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Amniotic membrane grafting, inlay (A) and overlay (B) techniques. Note that the running suture in the overlay technique is optional, at the surgeon's discretion.

Amniotic membrane grafting, inlay (A) and overlay (B) techniques. Note that the running suture in the overlay technique is optional, at the surgeon's discretion.

Table 1. 
Data on the 2 Patient Groups*
Data on the 2 Patient Groups*
Table 2. 
Results in Groups A and B and the 2 Groups Combined*
Results in Groups A and B and the 2 Groups Combined*
1.
Tsai  RJFTseng  SCG Effect of stromal inflammation on the outcome of limbal transplantation for corneal surface reconstruction. Cornea. 1995;14439- 449Article
2.
Foster  CSZelt  RPMai-Phan  TKenyon  KR Immunosuppression and selective inflammatory cell depletion. Arch Ophthalmol. 1982;1001820- 1824Article
3.
Thoft  RAFriend  JMurphy  HS  et al.  Ocular surface epithelium and corneal vascularization in rabbits, I. Invest Ophthalmol Vis Sci. 1979;1885- 92
4.
Brown  SIHook  CW Isolation of stromal collagenase in corneal inflammation. Am J Ophthalmol. 1971;721139- 1142
5.
Kenyon  KRBerman  MRose  JGage  J Prevention of stromal ulceration in the alkali-burned rabbit cornea by glued-on contact lens. Invest Ophthalmol Vis Sci. 1979;18570- 587
6.
Terranova  VPLyall  RM Chemotaxis of human gingival epithelial cells to laminin: a mechanism for epithelial cell apical migration. J Periodontol. 1986;57311- 317Article
7.
Khodadoust  AASilverstein  AMKenyon  KRDowling  JE Adhesion of regenerating corneal epithelium. Am J Ophthalmol. 1968;65339- 348
8.
Sonnenberg  ACalafat  JJanssen  H  et al.  Integrin α6/β4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell–basement membrane adhesion. J Cell Biol. 1991;113907- 917Article
9.
Barcellos-Hoff  MHAggeler  JRam  TGBissell  MJ Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development. 1989;105223- 235
10.
Guo  MGrinnel  F Basement membrane and human epidermal differentiation in vitro. J Invest Dermatol. 1989;93372- 378Article
11.
Streuli  CHBailey  NBissell  MJ Control of mammary epithelial differentiation. J Cell Biol. 1991;1151383- 1395Article
12.
Tseng  SCGPrabhasawat  PLee  SH Amniotic membrane transplantation for conjunctival surface reconstruction. Am J Ophthalmol. 1997;124765- 774
13.
Boudreau  NSympson  CJWerb  ZBissell  MJ Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science. 1995;267891- 893Article
14.
Boudreau  NWerb  ZBissell  MJ Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci U S A. 1996;933509- 3513Article
15.
Kurpakus  MAStock  ElJones  JCR The role of the basement membrane in differential expression of keratin proteins in epithelial cells. Dev Biol. 1992;150243- 255Article
16.
van Herendael  BJOberti  CBrosens  I Microanatomy of the human amniotic membranes. Am J Obstet Gynecol. 1978;131872- 880
17.
Fukuda  KChikama  TNakamura  MNishida  T Differential distribution of subchains of the basement membrane components type IV collagen and laminin among the amniotic membrane, cornea, and conjunctiva. Cornea. 1999;1873- 79Article
18.
Polzin  WJLockrow  EGMorishige  WK A pilot study identifying type V collagenolytic activity in human amniotic fluid. Am J Perinatol. 1997;14103- 106Article
19.
