Adler FH. The lacrimal apparatus. In: Physiology of Eye, 1950; pp 28-36, Henry Kimpton, London. 2) Aubaret E. Les replis valvularires des canalicules et du conduit lacrymo-nasal, au point de vue antomique et physiologique. Arch Opthalmol 1908; 28: ) Fernandez-Valencia R and Pellico LG. Functional anatomy of the human saccus lacrimalis. Acta Anat 1990; 139: ) Hurwitz JJ. Physiology of the lacrimal drainage system. In: The Lacrimal System, 1996; pp Lippincott-Raven, Philadelphia and New York. 5) Jones LT. An anatomical approach to problems of the eyelids and lacrimal apparatus. Archs Opthalmol 1961; 66: ) Maurice DM. The dynamics and drainage of tears. Int Opthalmol Clin 1973; 13: ) Paulsen F, Thale A, Kohla G, Schauer R, Rochels R, Parwaresch R and Tillmann B. Functional anatomy of human lacrimal duct epithelium. Anat Embryo' 1998; 198: ) Perra MT, Serra A, Sirigu P and Turno F. A histochemical and immunohitochemical study of certain defense mechanisms in the human lacrimal sac epithelium. Arch Histol Cytol 1995; 58: ) Schaeffer JP. The genesis and development of the nasolacrimal passages in man. Am J Anat 1912; 13: ) Tucker NA, Tucker SM and Linberg JV. The anatomy of the common canaliculus. Arch Opthalmol 1996; 114: Plate III