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ARTICLE

Correlation Between Recurrent Subconjunctival Hemorrhages


and Conjunctivochalasis by Clinical Profile and Successful
Surgical Outcome
Yasuaki Yamamoto, M.D., Ph.D., Norihiko Yokoi, M.D., Ph.D., Miki Ogata, M.D., Ph.D., Atsushi Shiraishi, M.D., Ph.D.,
Masahiko Yamaguchi, M.D., Ph.D., Toshihiko Uno, M.D., Ph.D., Kayoko Inagaki, M.D., Kozaburo Hayashi, M.D., Ph.D.,
Shigeru Kinoshita, M.D., Ph.D., and Yuichi Ohashi, M.D., Ph.D.

including essential hypertension, diabetes mellitus, and hemato-


Objective: To characterize the clinical profile of patients with recurrent
subconjunctival hemorrhages (SCHs) and evaluate the effect of conjuncti-
logic abnormalities have differed.1–7
vochalasis (CCh) surgery on disease recurrences. In 1942, Hughes8 reported that SCHs occurred frequently in
Methods: Three hundred and sixty-two patients with SCHs (mean age, patients with conjunctivochalasis (CCh). Di Pascuale et al.9 sug-
56.4616.0 years) were enrolled in this multicenter epidemiologic study. gested that the frequency of SCHs increased with CCh. Mimura
The severity of CCh, lifestyle at the time of SCH onset, and the frequency et al.10 expanded on this by reporting that patients with SCH
of previous SCHs were compared. Thirty-eight patients with 2 or more showed more severe CCh compared with controls. Thus, CCh
episodes of SCHs (mean age, 68.268.9 years) underwent surgery for has been considered a principal cause of SCH.
CCh. The effectiveness of surgery was evaluated by comparing the fre- Although recurrent bleeding is a feature of SCHs, the clinical
quency of SCH preoperatively and postoperatively. profile of the affected patients has not been well described. In this
Results: Patients with three or more recurrent SCHs showed a significantly
study, we investigated the prevalence and the clinical manifes-
(P¼0.003) higher grade of CCh and tended to be engaged in activities that
require visual concentration, such as watching a visual display terminal,
tations of recurrent SCHs in a prospective, multicenter epidemio-
knitting, reading, and driving. More than 80% of eyes that underwent logic survey and determined the effect of surgery for treating CCh.
surgery to CCh showed no recurrence of the hemorrhages, and the fre-
quency of SCH significantly (P,0.0001) decreased postoperatively.
Conclusions: Moderate or severe CCh and activities that may cause dry eye MATERIALS AND METHODS
can be considered to be risk factors for recurrent SCHs. Surgery to treat This study adhered to the tenets of the Declaration of Helsinki.
CCh is a useful option for patients with frequent recurrences of SCHs.
Each patient provided oral informed consent. The Institutional
Key Words: Recurrent subconjunctival hemorrhages—Conjunctivochalasis Review Board of each hospital approved this study.
surgery—Correlation.
Prospective Epidemiologic Study of SCH
(Eye & Contact Lens 2015;41: 367–372) The study group included 362 patients (171 men, 191 women;
mean age6standard deviation [SD], 56.4616.0 years). The partic-
ipants were outpatients at 23 university-affiliated hospitals and had

S ubconjunctival hemorrhage (SCH), an extremely common


conjunctival disorder, generally occurs in middle-aged or
elderly individuals and usually resolves within 1 to 2 weeks without
been examined over a 6-month period. Patients who experienced
acute conjunctivitis or ocular trauma with signs of conjunctival
infection or inflammation of the anterior segment were excluded
visual impairment.1–5 Fukuyama et al.3 reported that the etiology of based on slitlamp examination by an ophthalmologist. Patients
SCHs was unknown in half of the patients despite extensive phys- with a history of ocular surgery or trauma, the Valsalva maneuver,
ical examinations and laboratory testing. The results of a number of or systemic diseases, including essential hypertension, diabetes
studies designed to identify a relationship with systemic disorders, mellitus, and hematologic disorders, were excluded based on pre-
liminary interview or medical records.
Before the examination, the patients completed a questionnaire
From the Department of Ophthalmology (Y.Y., M.O., A.S., M.Y., T.U., that recorded the location of the hemorrhage and the frequency of
K.H., Y.O.), Ehime University Graduate School of Medicine, Ehime, Japan;
and Department of Ophthalmology (N.Y., K.I., S.K.), Kyoto Prefectural SCHs during the previous year. The patients were divided into
University of Medicine, Kyoto, Japan. three groups according to the frequency of the previous SCHs:
The authors have no funding or conflicts of interest to disclose. group 1, the current SCH was the first episode; group 2, the current
Y. Yamamoto and N. Yokoi contributed equally to this study. SCH was the second episode; and group 3, the current SCH was
Address correspondence to Yasuaki Yamamoto, M.D., Ph.D., Depart-
ment of Ophthalmology, Ehime University Graduate School of Medicine,
one of three or more episodes.
Shitsukawa, Toon, Ehime 791-0295, Japan; e-mail: yyasuaki@m.ehime-u. The patients’ lifestyle or behavior near the time of onset of current
ac.jp bleeding was asked in the questionnaire and classified by the con-
Accepted January 6, 2015. tents as follows: “keeping late hours or being sleep-deprived,”
DOI: 10.1097/ICL.0000000000000139 “activities that require visual concentration (such as watching a visual

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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.