Shimazaki  JShinozaki  NTsubota  K Transplantation of amniotic membrane and limbal autograft for patients with recurrent pterygium associated with symblepharon. Br J Ophthalmol. 1998;82235- 240Article
20.
Choi  YSKim  JYWee  WRLee  JH Effect of the application of human amniotic membrane on rabbit corneal wound healing after excimer laser photorefractive keratectomy. Cornea. 1998;17389- 395Article
21.
Wang  MGray  TPrabhasawat  P  et al.  Corneal haze is reduced by amniotic membrane matrix in excimer laser photoablation in rabbits [abstract]. Invest Ophthalmol Vis Sci. 1997;38suppl405
22.
Athayde  NEdwin  SSRomero  R A role for matrix metalloproteinase-9 in spontaneous rupture of the fetal membranes. Am J Obstet Gynecol. 1998;1791248- 1253Article
23.
Davis  JW Skin transplantation with a review of 550 cases at The Johns Hopkins Hospital. Johns Hopkins Med J. 1910;15307- 396
24.
Trelford  JDTrelford-Sauder  M The amnion in surgery, past and present. Am J Obstet Gynecol. 1979;134833- 845
25.
De Roth  A Plastic repair of conjunctival defects with fetal membrane. Arch Ophthalmol. 1940;23522- 525Article
26.
Batlle  JFPerdomo  FJ Placental membranes as a conjunctival substitute [abstract]. Ophthalmology. 1993;100107Abstract 9A.
27.
Kim  JCTseng  SCG Transplantation of preserved human amniotic membrane for surface reconstruction in severely damaged rabbit corneas. Cornea. 1995;14473- 484Article
28.
Shimazaki  JYang  HYTsubota  K Amniotic membrane transplantation for ocular surface reconstruction in patients with chemical and thermal burn. Ophthalmology. 1997;1042068- 2076Article
29.
Tsubota  KSatake  YOhyama  M  et al.  Surgical reconstruction of the ocular surface in advanced ocular cicatricial pemphigoid and Stevens-Johnson syndrome. Am J Ophthalmol. 1996;12238- 52
30.
Prabhasawat  PBarton  KBurkett  GTseng  SCG Comparison of conjunctival autografts, amniotic membrane grafts, and primary closure for pterygium excision. Ophthalmology. 1997;104974- 985Article
31.
Lee  SHTseng  SCG Amniotic membrane transplantation for persistent epithelial defects with ulceration. Am J Ophthalmol. 1997;123303- 312
32.
Pires  RTTseng  SCPrabhasawat  P  et al.  Amniotic membrane transplantation for symptomatic bullous keratopathy. Arch Ophthalmol. 1999;1171291- 1297Article
33.
Tseng  SCGPrabhasawat  PBarton  KGray  TMeller  D Amniotic membrane transplantation with or without limbal allografts for corneal surface reconstruction in patients with limbal stem cell deficiency. Arch Ophthalmol. 1998;116431- 441Article
34.
Shore  JWFoster  CSWestfall  CTRubin  PAD Results of buccal mucosa grafting for patients with medically controlled ocular cicatricial pemphigoid. Ophthalmology. 1992;99383- 395Article
35.
Dohlman  CHDoane  MG Some factors influencing outcome after keratoprosthesis surgery. Cornea. 1994;13214- 218Article
36.
Adinolfi  MAkle  CAMcColl  I  et al.  Expression of HLA antigens, β2-microglobulin and enzymes by human amniotic membrane. Nature. 1982;295325- 327Article
37.
Akle  CAAdinolfi  MWelsh  KILeibowitz  SMcColl  I Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet. 1981;21003- 1005Article
38.
Houlihan  JMBiro  PAHarper  HMJenkinson  HJHolmes  CH The human amniotic membrane is a site of MHC class 1b expression: evidence for the expression of HLA-E and HLA-G. J Immunol. 1995;1545665- 5674
Clinical Sciences
May 2001

