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Minor salivary glands and labial mucous membrane
graft in the treatment of severe symblepharon and dry
eye in patients with StevenseJohnson syndrome
Ana Estela B P P Sant’ Anna,
1
Rossen M Hazarbassanov,
2
Denise de Freitas,
2
Jose
´A
´lvaro P Gomes
2
ABSTRACT
Objective To evaluate minor salivary glands and labial
mucous membrane graft in patients with severe
symblepharon and dry eye secondary to
StevenseJohnson syndrome (SJS).
Methods A prospective, non-comparative, interventional
case series of 19 patients with severe symblepharon and
dry eye secondary to SJS who underwent labial mucous
membrane and minor salivary glands transplantation. A
complete ophthalmic examination including the Schirmer
I test was performed prior to and following surgery. All
patients had a preoperative Schirmer I test value of zero.
Results Nineteen patients with severe symblepharon and
dry eye secondary to SJS were included in the study. There
was a statistically significant improvement in the best
spectacle-corrected visual acuity in eight patients (t test;
p¼0.0070). Values obtained in the Schirmer I test
improved significantly in 14 eyes (73.7%) 6 months
following surgery (
c
2
test; p¼0.0094). A statistically
significant increase in tear production (Schirmer I test) was
found in eyes that received more than 10 glands per graft
compared with eyes that received fewer glands (
c
2
test;
p¼0.0096). Corneal transparency improved significantly in
11 (72.2%) eyes and corneal neovascularisation improved
significantly in five eyes (29.4%) (McNemar test; p¼0.001
and p¼0.0005). The symptoms questionnaire revealed
improvement in foreign body sensation in 53.6% of the
patients, in photophobia in 50.2% and in pain in 54.8%
(KruskaleWallis test; p¼0.0167).
Conclusion Labial mucous membrane and minor
salivary glands transplantation were found to constitute
a good option for the treatment of severe symblepharon
and dry eye secondary to SJS. This may be considered
as a step prior to limbal stem cell and corneal
transplantation in these patients.
INTRODUCTION
StevenseJohnson syndrome (SJS), also known as
erythema multiforme major, is an acute inflamma-
tory reaction involving the skin and mucous
membranes, characterised by the eruption of vesicles
and bullae, with cicatricial abnormalities developing
in the affected areas during the healing phase. The
syndrome is commonly associated with a causative
agent, usually a drug or an infectious process.
1
Ocular involvement occurs in about two-thirds of
cases and consists of severe mucopurulent, membra-
nous or pseudomembranous, diffuse, bilateral
conjunctivitis. The troubling ophthalmic complica-
tions occur during the chronic recovery phase.
The conjunctival inflammation with membrane or
pseudomembrane formation may lead to cicatricial
changes in the conjunctiva and destruction of the
limbal epithelial stem cells, resulting in symble-
pharon, entropion, trichiasis, tear film abnormalities,
keratinisation and corneal neovascularisation.
2 3
Management of the acute ocular process requires
the use of both oral and topical steroids. Additional
procedures that may be carried out include the
aggressive use of doughnut-shaped conformers,
daily lysis of adhesions, and the introduction of
plastic wrap or amniotic membrane into the fornix
to prevent the formation of symblepharon. Long-
term management includes the use of topical
lubricants to supplement the patient’s tear produc-
tion as well as surgical correction of entropion,
trichiasis and symblepharon. Limbal stem cell and
corneal transplantation may be indicated in cases in
which there is a total limbal stem cell deficiency
and corneal opacification. However, the develop-
ment of severe dry eye and cicatricial changes often
jeopardises functional and visual outcome.
4
Denig (1911) was the first to describe mucous
membrane grafting for the treatment of symble-
pharon.
5 6
Since then, mucous membrane grafting
has been popularised as one of the most effective
methods of treating different eyelid and conjunc-
tival disorders such as symblepharon, entropion,
ectropion and pterygium.
The use of salivary glands as a source of lubri-
cation to treat severe cases of dry eye has been
advocated since 1951, when it was proposed by
Filatov and Chevaljev, who described trans-
plantation of the Stensen’s duct in the parotid
gland to the conjunctival fornix with the objective
of replacing tears with salivary secretion. However,
complications such as excess tearing and parotiditis
limited its functional outcome.
