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INTRODUCTION
*From the Nuffield Laboratory of Ophthalmology, University of Oxford, England, and from
the University of Illinois Eye and Ear Infirmary, Chicago, Ill. Supported in part by a Macy
Foundation Faculty Scholar Award (Dr Goldberg), by core grant EY1792 from the National
Eye Institute, Bethesda, Maryland, and by an unrestricted research grant from Research to
Prevent Blindness, Inc, New York, NY.
TR. AM. OPHTH. SOC. vol. LXXX, 1982
156 Goldberg
Because little is known of the morphology of this region and because
angiographic studies have not previously been undertaken we present the
results of our biomicroscopic and angiographic investigations in both
normal and abnormal human limbuses.
RESULTS
CLINICAL MORPHOLOGY
Precise focusing of the slit-lamp (Fig 1A and B) and high magnification (Fig
1C) are necessary if the palisades are to be observed. They are found just
peripheral to the terminal capillary loops of the limbus (Fig 2). The
appearance of the palisade zone varies considerably from one individual to
the next. For example it is altered by the presence of melanin (Fig 3A and
B). In moderately or darkly pigmented individuals the palisades are easily
seen in diffuse illumination, because they are outlined by the melanin-
containing epithelial cells of the interpalisades (epithelial rete ridges).
Vessels in these palisades may be obscured by dispersed pigmentation. In
lightly pigmented whites the palisades may be difficult to see in diffuse
illumination, but can be observed rather well by scleral scatter. In some
individuals the palisades are not visualized well at all. In many instances,
Palisades of Vogt 157
158 Goldberg
FIGURE 2
Palisades of Vogt are located just peripheral to terminal capillary loops (arrows) of limbus.
FIGURE 1
Precise focusing at high magnification is necessary if palisades of Vogt are to be observed. A:
Each palisade (arrows) contains a radially oriented vascular complex; cf, Fig 1B. Open arrow
indicates marker vessel for orientation and comparison with Fig 1B. The angiogram is shown
in Fig 7. B: Same area as Fig LA, but focused slightly more superficially. The palisades
cannot be seen. Open arrow indicates marker vessel for orientation and comparison with Fig
1A. c: Limbal area at low magnification only faintly shows palisade zone as series of short,
radially oriented and parallel stripes (arrow).
Palisades of Vogt 159
I,ga.M
7
A j
FIGURE 3
The palisades of Vogt are more easily discerned when moderately dense limbal melanosis is
present. A: East Indian limbus; palisades outlined by melanin-containing cells of interpalisade
zones are easily seen in diffuse illumination. B: European limbus; palisades are seen well only
in scleral scatter.
FIGURE 4
Vessels (arrows) of the palisades are dilated and more visible when the conjunctiva is
inflamed, as in case of adenoviral conjunctivitis.
160 Goldberg
FIGURE 5
Palisades are more prominent and regular along lower limbus than at upper limbus. A:
Composite photograph of lower limbus of eye whose upper limbus is shown in Fig 5B. B:
Composite photograph of upper limbus of eye whose lower limbus is shown in Fig 5A.
:.
FIGURE 6
The shape ofindividual palisades varies considerably. A: Typical narrow rectangles are seen at
right, and more unusual dot and oval shapes are seen at left. B: Palisades shaped like H's, V's,
K's, or Y's may be seen, along with complex trabecular configurations.
palisadal vessel seen end on. The long, narrow, rectangular palisades often
interconnect, forming Y-, H-, X-, or K-shaped patterns (Figs 5, 6). Some-
times, more extensive connections give a trabecular appearance.
Measurements of the length and width of the palisades and interpal-
isades from 12 normal subjects are shown in the Table, and indicate that
the fibrovascular bundles are narrower than the epithelial rete ridges. The
average length of the palisades in our subjects was 0.36 mm 0.09 SD
(range: 0. 25 to 0. 59 mm), and their average width was 0. 04 mm + 0. 007 SD
(range: 0.03 to 0.05 mm). The variation of these dimensions is indicated by
the coefficients of variation, which were 26.7% for length and 18.5% for
width. The corresponding measurement for the width of the epithelial
interpalisades was as follows: average width, 0.07 mm + 0.02 SD (range:
0.05 to 0. 10 mm). The coefficient of variation was 22.7%. The length ofthe
interpalisades could not be determined because of the lack of discrete
margins.
