CLINICAL SCIENCES

In Vivo Laser Confocal Microscopic Findings

of Corneal Stromal Dystrophies
Akira Kobayashi, MD, PhD; Keiko Fujiki, PhD; Takuro Fujimaki, MD, PhD;
Akira Murakami, MD, PhD; Kazuhisa Sugiyama, MD, PhD

Objective: To investigate in vivo laser confocal micro-
scopic findings of genetically mapped corneal stromal
dystrophies and their relationship to histopathologic
findings.
Methods: Seven patients with Avellino corneal dystro-
phy, 2 patients with lattice corneal dystrophy, and 2 pa-
tients with macular corneal dystrophy were examined ge-
netically and using slitlamp biomicroscopy and in vivo
laser confocal microscopy. Corneal specimens obtained
after surgery in selected patients were histopathologi-
cally studied.
Results: In Avellino corneal dystrophy (Arg124His mu-
tation of human transforming growth factor ␤–induced
gene [TGFBI]), highly reflective granular materials with
irregular edges were observed in the superficial stroma.
In lattice corneal dystrophy (Arg124Cys and Leu527Arg
mutations of TGFBI), highly reflective branching fila-
ments of variable width were observed in the stroma. In
macular corneal dystrophy (Ala217Thr mutation of the
carbohydrate sulfotransferase gene [CHST6]), homoge-
neous reflective materials with dark striaelike images were
observed throughout the stroma. All confocal findings
correlated well with histopathologic findings.
Conclusions: In vivo laser confocal microscopy is ca-
pable of high-resolution visualization of characteristic cor-
neal microstructural changes related to 3 types of geneti-
cally mapped corneal stromal dystrophies. The use of laser
confocal microscopy may be valuable in the differential
diagnosis of corneal stromal dystrophies, especially when
diagnosis is otherwise uncertain.
Arch Ophthalmol. 2007;125(9):1168-1173

Author Affiliations:
Department of Ophthalmology,
Kanazawa University Graduate
School of Medical Science,
Kanazawa (Drs Kobayashi and
Sugiyama), and Department of
Ophthalmology, Juntendo
University School of Medicine,
Tokyo (Drs Fujiki, Fujimaki,
and Murakami), Japan.
D
URING THE PAST 2 DE -
cades, in vivo white-
light confocal micros-
copy has been a valuable
noninvasive technique
for the observation of living corneal mi-
crostructures at the cellular level.1 Its clini-
cal usefulness has been documented in
studies of healthy and diseased human cor-
neas, including granular,2 lattice,2,3 Reis-
Bücklers,2 and Thiel-Behnke4 corneal dys-
trophies.
Recently, in vivo laser confocal micros-
copy (Heidelberg Retina Tomograph 2
Rostock Cornea Module; Heidelberg En-
gineering GmbH, Dossenheim, Ger-
many) has become available.5,6 This de-
vice permits more detailed layer-by-layer
observations of the corneal microstruc-
ture with an axial resolution of approxi-
mately 4 µm,7 better than that obtained
using conventional white-light confocal
microscopes (eg, 10-µm axial optical reso-
lution with the ConfoScan 2 [Nidek Tech-
nologies, Vigonza, Italy]).8
In this study, we report in vivo micro-
structural characteristics of 3 genetically
mapped corneal stromal dystrophies using
in vivo laser confocal microscopy. We also
report relationships between in vivo mi-
croscopic images and subsequent histo-
pathologic section findings.
METHODS
The study was approved by the Ethics Com-
mittee of Kanazawa University Graduate School
of Medical Science and followed the tenets of
the Declaration of Helsinki. Before enroll-
ment, written informed consent was obtained
from all subjects. The Table summarizes demo-
graphic data of the 11 participants.
GENETIC ANALYSIS
Peripheral blood samples were obtained from
the patients. Genomic DNA was extracted from
peripheral leukocytes. Patients clinically diag-
nosed as having Avellino or lattice corneal dys-
trophy underwent genetic analysis of exons 4
and 12 of the human transforming growth fac-

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 Table. Eleven Patients From 9 Families With 1 of 3 Corneal Stromal Dystrophies