7
In 1986, Murube-del-Castillo proposed the
submandibular gland transplantation as a better and
less invasive alternative.
8
In 1997, that same author
described transplantation of a minor salivary gland as
an option for the treatment of severe dry eyes.
19
Minor oral salivary glands exist in large numbers in
the labial, buccal and palatal mucosa, and account for
approximately half the baseline secretion of saliva.
They can be transplanted together with the overlying
mucosa as a complex graft to the posterior lamella of
the eyelids in other to increase ocular surface and
reduce discomfort in patients with dry eye.
The purpose of the present study was to evaluate
salivary gland and labial mucous membrane graft
in patients with severe symblepharon and dry eye
secondary to SJS.
1
Oculoplastic Unit, Department
of Ophthalmology, Federal
University of Sa˜o Paulo, SP,
Brazil
2
Cornea and External Disease
Unit, Department of
Ophthalmology, Federal
University of Sa˜o Paulo, SP,
Brazil
Correspondence to
Ana Estela B P P Sant’ Anna,
Alameda dos Quinimuras, 34,
Planalto Paulista, Sa˜o Paulo
04068-000, Brazil;
anestela@uol.com.br
Accepted 3 April 2011
Published Online First
27 April 2011
234 Br J Ophthalmol 2012;96:234e239. doi:10.1136/bjo.2010.199901
Clinical science
PATIENTS AND METHODS
In this prospective, non-comparative, interventional case series,
patients who had developed sequelae to the ocular surface and
severe dry eye secondary to SJS were recruited from the Cornea
and External Diseases and Oculoplastic Unit of the Federal
University of Sao Paulo, Sao Paulo School of Medicine, Sao Paulo,
Brazil, between 2006 and 2009.
Only patients with poor visual acuity, 20/100 or worse, and
a Schirmer I test result of zero were included in the study. When
it proved impossible to place the paper strip of the Shirmer test
in eyes with symblepharon or ankyloblepharon, the test was
considered not measurable.
Of all patients with SJS attending the clinic, only those with
a Schirmer test of zero were selected for inclusion in the study. If
the Schirmer test was zero in both eyes, the eye in which
symblepharon was worse, in which visual acuity was poorer
and in which keratinisation was greater was selected. Exclusion
criteria consisted of any active infection and corneal melt or
perforation.
Surgical procedure
The same surgeon (AEBPPS) operated all the patients and general
anaesthesia was used in all cases. A mucotome (Ficas Mucotome,
São Paulo, Brazil) was used to obtain a thin split-thickness graft
to correct symblepharon. Minor salivary glands were obtained en
block from the mucous membrane of the patient’s own upper or
lower lip, above the orbicularis oris muscle. The thin split-
thickness graft of mucous membrane was sutured to the sclera
using absorbable sutures (poliglactyn, 8-0). The minor salivary
glands, attached to the submucosa, were sutured in the superior
and inferior conjunctival fornices using absorbable sutures (poli-
glactyn 8-0) and a transpalpebral 4-0 silk suture. At the end of the
procedure, a scleral shield was placed over the eye and central
blepharorraphy was performed (figure 1).
The following day, the blepharorraphy was opened and
patients were instructed to use eye drops containing dexa-
methasone 0.1% and tobramycin 0.3% four times daily for
7 days. After this period the medication was gradually reduced
over the following 3 weeks until the first removal of the scleral
lens 1 month after surgery. Patients were then instructed to
return to the clinic at weekly intervals, at which time the sclera
lens was removed, rinsed with saline solution and replaced. Cold
saline compresses were prescribed postoperatively for 1 month,
and patients were instructed to apply them more often in the
first 2 days after surgery.
The absorbable sutures (poliglactyn, 8-0) were removed after
7 days and the transpalpebral 4-0 silk suture was removed after
15 days.
It is worth mentioning that this technique differs from that
used by other authors, since in this clinic the treatment of
Figure 1 Surgical steps: (A)
preoperative; (B) obtaining mucous
membrane graft from the lower lip using
a Ficas mucotome; (C) obtaining the
salivary glands; (D) labial mucous
membrane attached to the sclera; (E)
fixing the salivary glands; (F)
postoperative.