FIGURE 7
Angiogram of lower limbal region shown in Fig 1A. A. Vessels of palisades (triple white
arrows) fill extremely quickly, at about same time as terminal capillary loops (single white
arrow). Both sets of vessels leak fluorescein slightly, and to lesser extent than bulbar vessels
of conjunctiva (open black arrows). B: Later venous stage of angiogram seen in Fig 7A. Very
little additional leakage is seen from vessels of palisades and from terminal capillary loops of
the marginal arcades, whereas bulbar conjunctiva is intensely hyperfluorescent due to
extreme leakage.
164 Goldberg
FIGURE 8
Angiogram of normal limbus. A Early arterial phase. Vessels of palisades (triple arrows) have
not yet become perfused. Open white arrow indicates same vessel in all phases of angiogram.
B: A few seconds later, vessels of palisades contain fluorescein (triple arrows), but there is
almost no leakage. Other bulbar vessels of conjunctiva have begun to leak (double arrows). c.
Early venous phase shows mild leakage from vessels of palisades (triple arrows). D: Late
venous phase shows little increase in leakage fr-om vessels of palisades (triple arrows),
although leakage from larger vessels of conjunctiva has increased markedly.
Furthermore, the palisadal tissue appears to enlarge, possibly because of
inflammatory edema and cellular infiltration, and the palisades becompe
wider than the interpalisades contrary to their normal proportions.
HISTOLOGIC FINDINGS
FIGURE 9
Angiogram oflimbus from patient with adenoviral conjunctivitis. A: Mid-venous phase. Note
hyperfluorescence of palisades (arrows) and negative image of their vessels. B: Late venous
phase. Palisades (arrows) are enlarged when inflamed, and amount of fluorescein leakage is
increased.
166 Goldberg
FIGURE 10
Histologic appearance of palisades of Vogt. The palisade is narrower than the interpalisade,
and contains blood vessels (arrows) (hematoxylin and eosin). A: Limbus of 84-year-old
woman. B: Another limbal area from same subject.
DISCUSSION
and feet. Here, as in the limbus, parallel rows of epithelial rete ridges
interdigitate with cords of fibrovascular connective tissue. In analogy with
the skin, the characteristic limbal anatomy can be called "conjunctivogly-
phics" ("conjunctival carvings") or "limboglyphics." There are several
additional points of similarity. The glyphics are not present on all skin
surfaces, nor are they found throughout the conjunctiva. Holocrine glands
or cells (sebaceous in the skin; goblet cells in the conjunctiva) are missing
from both of these specialized structures. The ridge patterns are unique to
each individual in the skin (eg, fingerprints) and also appear unique in the
conjunctiva. One difference between the dermatoglyphics and conjuncti-
voglyphics is the presence ofeccrine (sweat) gland openings on the epithe-
lial rete ridges in the former, and their absence in the latter.
In the skin there are characteristic changes in the ridge patterns in
different diseases (eg, trisomies, chromosomal deletions, ectodermal dys-
plasia, congenital rubella, nail-patella syndrome10); some minor differ-
ences between males and females; and some racial differences in the types
of individual ridge patterns. 11-16 Whether or not the study of conjunctivo-
glyphics proves to be as clinically or genetically as rewarding as that of
dermatoglyphics remains to be seen. In any event it would be desirable to
study the palisades and interpalisades to determine the following: if there
are age, race, sex, or twin differences; if there are associations with
chromosomal diseases; and if there are characteristic changes with such
acquired diseases as recurrent corneal erosions, delayed graft epithelial-
ization, chemical burns, melting diseases of the limbus, and various limbal
operations including fornix- and limbal-based flaps of the conjunctiva.
