Keywords microvascular submandibular gland transfer - salivary gland - dry eyes - keratoconjunctivitis
sicca
Introduction
Dry eye disease is a chronic debilitating problem of multifactorial origin which if
left untreated can lead to corneal ulceration and blindness. It affects 7.4 to 33.7%
of people depending on various studies and populations being surveyed. Initial phases
can be managed well with conservative measures.[1 ] In advanced cases, surgical options play a more vital role.[2 ] Submandibular gland secretion is mucino-serous and provides an ideal replacement
of the original tear film. But transferring the submandibular glands needs good microvascular
skills; therefore, it should be used as a last resort in severe keratoconjunctivitis
sicca cases only,[3 ] with possible indications such as:
Case Report
A 5-year-old boy was referred to the ophthalmology department with a diagnosis of
bilateral membranous conjunctivitis and dry eyes. Ocular examination revealed a visual
acuity of 1/60 in both the eyes, not improving with spectacles or pinhole. He was
orthotropic with full range of ocular movements and no nystagmus. Ocular examination
revealed normal lids with conjunctival xerosis involving bulbar, palpebral, and forniceal
conjunctiva in both eyes. Although the fornices were deep with no keratinization,
there was evidence of subconjunctival fibrosis in the superior forniceal conjunctiva.
Tear meniscus was not visible in either eye. Cornea was lusterless with hypertrophic
epithelium and 360 degrees superficial vascularization extending to the central cornea.
The other anterior segment details and retina evaluation were grossly within normal
limits.
Dry eye work-up showed spontaneous T-BUT of <1 second[4 ] and confluent punctate corneal erosions, though there was no obvious keratinization.
Schirmer's test values under anesthesia were <1 mm in both the eyes after 5 minutes.[5 ] The National Eye Institute (NEI) score was 12.5/15 for conjunctiva and 15/15 for
cornea in both the eyes.[6 ] A clinical diagnosis of severe ocular surface disease, because of congenital alacrima,
was made by the ophthalmologist.
Conjunctival biopsy with direct immunofluorescence was done to rule out early-onset
childhood cicatricial pemphigoid, which was unremarkable. As there were limited treatment
options and rapid deterioration of the ocular surface, he was advised microvascular
autologous transplantation of the submandibular gland in both the eyes. A possibility
of autoimmune degeneration of salivary glands was to be ruled out, hence a 99 m Tc-pertechnetate
scintigraphy was performed, which revealed good dye uptake in submandibular, sublingual,
and parotid glands, but no uptake was seen in the lacrimal glands.
Due to the complex nature of the surgery, and to avoid the problems associated with
prolonged anesthesia, it was decided that we would perform the surgery for each eye
separately. The right side was operated upon first, followed by the left eye. Initially
a decision of operating at an interval of 1 month was taken, but the left eye surgery
was delayed by 1 year and 5 months because the parents wanted to be sure about the
improvement in the right eye before going for the left-eye surgery.
Surgical Technique
Recipient Vessel and Bed Preparation
Superficial temporal vessels were located preoperatively using a Doppler and marked.
Flap marked and raised superficial to the deep temporal fascia. Superficial temporal
vessels were dissected and mobilized. A 3 × 3 cm trough created by excising the central
portion of temporalis muscle to accommodate the salivary gland. A subcutaneous tunnel
was made up to the upper lateral fornix to create an opening for the duct ([Figs. 1 ] and [2 ]).
Fig. 1 Preoperative marking.
Fig. 2 Space created in the temporalis muscle for the submandibular gland.
Submandibular Gland Harvest
Intraorally the Wharton's duct opening was cannulated, to prevent damage during the
dissection. Cervical neck incision was given, and the submandibular gland was identified
and dissected. Facial artery and vein were isolated and dissected both proximally
and distally. The Wharton's duct was traced up to the floor of the mouth, carefully
preserving the lingual nerve. Intraorally the incision was given around the cannulated
duct, preserving a cuff of oral mucosa around it. A suction drain was placed and wounds
were closed ([Fig. 3 ]).
Fig. 3 Harvested submandibular gland.