Br J Ophthalmol 2012;96:234e239. doi:10.1136/bjo.2010.199901 235
Clinical science
symblepharon and minor salivary gland transplantation is
performed as a single surgical procedure.
Pre- and postoperative evaluation
A complete ophthalmic examination including Schirmer I test,
slit lamp examination, funduscopy whenever possible (if
impossible ocular ultrasonography was then performed) and
measurement of intraocular pressure (using a Goldman tonom-
eter or finger tension) was performed prior to surgery, and 1 and
6 months following surgery. Clinical photographs were also
taken before and after surgery.
The visual acuity of the patients was evaluated before and
after surgery using decimal notation. It the case of patients were
unable to see the visual acuity charts from a distance of 1 m,
visual acuity was assessed by asking them to count the number
of fingers shown by the examiner. If they were unable to do this,
visual acuity was then recorded as the ability to see the
examiner’s hand movements or, in the worse cases, the ability to
perceive light projected into the eye.
10 11
Corneal transparency was evaluated and graded as:
1, completely transparency; 2, hazy; 3, iris partially visible; 4, iris
not visible. Vascularisation of corneal surface was monitored
photographically and graded according to its extent and inten-
sity; grade 1 indicating peripheral vascularisation; grade 2,
peripheral and midperipheral vascularisation; grade 3, modest
vascularisation, involving the entire cornea; and grade 4, massive
vascularisation of the entire cornea.
12
Patients were requested to complete a questionnaire on
symptoms such as foreign body sensation, dryness, photo-
phobia, pain and itching, and eye movements, indicating
to what extent the symptoms had improved following
surgery compared with before surgery. Answers were given on
a scale from 0 to 5 for each symptom, with 0 representing hardly
any improvement and 5 representing great improvement.
13
Six months after surgery, these patients were referred for the
next step: to evaluate reconstruction of the ocular surface with
limbal and corneal transplants.
Statistical analysis
For purposes of statistical analysis, counting fingers was rated as
acuity of 0.004, the perception of hand motion as 0.002 and the
perception of light as 0.001, whereas no perception of light was
ranked as 0.0001. Final postoperative visual acuity was defined
as the visual acuity measured at the most recent visit. These
values were compared with preoperative values using the
non-parametric Wilcoxon signed-rank test.
10
The statistical tests used to compare variables between two
groups were McNemar test of paired proportions, the
c
2
test
with Yates’correction for proportions, Student t test and anal-
ysis of variance. The SPSS statistical software program, version
12 (SPSS Inc., Chicago, Illinois, USA) was used to perform
statistical analysis. p Values <0.05 were considered statistically
significant. The Bonferroni correction was used for repeat tests
to correct for cumulative type I errors.
RESULTS
Nineteen patients with severe symblepharon and dry eye
secondary to SJS were included in the study. Mean age of
patients was 31.5613.9 years (mean6SD).
Of the 40 patients diagnosed with SJS and registered at
corneal diseases unit of the Federal University of São Paulo only
those with severe symblepharon and a Schirmer I test of zero
were selected; however, the rarity of the disease did not allow
patient selection to be limited exclusively to those who had not
undergone any previous surgery.
All patients were submitted to unilateral surgery and there
were no serious intraoperative complications. Two patients
developed hypoesthesia of the lower lip, which improved within
5 months, and one patient had graft decentration that required
a second surgical procedure 2 weeks later. In addition, a second
procedure was required in six patients (31.6%) to correct residual
symblepharon and the cicatricial entropion, while one patient
(5.3%) had to undergo a third surgical procedure to correct the
residual entropion.
Although the surgical procedure to correct symblepharon was
performed at the same time as transplantation of the minor
salivary glands at the same donor site, this had no negative effect
on the final outcome of surgery.
There was a statistically significant improvement in the best
spectacle-corrected visual acuity in eight (42.1%) of the 19
patients after surgery (paired simple t test; p¼0.0070) (table 1,
figures 2 and 3).
Schirmer I test values improved significantly in 14 eyes
(73.68%) when evaluated 6 months after surgery (
c
2
test;
p¼0.0094). In one case, the Schirmer I test improved from 0 to
11 mm in the first month after surgery. In five eyes, the Schirmer
I test result was still zero.