It is of interest that a large number of previous angiographic
studies" 9"17-24 have failed to visualize or describe the vasculature of the
palisades of Vogt. Good clinical descriptions and diagrams may be found in
the work by Vogt, himself,3 by Graves,8 by Hogan et al,25 and by Duke-
Elder and Wybar.26 The fact that fluorescein leakage from the palisadal
vessels occurs relatively late in the angiographic sequence and is relatively
mild suggests that some intercellular junctional complexes in the endo-
thelium may be functionally competent and/or that there are few, if any,
endothelial fenestrations. In an electron microscopic study of conjunctival
vessels Hogan was able to demonstrate some zonulae occludentes, only a
few cytoplasmic fenestrations, good basement membrane formation, and a
few pericytes.25 In any event, the angiographic appearance ofthe palisadal
vessels suggests that this distinctive microvasculature has functional prop-
erties different from those of the more peripheral bulbar conjunctiva.
168 Goldberg
SUMMARY
The palisades of Vogt are distinctive normal features of the human cor-
neoscleral limbus. Our clinical studies indicate that they are more discrete
in younger and in more heavily pigmented individuals, and that they
appear more regular and prominent at the lower limbus than at the upper
limbus. They are seen only infrequently in the horizontal meridian. There
is some symmetry (though it is not exact) from one eye to the other in the
same person. The anatomy ofthe palisades appears to be unique for a given
individual. In this respect, as well as in their microscopic anatomy, the
palisades of Vogt appear comparable to fingerprints, and the term "con-
junctivoglyphics" ("conjunctival carvings") or "limboglyphics" is suggested
in analogy with "dermatoglyphics."
The palisades of Vogt have a distinct vasculature with narrow, barely
visible, arterial and venous components of radially oriented hairpin loops.
Angiography reveals that these vessels leak fluorescein relatively late and
only to a moderate extent. They respond to inflammation by dilatation and
gross breakdown of their physiologic barrier properties.
The functions of the palisades of Vogt are not known with certainty, but
their interpalisadal epithelial rete ridges may serve as a repository for
corneal epithelial cells. They may thus be important in both aging and
diseases of the cornea.
REFERENCES
1. Bron AJ, Goldberg MF: Clinical features of the human limbus, in Trevor-Roper P (ed):
The Cornea in Health and Disease: Proceedings of the VIth Congress of the European
Society of Ophthalmology. London, Academic Press Inc, 1981.
2. Aurell G, Kornerup T: On glandular structures at the corneo-scleral junction in man and
swine: The so-called "Manz glands." Acta Ophthalmol 27:19, 1949.
3. Vogt A: Atlas of the Slitlamp-Microscopy of the Living Eye. Berlin, Springer, 1921.
4. Dobree JH: Superficial perilimbal vessels in the normal and congested eye. Br J
Ophthalmol 34:720, 1950.
5. Maumenee AE: Repair in the cornea, in Montagna W, Billingham RE (eds): Advances in
Biology of Skin. New York, Macmillan Co, 1964, vol 5.
6. von Heydenreich A: Die Zellmigration im Bereich der Hornhaut. Ber Dtsch Ophthalmol
Ges 62:287, 1959.
7. Bron AJ: Vortex patterns of the corneal epithelium. Trans Ophthalmol Soc UK 93:455,
1973.
8. Graves B: Certain clinical features of the normal limbus. BrJ Ophthalmol 18:305, 1934.
9. Bron AJ, Easty DL: Fluorescein angiography of the globe and anterior segment. Trans
Ophthalmol Soc UK 90:339, 1970.
10. Verbov J: Clinical significance and genetics of epidermal ridges: A review of der-
matoglyphics. J Invest Dermatol 54:261, 1970.
11. Miller JR: Dermatoglyphics. J Invest Dermatol 60:435, 1973.
12. Holt SB: The significance of dermatoglyphics in medicine: A short survey and summary.
Clin Pediatr 12:471, 1973.
Palisades of Vogt 169
13. Preus M, Fraser FC: Dermatoglyphics and syndromes. Am J Dis Child 124:933, 1972.
14. Cherrill FR: The Finger Print System at Scotland Yard. London, Her Majesty's Station-
ery Office, 1954.