Patient No./ Clinical Diagnosis

Sex/Age, y of Corneal Dystrophy Eye Previous Surgery Gene Mutation
1/F/83 Avellino R NA TGFBI Arg124His (heterozygous)
L Deep lamellar keratoplasty
2/F/66 Avellino R NA TGFBI Arg124His (heterozygous)
L NA
3/M/59 Avellino R NA TGFBI Arg124His (heterozygous)
L NA
4/F/49 Avellino R NA TGFBI Arg124His (heterozygous)
L Pterygium excision (amniotic
membrane transplantation)
5 (Son of Avellino R NA TGFBI Arg124His (heterozygous)
patient 1)/M/61 L NA
6/F/73 Avellino R NA TGFBI Arg124His (heterozygous)
L NA
7/M/51 Avellino R NA TGFBI Arg124His (heterozygous)
L NA
8/F/59 Lattice type I R Deep lamellar keratoplasty TGFBI Arg124Cys (heterozygous)
L NA
9/M/82 Lattice type IV R Deep lamellar keratoplasty TGFBI Leu527Arg (heterozygous)
L NA
10/M/65 Macular R Penetrating keratoplasty CHST6 Ala217Thr (homozygous)
L NA
11 (Brother of Macular R Deep lamellar keratoplasty CHST6 Ala217Thr (homozygous)
patient 10)/M/59 L NA

Abbreviation: NA, not applicable.

tor ␤–induced gene (TGFBI) as described previously.9 Pa- SLITLAMP EXAMINATION

tients clinically diagnosed as having macular corneal dystro-
phy had all exons of the carbohydrate sulfotransferase gene
(CHST6) analyzed as described previously.10
IN VIVO LASER
CONFOCAL MICROSCOPY
After applying a large drop of contact gel (Comfort Gel oph-
thalmic ointment; Bausch & Lomb, Berlin, Germany) on the
front surface of the microscope lens, a sterile cap (TomoCap;
Heidelberg Engineering GmbH) was mounted on the holder
to cover the microscope lens. Then the centers of the cornea
of both eyes were examined layer by layer. The in vivo laser
confocal microscopy module uses a ⫻ 60 water immersion
objective lens (Olympus Europa, Hamburg, Germany) and a
670-nm diode laser as the light source (area of observation,
400 µm ⫻ 400 µm).7 Two examinations per eye were per-
formed.
RESULTS
GENETIC ANALYSIS
All 7 patients with Avellino corneal dystrophy had an
Arg124His (R124H) heterozygous missense mutation of
TGFBI, confirming clinical diagnosis. The 2 patients with
lattice corneal dystrophy had an Arg124Cys (R124C [lat-
tice corneal dystrophy type I]) and a Leu527Arg (L527R
[lattice corneal dystrophy type IV])11 heterozygous mis-
sense mutation of TGFBI, confirming clinical diagnosis.
The 2 patients with macular corneal dystrophy had an
Ala217Thr (A217T) homozygous missense mutation of
CHST6, confirming clinical diagnosis.10
All 7 patients with Avellino corneal dystrophy (patients
1-7) had multiple, discrete, round, sharply demarcated
gray-white deposits, as well as scattered stellate opaci-
ties (Figure 1A). However, latticelike lines are subtle,
and they are not discernible by slitlamp examination in
most cases. Areas between dense opacities were clear in
all patients. The Descemet membrane and endothelium
appeared normal in all patients.
In the patient with lattice corneal dystrophy type I (pa-
tient 8), slitlamp biomicroscopy showed numerous thread-
like, radially oriented fine spicules throughout the stroma
(Figure 2A). The central anterior stroma of both eyes
showed dense opacification. In the patient with lattice
corneal dystrophy type IV (patient 9), slitlamp biomi-
croscopy showed typical thick lattice lines with radial ori-
entation (Figure 3A).
In the patients with macular corneal dystrophy (pa-
tients 10 and 11), slitlamp biomicroscopy showed ground-
glass–like haze with indistinct borders throughout the
thickness of the cornea. Scattered gray-white lesions were
also seen (Figure 4A).
IN VIVO LASER CONFOCAL MICROSCOPY
All 7 patients with Avellino corneal dystrophy had simi-
lar images. In the basal epithelial layer, focal deposition
of highly reflective granular materials without dark shad-
ows was observed (Figure 1D). At the level of the super-
ficial and middle stroma, clusters of highly reflective
granular materials with irregular edges were observed
(Figure 1F-H). However, we could not find any confo-