Ten of the 19 patients (52.6%) received 10 salivary glands or
fewer in the submucosal graft, while nine patients (47.4%)
received more than 10 glands. A statistically significant
increase in tear production (according to Schirmer I test) was
found in eyes that received more than 10 glands per graft
compared with eyes that received fewer glands (
c
2
test;
p¼0.0096) (table 2).
Corneal transparency improved significantly in 11 (72.2%) out
of 18 eyes, decreasing in severity from grade 4 to grade 3 within
6 months of surgery (McNemar tests on paired proportions;
p¼0.001) (table 3). Similarly, corneal neovascularisation
improved significantly in 5/17 eyes (29.4%), which decreased in
severity from grade 4 to grade 3 within 6 months of surgery
(McNemar test on paired proportions; p¼0.0005) (table 4).
Table 1 Outcome of salivary gland and labial mucous membrane
transplantation in the treatment of severe symblepharon and dry eye in
patients with StevenseJohnson syndrome
Case no.
Schirmer I test BSCVA (logMAR)
Preoperative Postoperative Preoperative Postoperative
1 0 0 2.398 2.398
2 0 1 2.699 2.699
3 0 2 2.699 2.699
4 0 1 2.699 2.699
5 0 0 2.398 2.398
6 0 3 2.398 2.398
7 0 0 2.699 2.398
8 0 1 2.699 2.398
9 0 3 2.699 2.699
10 0 1 2.398 2.398
11 0 3 3 2.398
12 0 4 2.699 2.398
13 0 0 3 2.699
14 0 11 2.699 2.699
15 0 3 2.398 2.398
16 0 3 3 2.699
17 0 0 3 2.398
18 0 5 3 2.699
19 0 4 0.222 0.222
BSCVA, best spectacle-corrected visual acuity; logMAR, logarithm of the minimum angle of
resolution.
236 Br J Ophthalmol 2012;96:234e239. doi:10.1136/bjo.2010.199901
Clinical science
Eighteen of the 19 patients (94.7%) completed the question-
naire on symptoms in which foreign body sensation, dryness,
photophobia, pain and eye movements were evaluated individ-
ually (table 5). An improvement was found in foreign body
sensation in 53.7% of the patients, in photophobia in 50.2% and
in pain in 54.8% of the patients (KruskaleWallis test; p¼0.0167)
(table 5).
DISCUSSION
Murube-del-Castillo
8
was the first to describe mucous
membrane and minor salivary gland transplantation for the
treatment of severe cases of dry eye syndrome.
6
Soares and
França described a successful outcome with the same surgical
treatment in 21 cases of severe dry eye, 12 (57.1%) of which
occurred secondary to SJS. Surgery consisted of transplantation
Figure 2 Preoperative (A, C, E, G) and
postoperative (B, D, F, H) pairs of
photographs in five patients.
Br J Ophthalmol 2012;96:234e239. doi:10.1136/bjo.2010.199901 237
Clinical science
of salivary glands to the superior conjunctival fornix, with graft
survival and integration into the host tissue in 97.2% of cases.
14
In the present study, only patients with SJS were analysed and
salivary glands were implanted into the superior and inferior
conjunctival fornix. All grafts were still intact 6 months
following surgery.
Several authors have presented different techniques for the
treatment of symblepharon using substitutes for conjunctiva
that range from alloplastic material such as polytetrafluo-
ethylene to nasal or amniotic membranes, egg membrane, rectal
mucosa, preputial mucosa and maxillary sinus mucosa. The
most popular technique is the use of oral mucosa and the
outcome is successful in about 85e100% of cases of symble-
pharon. In the present study, symblepharon was corrected with
the use of oral mucous membrane graft.
5615e25
One of the difficulties found in operating on these patients
was the cicatricial changes found in their eyes and oral mucosa,
which were probably caused by the disease itself and by previous
surgeries (18 of the 19 patients reported having previous
surgeries to corrected symblepharon, trichiasis and entropion). It
is possible that if this surgery had been performed in naïve eyes,
more salivary glands could have been transplanted, with less
conjunctival cicatrisation and a better outcome.
It was surprising that the number of salivary glands was
sufficient for transplantation in more than 50% of the patients
with SJS in the present study. Compared with cicatricial
diseases, prognosis may be poorer in the case of diseases such as
Sjögren’s syndrome that affect the salivary glands. SJS and
ocular cicatricial penphigoid are more severe than Sjögren’s
syndrome because of the cicatricial changes.