15. Schaumann B, Alter M: Dermatoglyphics in Medical Disorders. New York, Springer-
Verlag, 1976.
16. Holt SB: The Genetics of Dermal Ridges. Springfield, Ill, Charles C Thomas, 1968.
17. Easty DL, Bron AJ: Fluorescein angiography of the anterior segment: Its value in corneal
disease. Br J Ophthalmol 55:671, 1971.
18. Mitsui Y, Matsubara M, Kanagawa M: Fluorescence irido-corneal photography. Br J
Ophthalmol 53:505, 1969.
19. Fetkenhour CL, Choromokos E: Anterior segment fluorescein angiography with a retinal
fundus camera. Arch Ophthalmol 96:711, 1978.
20. Bruun-Jensen J: Fluorescein angiography of the anterior segment. Am J Ophthalmol
67:842, 1969.
21. Amalric P, Rebi E: New indications offluorescein angiography of the anterior segment of
the eye: IV. Several examples of scleral and corneal pathology. Ann Ocul (Paris) 204:731,
1971.
22. Marsh RJ, Ford SM: Blood flow in the anterior segment of the eye. Trans Ophthalmol Soc
UK 100:388, 1980.
23. Talusan ED, Schwartz B: Fluorescein angiography: Demonstration of flow pattern of
anterior ciliary arteries. Arch Ophthalmol 99:1074, 1981.
24. Minatoya H, Acacio I, Goldberg MF: Fluorescein angiography of the bulbar conjunctiva
in sickle cell disease. Ann Ophthalmol 5:980, 1973.
25. Hogan MJ, Alvarado JA, Weddell JE: Histology of the Human Eye: An Atlas and
Textbook. Philadelphia, WB Saunders, 1971.
26. Duke-Elder S, Wybar KC: TheAnatomy of the Visual System: System of Ophthalmology.
London, Henry Kimpton, 1961, vol 2.
DISCUSSION
DR WILLIAM H SPENCER. The authors have carefully studied the biomicroseopic
appearance, vascular dynamics and anatomic substrate of the specialized epithelial
and subepithelial fibrovascular structures located at the limbus known as the
"palisades of Vogt." The authors note considerable variation in pattern, distribution
and number of ridge-like palisades from one person to another and suggest that,
like fingerprints, the limbal palisades are distinctive for a given individual. The
authors speculate about the function of the epithelial and vascular components
noting that the thick layer of inter-palisadal epithelial cells may serve as a depot of
cells ready to migrate onto the cornea to replace diseased or destroyed corneal
epithelial cells, and they suggest that the vessels serve to nourish these cells.
In histologic sections of normal skin the border between the dermis and epi-
dermis is irregular due to the presence of dermal papillae that extend upward into
the epidermis. The ridges of epidermis separating the papillae are known as rete
ridges. This pattern is relatively inconspicuous wherever the skin is loosely
adherent to underlying tissues, but is quite prominent at sites of firm subepithelial
adhesions. In the hand the skin ofthe dorsum is quite "loose" and has relatively few
rete ridges, but the firmly attached palmar surface ofthe skin contains many ridges.
Similarly the thin skin of the eyelid surface containing epithelium of uniform
170 Goldberg
thickness is readily "ballooned up" by a subepithelial injection offluid until the lid
margin is reached where firm rete ridges and dermal papillae inhibit further fluid
dissection. These anatomic specializations are also found in mucous membrane,
especially at zones of transition and attachment. Doctors Goldberg and Bron have
called our attention to the anchoring sites of the conjunctiva at the limbus.
Corresponding attachments are found where the conjunctiva adheres to the tarsus
and to the lid margin at the mucocutaneous junction. In the tarsus the spread of
vascular and perivascular inflammation is to a degree limited by these structures
causing characteristic papillae to form, some with a "paving block" configuration.
The spread of inflammatory transudate from the vessels of the limbal palisades may
also be in part limited by the inter-palisadal attachments. Perhaps this accounts for
the papillary configuration of the circumscribed elevations occasionally seen at the
limbus in individuals with vernal kerato-conjunctivitis.