Gland Transfer
Gland was placed and fixed in the trough created by excising a part of the temporalis
muscle, this was done to avoid the postoperative bulging. The superficial temporal
artery and vein were anastomosed to the facial artery and vein, end to end using 10/0
Nylon sutures. A silk suture was used to engage the Wharton's duct and it was tunneled
to the lateral fornix by gently pulling on the suture. Care was taken to avoid twisting
of the duct. Duct opening was sutured to the palpebral conjunctiva using 8–0 nylon
interrupted sutures. The duct was cannulated using a silicone tube, to act as a stent
for 2 weeks, which was fixed just outside the lateral canthus. The temporal wound
was closed in two layers ([Figs. 4 ] and [5 ]).
Fig. 4 Gland after microvascular anastomosis.
Fig. 5 Salivary duct fixation in superior fornix of right eye.
Postoperative Care
The patient was kept in the intensive care unit for 5 days to allow for close monitoring
of the circulation using a Doppler.
Evaluation under anesthesia was done within 2 weeks with the following objectives:
Remove the silicon tube placed in Wharton's duct.
Ensure patency of the duct in conjunctival cul de sac.
Irrigate Wharton's duct and remove any thick mucus plugs.
Tc-Pertechnetate scintigraphy was done to document the gland viability at 3 months.
The same surgical technique was applied for the surgery of the left eye ([Figs. 6 ]
[7 ]
[8 ]
[9 ]).
Fig. 6 Preoperative and 2 weeks postoperative right eye.
Fig. 7 Preoperative and 1 year postoperative right eye.
Fig. 8 Preoperative and 3 months postoperative left eye.
Fig. 9 Pre- and postoperative Tc-pertechnetate scintigraphy.
Results
The immediate postoperative period for both the surgeries was uneventful with no microvascular
complications. The stent on each side was retained for a period of 2 weeks. The patient
has been followed up for a period of 2 years for the right eye and 7 months for the
left eye.
The patient has been objectively assessed as follows.
Right Eye
Visual acuity: Improved from counting fingers close to face (6/120) to counting fingers
at 3 m (3/60). A definite improvement in functional vision was also noted by the parents.
Gland secretion: Initial epiphora was present for a few days which subsided, as the
gland secretion entered the latent phase. He was prescribed systemic pilocarpine (5 mg
thrice daily) to stimulate salivary secretion for the first 3 months. After 2 months
the secretion started improving and stabilized, with epiphora occurring only during
increased activity.
Ocular examination findings: Slit lamp examination showed hypertrophic corneal epithelium
with clear stroma and endothelium. Other anterior segment findings and retinal examination
were within normal limits. There was a notable difference in ocular surface. The dry
lusterless conjunctiva and cornea was replaced by a moist shiny surface. The tear
meniscus height improved from 0 to 1 mm.
Dry eye work-up: T-BUT increased to 4 seconds. Schirmer's values also dramatically
improved to >10 mm at 5 minutes. Ocular surface staining also showed remarkable improvement.
NEI score was 0/15 for conjunctiva (preoperative 12.5/15) and 7.5/15 for cornea (15/15
preoperatively).
Left Eye
There was marked difference between the two eyes. While the right eye showed dramatic
improvement, as detailed earlier, in the left eye, conjunctiva revealed xerosis all
around with keratinization. There was partial obliteration of fornices with subconjunctival
fibrosis. Tear meniscus was not visible. Cornea showed keratinization of the surface
with 360 degrees superficial vascularization. The other anterior segment details and
retinal examination were very hazy but grossly within normal limits.
In the postoperative period, the eye became moist with a Schirmer's value of >10 mm.
Ocular surface improved with some reversal of surface keratinization and reduction
in corneal fluorescein staining ([Table 1 ]).
