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Eye & Contact Lens Volume 41, Number 6, November 2015 367
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Y. Yamamoto et al. Eye & Contact Lens Volume 41, Number 6, November 2015
display terminal, knitting, reading, and driving),” “excessive drink- Statistical Analyses
ing of alcohol,” and “shoulder stiffness.” The items that applied to The Steel–Dwass multiple comparison tests were used to com-
more than 5% (19 patients) were analyzed. pare the average patient age with the CCh grades in the three
An ophthalmologist at each university-affiliated hospital exam- groups of SCHs. Chi-square test was used to compare patients’
ined the location and extent of the SCH by slitlamp biomicroscopy. rates of the answered questionnaire in the three groups. The num-
Conjunctivochalasis was assessed by fluorescein dye staining at the bers and the sizes of the hemorrhages before and after the surgery
lower lid margin according to grading of lid-parallel conjunctival were compared using the Wilcoxon signed-rank test. Ordinal logis-
folds on a scale of 0 to 3 as described by Höh et al.,11 with tic regression analysis was applied to estimate the recurrent risk
0 indicating no persistent fold; 1, one small fold; 2, more than factors in the three groups. The results were analyzed using JMP
two folds not higher than the tear meniscus, and 3, multiple folds software (version 10.0; SAS Institute, Inc., Cary, NC). P,0.05 was
higher than the tear meniscus. considered statistically significant.
368 Eye & Contact Lens Volume 41, Number 6, November 2015
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Eye & Contact Lens Volume 41, Number 6, November 2015 Hemorrhages and Conjunctivochalasis
FIG. 2. Hemorrhagic sites. The numbers in the circles and ellipses represent the number of SCH cases.
The location was assigned one site based on the center of the extent of the hemorrhage. The sizes of the
ellipses and/or circles show the relative frequency of the SCHs. The center circle corresponds to the
cornea. SCH, subconjunctival hemorrhages.
the Steel–Dwass multiple comparison test) higher grade of CCh Fifty-eight patients (16.0%) experienced pain or a foreign-body
(mean CCh grades, 1.9060.79, compared with patients in group 1 sensation in the eye at the time of bleeding (Table 1). Patients in
[1.5160.75]) (Fig. 3). group 3 experienced significantly (P¼0.042, by the x2 test) more
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Y. Yamamoto et al. Eye & Contact Lens Volume 41, Number 6, November 2015
FIG. 3. The CCh grades in SCH. Conjunctivochalasis was assessed at the lower lid margin as follows: 0, no persistent fold; 1, one small fold; 2,
more than two folds not higher than the tear meniscus; and 3, multiple folds higher than the tear meniscus. The percentages of the CCh grades in
362 patients (total) and for the 3 groups based on the frequency of the previous episodes of SCHs were shown on the y-axis. The CCh grade was
analyzed by the Steel–Dwass multiple comparison test. *P¼0.003. CCh, conjunctivochalasis; SCH, subconjunctival hemorrhages.
pain or foreign-body sensations than the patients in groups 1 Multiple ordinal logistic regression analysis showed that a dif-
and 2. ference between CCh grade 1 and 2 (P¼0.005) and participation in
About a quarter of patients reported either keeping late hours or the activities that require visual concentration (P¼0.023) was sig-
being sleep-deprived or engaged in an extended period of activities that nificantly related to the order of the 3 groups (Table 1).
require visual concentration, such as watching a visual display terminal, Because we considered that a difference between CCh grade 1 and 2
knitting, reading, and driving. Some patients reported shoulder stiffness of the eyes can affect the order of the recurrent groups, these eyes were
or excessive drinking of alcohol (Table 1). Patients in group 3 reported categorized into 2 new groups: CCh grade“0&1” (155 eyes; mean
engaging in more activities that require visual concentration than those age6SD, 49.7617.0 years) and CCh grade“2&3” (207 eyes;
in the other two groups (P¼0.008 by the x2 test). 61.4613.1 years), and were analyzed by multiple ordinal logistic
370 Eye & Contact Lens Volume 41, Number 6, November 2015
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Eye & Contact Lens Volume 41, Number 6, November 2015 Hemorrhages and Conjunctivochalasis
regression analysis. In the eyes with CCh grade“0&1,” participation in Furthermore, it was revealed that the activity that requires visual
the activities that require visual concentration (P¼0.005) was signifi- concentration is a risk factor of recurrent SCHs in the eyes with mild
cantly related to the order of the 3 groups, but it was not in the eyes to moderate CCh, which corresponds to CCh score 0 or 1. These
with CCh grade“2&3” (P¼0.300) (Table 2). patients are relatively young in the entire patient group and should
have well-maintained tension of the orbicular and superior levator
Effect of Surgery for Conjunctivochalasis muscles; they are therefore expected to have stronger friction against
Postoperatively, more than 80% of eyes that underwent surgery superficial conjunctival vessels during blinking than the elderly.