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 A B
C D
E F
G H
e b s
Figure 1. Patient 1 (with Avellino corneal dystrophy). A, Slitlamp photograph
reveals round gray-white deposits and scattered stellate opacities in the
superficial and middle stroma. B, In anterior cornea tissue, there are clusters
of deposits with irregular edges (Azan stain). C, Some deep stromal deposits
are positive (arrow) for amyloid stain and show apple-green birefringence
under polarized light (inset). D, Laser microscopy of the basal epithelium
shows focal deposits of highly reflective material with irregular edges.
E, Normal keratocyte nuclei are found in the superficial and middle stroma.
F and G, In a different area at the same level, clusters of highly reflective
granular materials with irregular edges are seen. H, Oblique section of the
superficial layer has highly reflective granular materials just beneath the
Bowman layer. Normal subbasal nerves are seen at the Bowman layer.
b indicates Bowman layer; e, epithelium; and s, anterior stroma. All are
confocal images, 400 ⫻400 µm (original magnification ⫻300). Bar indicates
100 µm.
cal images that would correspond to the latticelike le-
sions because lattice lines are not discernible in patients
with Avellino corneal dystrophy. The surrounding stroma
and keratocyte nuclei (Figure 1E), as well as the endo-
thelial layer, appeared normal.
In the basal epithelial layer of patient 8 (with lattice
corneal dystrophy type I), reticular, highly reflective ex-
tracellular deposits were observed (Figure 2E). At the level
of the superficial and middle stroma, highly reflective
branching filaments were observed (Figure 2G and H).
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A B
C D
E F
G H
Figure 2. Patient 8 (with lattice corneal dystrophy type I). A, Slitlamp
photograph shows superficial punctate keratopathy with central subepithelial
and anterior stromal haze. Inset is a retroillumination photograph showing
numerous delicate, thin branching lattice lines throughout the stroma. B, In
anterior cornea tissue, stromal deposits are positive for amyloid (direct fast
scarlet stain). C, Deposits show apple-green birefringence under polarized
light. D, In the basal epithelium, irregularity of cells is observed using in vivo
laser confocal microscopy. E, Another area in the basal epithelium shows
highly reflective reticular extracellular deposits. F, In the Bowman layer, a
subbasal nerve is seen in an increased background. G and H, At the levels of
the superficial and middle stroma, respectively, highly reflective branching
filaments are observed. All are confocal images, 400 ⫻ 400 µm (original
magnification ⫻300). Bar indicates 100 µm.
In patient 9 (with lattice corneal dystrophy type IV), highly
reflective deposits were observed in the Bowman layer
(Figure 3E). In the superficial and middle stroma, highly
reflective lattice-shaped materials were seen (Figure 3F
and H). Some stromal images showed highly reflective
thick, branching deposits (Figure 3G).
In both patients with macular corneal dystrophy (pa-
tients 10 and 11), the epithelial layer appeared normal
(Figure 4C). In the basal epithelial layer and superficial
stroma, highly reflective deposits without distinct bor-
ders were observed (Figure 4D and E). Subepithelial
nerves can partly be seen at the level of Bowman layer
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 A B
C D
E F
G H
Figure 3. Patient 9 (with lattice corneal dystrophy type IV). A, Slitlamp
photograph shows radially oriented thick lattice lines. B, In anterior cornea
tissue, stromal deposits are positive for amyloid (direct fast scarlet stain). C,
Deposits show apple-green birefringence under polarized light. D, The basal
epithelium appears normal. E, In the Bowman layer, highly reflective deposits
are observed using in vivo laser confocal microscopy. F, In the superficial
and middle stroma, highly reflective lattice-shaped materials are observed. G,
Some stromal images show highly reflective, thick branching deposits. H,
Oblique section of the superficial layer shows highly reflective lattice-shaped
materials just beneath the Bowman layer. b indicates Bowman layer;
e, epithelium; and s, anterior stroma. All are confocal images, 400 ⫻ 400 µm
(original magnification ⫻300). Bar indicates 100 µm.
(Figure 4F). In the superficial and middle stroma, ho-
mogeneous reflective materials with dark striaelike im-
ages were observed (Figure 4G and H). Normal kerato-
cytes were not seen. The endothelial layer appeared
normal.
HISTOPATHOLOGIC FINDINGS
In the anterior corneal tissue section from patient 1 (with
Avellino corneal dystrophy), clusters of deposits with ir-
regular edges were observed using Azan stain (Figure 1B).
Some deep stromal deposits were positive for amyloid
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A B
C D
E F
G H
Figure 4. Patient 10 (with macular corneal dystrophy). A, Slitlamp
photograph shows anterior and deep stromal opacities with indistinct
borders. Some gray-white discrete deposits can be seen in the stroma. B, In