Table 1
Objective analysis
Test
Normal
Preoperative
Right eye postoperative 2 years
Left eye postoperative 7 months
Visual acuity
6/6
Counting fingers at 0.5 m
Counting fingers at 4 m
Counting fingers at 3 m
Tear meniscus height
0.21–0.46 mm
0 mm
1 mm
1 mm
Schirmer's test
>10 mm at 5 min
0 mm at 5 min
>10 mm at 5 min
>10 mm at 5 min
Tear break-up time
>10 s
0 s
4 s
4 s
Corneal epithelial staining
No visible staining
Marked staining
Reduced staining
Reduced staining
National Eye Institute scoring
0/15
(best)
15/15
(worst)
4/15
6.5/15
Postoperative biochemical analysis of the secretion from the transposed submandibular
glands was done from both the eyes separately and it was compared with the normal
submandibular gland secretion and normal tear secretion based on five parameters,
namely, sodium, potassium, osmolality, amylase, and secretory immunoglobulin. This
suggests that the characteristics of transferred submandibular gland secretions slowly
drift toward that of the normal lacrimal secretion. Geerling et al performed a similar
analysis in their study, but a comparison with normal tear composition was not performed
and the follow-up time was only 1 year ([Table 2 ]).[7 ]
Table 2
Postoperative tear analysis
Test
Normal SMG
Left eye salivary tears at 7 months
Right eye salivary tears at 2 years
Normal lacrimal tears
Sodium, mmol/L
7.26 ± 2.23
18
24
156 ± 20.34
Potassium, mmol/L
12.8 ± 3.63
23
19
18.4 ± 8.93
Osmolality, mOsm/kg
96 ± 24
42
81
303.7 ± 22.9
Amylase, u/L
30,900 ± 20,000
2,289
209
1,854 ± 1,200
S IgA, mg/dL
4.26 ± 3.85
10.7
14.4
26 ± 13
Abbreviation: S IgA, secretory immunoglobulin A.
Discussion
The treatment for advanced cases of dry eye is challenging. Surgical treatment was
initiated with the replacement of tear film secretion with salivary secretion. All
three major salivary glands have been used as alternate sources for tear production.
Parotid duct transposition was originally described by Filatov and Chevaljev[8 ] in 1951. By this method the parotid duct was transposed from its original position
to the lower conjunctival fornix. Pierce et al described a modification by which the
procedure could be performed completely intraorally.[9 ] The problems associated with parotid gland secretion are its excessive in quantity
and being more serous; this does not match natural tear secretion.
Sublingual gland transplantation was first described by Murube et al,[10 ] which involved excision of a block of sublingual gland along with overlying mucosa
which was transplanted to the recipient conjunctival bed. As these transfers were
nonvascularized, suboptimal results were seen.
Murube-Del-Castillo is credited with the first use of microvascular submandibular
gland transfer.[11 ] The use of microvascular submandibular gland transfer for tear replacement is considered
to be ideal due to its reliable blood supply, sero-mucinous nature of saliva, and
denervation of the gland during harvest, which avoids gustatory reflex salivation.[12 ]
Zhang et al conducted a long-term study to evaluate the effect of microvascular autologous
submandibular gland transfer in 185 patients, which proved that it grants long-term
improvement and symptomatic relief in cases of severe dry eye.[13 ]
Our case is of a 5-year-old boy with severe bilateral dry eye. Vascularized submandibular
gland transfers were performed for both eyes. The follow-up period is 2 years for
the right eye and 7 months for the left eye. There is significant improvement in visual
acuity, and improvement in corneal morphology and function. Slit lamp examination
shows improvement and healing of ulcers. Specific tests for dry eye such as T-BUT,
Schirmer's test, and NEI scoring also showed significant improvement following submandibular
gland transfer.
The presence of amylase does not damage the cornea as it does not have any proteolytic
and lipolytic activity against the corneal epithelium. In fact, it has bactericidal
activity[14 ] and secretory immunoglobulin A, which also give immunologic protection against bacteria.
The disadvantages of this procedure are the prolonged operative time and physical
activity–related epiphora, which may be controlled by topical application of atropine
gel, botulinum toxin injections, or by direct reduction in the size of the gland by
partial excision.[15 ]
Conclusion
In severe cases of keratoconjunctivitis sicca, this promising technique could be of
vital importance in salvaging vision. Even if visual acuity of the patient does not
improve further, it gives hope by making the ocular surface moist enough to allow
for corneal transplantation. If adopted by more microvascular surgeons, it could open
a relatively untapped field of reconstructive surgical endeavor, with the potential
to improve the quality of life of a large number of patients.