Effect of Surgery to Treat Conjunctivochalasis


Forty-two eyes of 38 patients (4 men, 34 women; average age, RESULTS
68.268.9 years) with 2 or more episodes of SCHs over the pre- Epidemiologic Survey of Recurrent SCH
vious year underwent surgery to treat CCh. The patients showed Most patients were between 40 and 70 years of age, with a peak
grade 2 or 3 CCh with no systemic disorders. The surgery was in the 60s (Fig. 1). Most patients (n¼254) were in group 1, fol-
suitable for treating all types of CCh and included four basic steps. lowed by 66 patients in group 2, and 42 patients in group 3. The
Briefly, step 1, an arc-like incision was made parallel to and 2.0 patients in group 3 were from 40 to 70 years of age. The average
mm from the limbus in the bulbar conjunctiva; step 2, Tenon’s patient age in group 3 (62.169.2 years) was significantly
capsule was removed; step 3, four radial cuts were made along (P¼0.031, by the Steel–Dwass multiple comparison tests) older
the first incision to remove the excisable redundancy in each area; than that in group 1 (54.8617.3 years) (Fig. 1).
and step 4, the incision was sutured.12,13 The patients were fol- The most common site of bleeding was the temporal interpalpebral
lowed postoperatively for 1 to 4 years and 7 months (average, 2 area (39.8%), followed by the nasal interpalpebral area (28.2%), and
years and 9 months). The frequency of the hemorrhages was the temporal side of the lower lid margin (15.5%) (Fig. 2). Hemor-
grouped based on patient recollection from the first awareness of rhages in the interpalpebral area (69.3%) were more prevalent than in
a SCH to the time of surgery: group T1, 1 to 2 times; group T2, 3 to the upper and lower lid margins (4.4% and 26.2%, respectively)
4 times; group T3, 5 to 9 times; and group T4, more than 10 times. (Table 1). The SCHs recurred in 108 cases (29.8% in groups 2 and
The sizes of the hemorrhages before and after surgery were 3). The sites of the hemorrhages were the same in 40 cases, different
described as follows: small, a hemorrhage covering only part of in 17 cases, either the same or different in 7 cases, and unknown in 44
one side of the bulbar conjunctiva; medium, a hemorrhage cover- cases (Table 1); thus, approximately 62.5% (40 of 64 cases) or more
ing one side of the bulbar conjunctiva; large, a hemorrhage cover- cases experienced bleeding that recurred at the same site.
ing one side of the bulbar conjunctiva and extending into the other Most of the patients with a SCH showed grade 1 or 2 CCh,
side; and varied, multiple hemorrhages that varied in size. whereas patients in group 3 showed a significantly (P¼0.003, by

FIG. 1. Age distribution of cur-


rent SCH and the frequency of
history of hemorrhagic episodes.
The patients were divided into 3
groups according to the fre-
quency of the previous SCHs:
group 1 (254 cases, 70.2%), the
current SCH was the first episode;
group 2 (66 cases, 18.2%), the
current SCH was the second epi-
sode; and group 3 (42 cases,
11.6%), the current SCH was 1 of
3 or more episodes. The Steel–
Dwass multiple comparison test
was used to compare the mean
patient age of these groups.
*P¼0.031. SCH, subconjunctival
hemorrhages.

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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