The Schirmer I test improved in 14/19 eyes (73.7%). Greater
tear production was observed in patients who received submu-
cosal grafts containing more than 10 glands. Although difficult
to estimate, it is reasonable to assume that this variable would
interfere directly with clinical outcome and this assumption was
confirmed by the finding in the present study that lubrication
was better in eyes that received more glands per graft.
Corneal transparency and neovascularisation improved in
11/19 eyes (72.2%) and 5/19 eyes (29.4%), respectively,
6 months after mucous membrane and salivary gland trans-
plantation. These results may explain the improvement in best
spectacle-corrected visual acuity in 8/19 eyes (42.1%).
It must be emphasised that the sample population in the
present study was very homogeneous compared with those in
other similar studies. All the patients had a value of zero in an
initial Schirmer I test and achieved an improvement in the
regularity of the ocular surface and in humidity. It is also
important to take into consideration the fact that salivary
secretion is denser and the Schirmer I test values may therefore
have been underestimated following surgery.
The results of the questionnaire showed an improvement in
symptoms, foreign body sensation improving in 53.6%, photo-
phobia in 50.2% and pain in 54.8% of cases. This may be related
to the correction of symblepharon and cicatricial entropion,
which improved eye movement and decrease foreign body
sensation.
Figure 3 Preoperative versus final visual acuity. CF, counting fingers;
HM, hand movements; LP, light perception; NLP, no light perception.
Table 2 Schirmer I test (without anaesthesia) 6 months
postoperatively
Schirmer I[0 Schirmer I £2 Schirmer I >2
c
2
test p value
Glands (<10) 40.0 (4/10) 30.0 (3/10) 30.0 (3/10) 0.8607
Glands (>10) 10 (1/10) 20.0 (2/10) 70 (7/10) 0.0096
c
2
test p value 0.3017 1.0 0.1797 0.371
Table 4 Corneal neovascularisation
Neovascularisation, % (n/n)
Preoperative Postoperative
Grade 3 0.0 (0/17) 29.4 (5/17)
Grade 4 100.0 (17/17) 70.6 (12/17)
McNemar test (paired proportions); p¼0.0005.
Table 5 Symptoms questionnaire results
Case no. FBS DE FF Pain EM
152553
253552
355342
453434
532553
653552
755454
811312
934353
10 5 3 3 3 5
11 3 3 4 4 5
12 5 4 2 5 4
13 3 3 5 4 2
14 5 5 5 5 1
15 3 1 1 2 3
16 1 1 1 1 1
17 4 4 5 5 3
18 5 3 5 5 3
0, no change; 1, mild improvement; 2, mild improvement to moderate improvement; 3,
moderate improvement; 4, significant improvement; 5, great improvement.
DE, dryness; EM, eye movement; FBS, foreign body sensation; FF, photophobia.
Table 3 Corneal transparency
Transparency, % (n/n)
Preoperative Postoperative
Grade 3 11.11 (2/18) 72.2 (13/18)
Grade 4 88.9 (16/18) 27.78 (5/18)
McNemar test (paired proportions); p¼0.001.
238 Br J Ophthalmol 2012;96:234e239. doi:10.1136/bjo.2010.199901
Clinical science
As the severity of dry eye is a major prognostic factor for
limbal and corneal graft in patients with SJS,
17
it is reasonable to
believe that improving lubrication may lead to an improvement
in the outcome of ocular surface reconstruction using mucous
and salivary gland transplantation. Since experience with this
technique is still very limited, prospective controlled studies will
have to be performed to establish the long-term survival of the
transplanted glands and to classify the salivary tear film and
evaluate its impact on the ocular surface.
In conclusion, salivary gland and oral mucosa transplantation
appears to constitute an effective method of treating severe dry
eye secondary to SJS and should be considered as a step prior to
limbal and corneal graft in these patients.
Further studies involving larger numbers of patients need to
be performed to investigate this subject further; however, this
may represent the first step in successfully treating this disease.
Competing interests None to declare.
Patient consent Obtained.
Ethics approval This study was conducted with the approval of the Research Ethics
Committee of the Paulista School of Medicine (CEP0427/08).
Provenance and peer review Not commissioned; externally peer reviewed.
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