anterior cornea tissue, deposits throughout the stroma stain using Alcian
blue, representing the presence of mucopolysaccharide deposits. Deposits
accumulated in subepithelial locations. C, The superficial epithelium appears
normal. D, In the basal epithelium, highly reflective deposits without distinct
borders are observed using in vivo laser confocal microscopy. E, In the
superficial stroma, highly reflective deposits were also seen. F, In a level of
the Bowman layer, subbasal nerves with increased background are observed.
G and H, In the superficial and middle stroma, respectively, homogeneous
reflective materials with dark striaelike images are observed. Normal
keratocytes were not seen. All are confocal images, 400 ⫻ 400 µm (original
magnification ⫻300). Bar indicates 100 µm.
(Figure 1C, direct fast scarlet stain), with apple-green bi-
refringence under polarized light (Figure 1C, inset).
In corneal sections from patients 8 and 9 (with lat-
tice corneal dystrophy), anterior stromal deposits were
positive for amyloid (Figures 2B and 3B, direct fast scar-
let stain). They showed apple-green birefringence un-
der polarized light (Figures 2C and 3C).
In corneal sections from patients 10 and 11 (with macu-
lar corneal dystrophy), deposits throughout the anterior
stroma were positive for Alcian blue (Figure 4B). This rep-
resented the presence of mucopolysaccharide deposits.
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 COMMENT
In this study, we demonstrate in vivo laser confocal mi-
croscopic findings for the first time (to our knowledge)
for 3 genetically mapped corneal stromal dystrophies,
namely, Avellino, lattice, and macular corneal dystro-
phies. Characteristic pathologic microstructures were vi-
sualized noninvasively and with high resolution. In Av-
ellino corneal dystrophy, highly reflective granular
materials with irregular edges were observed in the su-
perficial stroma. In contrast, in lattice corneal dystro-
phy types I and IV, highly reflective branching fila-
ments were observed in the stroma. In macular corneal
dystrophy, homogeneous reflective materials with dark
striaelike images were observed throughout the stroma,
along with highly reflective deposits in the stroma. Be-
cause observations obtained using in vivo laser confocal
microscopy are unique to each stromal dystrophy, we con-
clude that this modality can differentiate these stromal
dystrophies in vivo.
In vivo laser confocal microscopic characteristics have
recently been reported for the following 2 genetically
proven Bowman layer dystrophies: Thiel-Behnke cor-
neal dystrophy (dystrophy of Bowman layer and super-
ficial stroma type II [TGFBI R555Q]) and Reis-Bücklers
corneal dystrophy (dystrophy of Bowman layer and su-
perficial stroma type I [TGFBI R124L]).12 In Thiel-
Behnke corneal dystrophy, deposits in the epithelial basal
cell layer showed homogeneous reflectivity with round-
shaped edges accompanying dark shadows. In contrast,
deposits in the same cell layer for patients with Reis-
Bücklers corneal dystrophy showed high reflectivity from
small granular materials without shadows. In each dys-
trophy, the Bowman layer was totally replaced with patho-
logic material; reflectivity was much higher in Reis-
Bücklers corneal dystrophy than in Thiel-Behnke corneal
dystrophy. It was concluded that in vivo laser confocal
microscopy can differentiate Thiel-Behnke and Reis-
Bücklers corneal dystrophies in vivo; differentiation is
impossible using conventional white-light confocal mi-
croscopy because of limited resolution.4 The small granu-
lar materials with high reflectivity in the epithelial basal
layer in Reis-Bücklers corneal dystrophy are similar to
those observed in the present study in Avellino corneal
dystrophy in shape and laser light reflectivity. Mashima
et al investigated histologic features of genetically proven
Reis-Bücklers corneal dystrophy and proposed that it is
histologically a “superficial variant of granular corneal
dystrophy.”13(p92) In contrast, Avellino corneal dystro-
phy, also referred to as combined granular-lattice cor-
neal dystrophy, is a variant of granular corneal dystro-
phy that has histologic features of lattice and granular
corneal dystrophies. 14 Because Avellino and Reis-
Bücklers corneal dystrophies have histologic features of
granular dystrophy, it is not surprising that they have simi-
lar laser confocal images. In vivo laser confocal micros-
copy is able to differentiate these 2 histologically similar
dystrophies because there is no apparent stromal involve-
ment in Reis-Bücklers corneal dystrophy.
In our study, histologic sections from patients with
lattice corneal dystrophy showed deposition in the su-
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perficial stroma that was positive for amyloid staining and
demonstrated apple-green birefringence under polar-
ized light, confirming a previous report.15 Using in vivo
laser confocal microscopy, these lattice lines were ob-
served as highly reflective branching filaments, consis-
tent with slitlamp biomicroscopic and histologic find-