TABLE 1. Clinical Profile of Patients With Recurrent Subconjunctival Hemorrhages


Total Group 1 Group 2 Group 3 Estimate Standard Error P

Number of subjects 362 254 66 42


Sex
Men 171 127 29 15
Women 191 127 37 27 0.181 0.120 0.131
Age (y) 56.4616.0 54.8617.3 59.2612.8 62.169.2
CCh grade 1.5760.75 1.5160.75 1.6160.68 1.9060.79
Grade (0–1) 20.362 0.495 0.464
Grade (1–2) 0.760 0.272 0.005a
Grade (2–3) 0.120 0.402 0.765
Lifestyle at the time of bleeding, n (% in each groups)
Keeping late hours or sleep-deprived 86 (23.8) 56 (22.0) 20 (30.3) 10 (23.8) 0.078 0.134 0.561
Activities that require visual concentration 78 (21.5) 48 (18.9) 13 (19.7) 17 (40.5) 0.307 0.135 0.023a
Shoulder stiffness 27 (7.5) 18 (7.1) 5 (7.6) 4 (9.5) 0.097 0.217 0.653
Excessive alcohol drinking 19 (5.2) 13 (5.1) 5 (7.6) 1 (2.4) 0.170 0.267 0.525
Symptom at the time of bleeding, n (% in each groups)
Pain or foreign-body sensation in the eye 58 (16.0) 36 (14.2) 10 (15.2) 12 (28.6) 0.223 0.150 0.136
Sites of hemorrhage, n (% in each groups)
Upper lid margin 16 (4.4) 11 (4.3) 3 (4.5) 2 (4.8)
Interpalpebral 251 (69.3) 174 (68.5) 47 (71.2) 30 (71.4)
Lower lid margin 95 (26.2) 69 (27.2) 16 (24.2) 10 (23.8)
Site of recurrent hemorrhage (% in each groups)
Same — — 24 (36.4) 16 (38.1)
Different — — 14 (21.2) 3 (7.1)
Either — — — 7 (16.7)
Unknown — — 28 (42.4) 16 (38.1)
a
Multiple ordinal logistic regression analysis.
CCh, conjunctivochalasis.

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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

TABLE 2. Clinical Profile of Patients With Eyes of CCh Grade“0&1” or “2&3”


CCh Grade“0&1” Total Group 1 Group 2 Group 3 Estimate Standard Error P

Number of subjects 155 121 25 9


Sex
Men 80 66 10 4
Women 75 55 15 5 0.281 0.218 0.199
Age (y) 49.7617.0 48.7618.5 53.2610.3 54.867.6 20.020 0.014 0.162
Lifestyle at the time of bleeding, n (% in each groups)
Keeping late hours or sleep-deprived 30 (19.4) 24 (19.8) 5 (20.0) 1 (11.1) 20.267 0.273 0.328
Activities that require visual concentration 33 (21.3) 21 (17.4) 7 (28.0) 5 (55.6) 0.660 0.234 0.005a
Shoulder stiffness 14 (9.0) 9 (7.4) 4 (16.0) 1 (11.1) 0.218 0.314 0.487
Excessive alcohol drinking 9 (5.8) 6 (5.0) 3 (12.0) 0 (0.0) 0.765 0.416 0.066
Symptom at the time of bleeding, n (% in each groups)
Pain or foreign-body sensation in the eye 19 (12.3) 12 (9.9) 5 (20.0) 2 (22.2) 0.484 0.272 0.076

CCh Grade“2&3” Total Group 1 Group 2 Group 3 Estimate Standard Error P

Number of subjects 207 133 41 33


Sex
Men 91 61 19 11
Women 116 72 22 22 0.099 0.150 0.510
Age (y) 61.4613.1 60.3614.1 62.8612.9 64.168.6 20.020 0.012 0.090
Lifestyle at the time of bleeding, n (% in each groups)
Keeping late hours or sleep-deprived 56 (27.1) 32 (24.1) 15 (36.6) 9 (27.3) 0.250 0.167 0.133
Activities that require visual concentration 45 (21.7) 27 (20.3) 6 (14.6) 12 (36.4) 0.176 0.170 0.300
Shoulder stiffness 13 (6.3) 9 (6.8) 1 (2.4) 3 (9.1) 20.032 0.304 0.915
Excessive alcohol drinking 10 (4.8) 7 (5.3) 2 (4.9) 1 (3.0) 20.092 0.364 0.800
Symptom at the time of bleeding, n (% in each groups)
Pain or foreign-body sensation in the eye 39 (18.8) 24 (18.1) 5 (12.2) 10 (30.3) 0.116 0.182 0.524
a
Multiple ordinal logistic regression analysis.
CCh, conjunctivochalasis.

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Eye & Contact Lens  Volume 41, Number 6, November 2015 Hemorrhages and Conjunctivochalasis

FIG. 4. Surgery to treat CCh decreases


the frequency and size of hemorrhages
before and after surgery. The frequency
(A) and size (B) of hemorrhages before
surgery were plotted against those after
surgery, with individual patients repre-
sented by single dots. The Wilcoxon
signed-rank test was used to compare
preoperative and postoperative status
(P,0.0001). CCh, 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

ACKNOWLEDGMENTS 10. Mimura T, Usui T, Yamagami S, et al. Subconjunctival hemorrhage and


The authors thank Dr. Shoko Iwaki for editing the article. conjunctivochalasis. Ophthalmology 2009;116:1880–1886.
11. Höh H, Schirra F, Kienecker C, et al. Lidparrallele konjunktivale Falten
(LIPCOF) sind ein sicheres diagnostisches Zeichen des trockenen Auges [in
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