The authors have provided us with interesting data pertaining to the fluorescein
leakage pattern from normal palisadal vessels. It is to be hoped that they will
continue this investigation since so little is known about the responses of these
vessels to a variety ofstimuli and the role that they play in such diverse conditions as
peripheral corneal immune reactions and the development of a pannus.
One of the most intriguing aspects of this study is the suggestion that the thick
layer of inter-palisadal epithelial cells can serve as a repository for cells that can
migrate onto the cornea to replace diseased or destroyed corneal epithelial cells.
Normally the epithelial cells of the cornea are, in part, replaced by cells from the
basal layer where cell division takes place. Undoubtedly central migration of
peripheral cells also occurs. As evidence of this phenomenon the authors draw our
attention to the characteristic vertically oriented curvilinear pattern of corneal
epithelial opacification that occurs in Fabry's disease and after utilization of drugs
such as Amiodarone or chloroquine. Additional evidence is seen in another
condition occurring primarily in blacks, known as striate melanokeratosis where
limbal pigment bearing cells migrate toward the center of the cornea after chronic
inflammation or injury. I would like to ask ifthe authors have observed the pattern
of opacification in Fabry's disease to begin at the superior and inferior limbus and to
advance centrally. These photographs from the collection of Doctor Richard Abbott
at the Pacific Medical Center in San Francisco show the characteristic pattern of
corneal epithelial opacification in Fabry's disease and after use ofAmiodarone. The
participation by peripheral cells in the process is difficult to determine. I would
assume that the cells most likely to become affected would be those that are most
active metabolically, and would expect the opacity to arise centrally as well as
peripherally. Perhaps an animal model using a radiomarker, such as tritium-
labeled thymidine, could be used to study the participation of the inter-palisadal
epithelial cells in these conditions, and in the normal turnover of corneal epithelial
cells.
I very much appreciate the opportunity to discuss this fine contribution to the
literature and wish to thank the authors for sending me their manuscript well in
advance of the meeting.
Palisades of Vogt 171
DR GEORGE SPAETH. One observation on gonioscopy is that the posterior trabecular
meshwork is almost always less pigmented in the 3:00 and 9:00 o'clock positions
than elsewhere. I have never been able to understand this. I wonder if Doctor
Goldberg believes that there is less flow of aqueous out of these particular areas,
which may explain this peculiar distribution of pigmentation or rather lack of
pigmentation in these areas.
DR MORTON GOLDBERG. Thank you. With respect to Doctor Spaeth's query, I have no
explanation of that observation. We do not think that it would be directly at-
tributable to the palisades. With respect to Doctor Spencer's comments, I think
they were extremely valuable. The labelling studies would, in a proper subhuman
primate, probably answer the question as to the migration ofpericorneal cells onto
the center of the cornea. There is no doubt, from a variety of animal as well as
human studies, that surface corneal epithelial cells come not only from the basal
layer of the corneal epithelium but also from the pericorneal limbus. The peri-
corneal limbal cells have a higher mitotic rate than those in the center ofthe cornea.
One might theorize, therefore, that the more rapidly reproducing cells might
migrate into zones where the reproduction rate is slower. That would explain the
appearance we see in the otherwise dissimilar whirlpool or vortex patterned
dystrophies of the corneal epithelium. This group of diseases is extremely het-
erogeneous from the etiologic point of view. There are, for example, inherited
storage diseases, such as Fabry's disease, in which macrolipid marks the presence
of the apparently migrating corneal epithelial cells. One sees the same biomi-
croscopic appearance in toxic keratopathies, such as those caused by chloroquine
and Amiodarone. One sees the same thing as a normal manifestation of epithelial
slide in heavy pigmented individuals (striate melanokeratosis). It would seem that
the common denominator of these quite dissimilar diseases would involve the
pattern of cell migration, because these conditions have virtually nothing else in
common. However, the proof is in the pudding, and we have not performed the
experiments suggested by Doctor Spencer. I would agree that further work is
indicated, and I hope that many of the members would proceed with it.