ings. A previous in vivo white-light confocal microscopic
study2 of lattice corneal dystrophy type I showed punc-
tiform structures and highly reflective irregular materi-
als in the epithelial and Bowman layers, with the stroma
containing reflective filaments up to 50 µm in diameter
with blurred edges and characteristic reflective branch-
ing filaments 80 to 100 µm in diameter. Chiou et al3 re-
ported that white-light confocal microscopy of a cornea
with lattice corneal dystrophy revealed linear and branch-
ing structures in the stroma measuring approximately 40
to 80 µm in width with changing reflectivity and poorly
demarcated margins. These observations are consistent
with our findings obtained using in vivo laser confocal
microscopy. However, in this study we tested only 1 pa-
tient each with lattice corneal dystrophy type I and type
IV. Further analysis using multiple patients with lattice
corneal dystrophy is required to fully understand the in
vivo histologic features of this type of dystrophy, as some
corneal dystrophies are known to represent several dif-
ferent phenotypes clinically, even with the same genetic
mutation.
Herein, histologic sections from patients with macu-
lar corneal dystrophy showed deposits throughout the
cornea that were positive for Alcian blue, representing
the presence of mucopolysaccharides as previously re-
ported.10 In vivo laser confocal microscopy showed ho-
mogeneous reflective materials throughout the stroma
(Figure 4G), which may represent the diffuse stromal
opacity of macular corneal dystrophy. In contrast, the
highly reflective deposits observed in the epithelial basal
cell layer and superficial stroma (Figure 4D and E) may
correspond to the scattered gray-white discrete deposits
as seen using the slitlamp. Numerous dark striaelike im-
ages were observed in the stroma in both patients. These
striaelike images are not indentation lines from the flat
microscope lens cap (TomoCap), as the images were pre-
sent without any cap pressure. In vivo white-light con-
focal microscopic observation of similar dark striae was
previously reported among stromal materials with high
reflectivity in the posterior stroma adjacent to the endo-
thelium in patients with central cloudy dystrophy of
François.16 The significance of these dark striae remains
unclear.
In conclusion, in vivo laser confocal microscopy is ca-
pable of visualizing with high resolution the microstruc-
tural changes related to 3 types of genetically mapped cor-
neal stromal dystrophy. These results suggest that this
technique may be valuable in the differential diagnosis
of corneal stromal dystrophies, particularly when diag-
nosis is uncertain. It may also be useful for further re-
search into corneal dystrophies, especially to follow their
natural courses.
Submitted for Publication: January 3, 2007; final revi-
sion received February 19, 2007; accepted February 21,
2007.
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Correspondence: Akira Kobayashi, MD, PhD, Depart-
ment of Ophthalmology, Kanazawa University Gradu-
ate School of Medical Science, 13-1 Takara-machi, Ka-
nazawa-shi, Ishikawa-ken 920-8641, Japan (kobaya
@kenroku.kanazawa-u.ac.jp).
Author Contributions: Dr Kobayashi had full access to all
the data in the study and takes responsibility for the in-
tegrity of the data and the accuracy of the data analysis.
Financial Disclosure: None reported.
REFERENCES
1. Cavanagh HD, Petroll WM, Alizadeh H, et al. Clinical and diagnostic use of in vivo
confocal microscopy in patients with corneal disease. Ophthalmology. 1993;
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in Bowman and stromal corneal dystrophies. Ophthalmology. 1999;106(9):
1697-1704.
3. Chiou AG, Beuerman RW, Kaufman SC, Kaufman HE. Confocal microscopy in
lattice corneal dystrophy. Graefes Arch Clin Exp Ophthalmol. 1999;237(8):
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4. Kobayashi A, Sakurai M, Shirao Y, et al. In vivo confocal microscopy and geno-
typing of a family with Thiel-Behnke (honeycomb) corneal dystrophy. Arch
Ophthalmol. 2003;121(10):1498-1499.
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From the Archives of the Archives

There were innumerable articles during the past cen-

tury warning against probing the nasolacrimal duct in
cases of dacryocystitis in infancy.
In the cases of dacryocystitis in which early probing
was used recovery was prompt, and no untoward re-
sults of injury were experienced. In the American or the
foreign literature I could find expressed only fears as to
what might happen with early probing, and no evi-
dence to substantiate the belief that injury resulted from
early instrumentation. In my own cases, and in those of
the ophthalmic literature, probing the duct (like push-
ing a stylet through an obstructed hypodermic needle)
cleared the dacryocystitis in most instances with a single
probing.
Reference: Cassady JV. Dacryocystitis of infancy: a re-
view of one hundred cases. Arch Ophthalmol. 1948;39:
491, 507.

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