showed no recurrences of the hemorrhages during the follow-up However, SCH does not occur every time they blink, and there must
period for 1 to 4 years and 7 months (average, 2 years and 9 be some other causes of recurrent SCHs in these patients. The
months). The frequency and size of the hemorrhages markedly activities that require visual concentration are characterized by
decreased (P,0.0001, by the Wilcoxon signed-rank test) after sur- reduced blinking that promotes tear film evaporation.14–18 The pres-
gery (Fig. 4A,B). ence of CCh aggravates the extent of the dry eye by occupying the
lower tear meniscus.9,12,13,19 As a result, increased friction at the time
of blinking induces stretching of the conjunctival vessels and may
DISCUSSION eventually lead to blood vessel rupture.
The current results are consistent with those of Mimura et al.10 The bleeding was most prevalent in the temporal area of the
who reported the association between the severity of CCh and the interpalpebral zone followed by the nasal area of the interpalpebral
occurrence of SCHs. In the present study, recurrent SCHs devel- zone, the temporal area of the lid margin, and the nasal area of the
oped in approximately 30% of the patients most prevalently lid margin. Most patients with recurrent SCHs experienced
between the ages of 40 and 70 years. Patients with three or more bleeding at the same site, which may indicate that a certain
recurrent SCHs (in group 3) showed a higher grade of CCh. anatomic characteristic susceptible to bleeding must be present in
Hughes8 first addressed the association of CCh with SCH. Since these individuals. Around the limbus, the anterior ciliary artery
then, a possible relationship between SCHs and CCh has been provides numerous branches, some of which bend as recurrent
reported repeatedly.9,10 In our study, the association between branch vessels and communicate with the posterior conjunctival
CCh and SCHs was strongly supported by the successful surgical arteries.20 Because the recurrent branch vessels are fixed firmly at
outcomes in the patients with recurrent SCHs. The frequency and the limbus, mechanical stress on these vessels presumably can be
the degree of the hemorrhages were markedly suppressed by a sim- exaggerated to the rupturable point.
ple band-form resection of redundant bulbar conjunctiva in the The frequency of SCH decreased in the patients in the ninth
lower portion. Therefore, the success of this surgery was not due decade of life. The reason for this is unclear. One explanation may
to direct excision of the bleeding site, but rather by the decreased be related to the tension of the orbicular and superior levator
friction during blinking resulting from adhesion of redundant con- muscles that is reduced by sagging eyelids in patients over 80 years
junctiva to the scleral surface. of age. The friction is decreased with blinking and may not produce
In CCh, the bulbar conjunctiva adheres poorly to the sclera. The substantial stress on the conjunctival vessels.
bulbar conjunctiva and superficial blood vessels are compressed In conclusion, the current study showed that moderate or severe
because of the friction of the upper lid during eye closing. As a result, CCh and activities that may cause dry eye can be considered to be
superficial conjunctival blood vessels tend to stretch with blinking. In risk factors for recurrent SCHs by enhanced friction on ocular
support of this friction hypothesis, approximately 16% of the current surface. Surgery to treat CCh can markedly suppress the recurrent
patients reported in the questionnaire that they experienced a foreign- hemorrhages and is a good and reasonable option for patients with
body sensation in the eye at the onset of the disease. frequent recurrences of SCHs.
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Y. Yamamoto et al. Eye & Contact Lens Volume 41, Number 6, November 2015
372 Eye & Contact Lens Volume 41, Number 6, November 2015
Copyright @ Contact Lens Association of Opthalmologists, Inc. Unauthorized reproduction of this article is prohibited.