Amniotic Membrane Inlay and Overlay Grafting for Corneal Epithelial Defects and Stromal Ulcers

Author Affiliations

From the Immunology and Uveitis Service (Drs Letko, Romero, Samson, Nguyen, Harper, and Foster) and Cornea Service (Drs Stechschulte, Primack, Azar, and Dohlman), Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston; Cornea Consultants, Boston (Drs Stechschulte and Kenyon); Ludwigs Maximilian Universitat Augenklinik, München, Germany (Drs Kenyon and Gruterich); Al-Bahar Ophthalmology Center, IBN Sina Hospital, Safat, Kuwait(Dr Sadeq); and General Hospital of Athens, University Eye Clinic, Athens Medical School, Athens, Greece (Dr Baltatzis).

Arch Ophthalmol. 2001;119(5):659-663. doi:10.1001/archopht.119.5.659
Abstract

Objectives  To determine the effect of amniotic membrane transplantation (AMT) on persistent corneal epithelial defects (PEDs) and to compare the efficacy between inlay and overlay techniques.

Methods  Thirty patients (30 eyes) underwent AMT for PED. The use of AMT was restricted to patients in whom all previous measures, including bandage contact lens and tarsorrhaphy, had failed. The amniotic membrane was placed on the surface of the cornea in overlay (group A) or inlay (group B) fashion.

Results  The PED healed after the first AMT in 21 eyes (70%) within an average of 25.5 days after surgery and recurred in 6 eyes (29%). Among the 22 eyes treated with an overlay AMT (group A), the PED healed after the first AMT in 14 eyes (64%) within an average of 24.5 days and recurred in 4 eyes (29%). Among the 8 eyes treated with an inlay AMT (group B), the PED healed within an average of 27.4 days after AMT, which did not statistically significantly differ from group A (P = .72). The PED healed after the first AMT in 7 eyes (88%) and recurred in 2 (29%) of 7 eyes.

Conclusions  The AMT can be helpful in the treatment of PED in which all other conventional management has failed. However, the success rate in our study was not as high as that previously reported, and our results showed a high incidence of recurrences of epithelial defects. We did not find any difference between overlay and inlay techniques in terms of healing time and recurrence rate.

PERSISTENT CORNEAL epithelial defects (PEDs) induced by primary ocular surface disorders, such as chemical injury, neurotrophic keratitis, and keratoconjunctivitis sicca, or associated with systemic diseases, such as ocular cicatricial pemphigoid, Stevens-Johnson syndrome, or toxic epidermal necrolysis, are extremely difficult to treat. Such disorders cause prolonged inflammation of the ocular surface, damaging corneal stem cells and epithelial basement membrane (BM)1 and resulting in corneal scarring,2 neovascularization,3 and decreased vision. In addition, matrix metalloproteinases produced by keratocytes,4 epithelial cells, and neutrophils5 can cause progressive stromal ulceration with risk of corneal perforation.

Previous studies have shown that the epithelial BM facilitates migration of epithelial cells,6 reinforces adhesion of basal epithelial cells,7,8 promotes epithelial differentiation,912 and militates against epithelial apoptosis.13,14 Even when an extensive PED develops, in the presence of an intact BM, the corneal surface can be replaced by conjunctivally derived epithelium that can acquire a corneal-type phenotype, ie, express 55-kd keratin.15

Human placental amnion is composed of a single epithelial cell layer, a BM, and an avascular stroma.16 Both collagens IV and VII, components of corneal epithelial BM, are present in the BM of amniotic membrane.17 In addition, collagens I through III and V are also present in human placental amnion.18 Amniotic epithelium produces basic fibroblast growth factor, hepatocyte growth factor, and transforming growth factor β.19 Amnion prevents inflammatory cell infiltration20 and reduces apoptosis in keratocytes after transplantation onto the corneal surface.21 It is noteworthy that matrix metalloproteinases have also been identified in human amniotic membrane.22

Davis23 first reported on the use of amniotic membrane for skin transplantation in 1910. Since then, living rather than preserved amniotic membrane has been used for various purposes,24 and in 1940, De Roth25 first reported its use in the eye, using fresh amnion for the reconstruction of conjunctival defects. In the early 1990s, Batlle and Perdomo26 reintroduced the use of amniotic membrane transplantation (AMT) for ocular disorders in North America. Kim and Tseng27 then showed in 1995 that preserved amniotic membrane facilitated corneal surface reconstruction in rabbits after epithelial removal and limbal lamellar keratectomy. Amniotic membrane transplantation has recently been used for ocular surface reconstruction in patients after chemical burn,28 in patients with advanced ocular cicatricial pemphigoid and Stevens-Johnson syndrome,29 and for pterygium excision,30 conjunctival surface reconstruction,12 sterile corneal ulceration,31 and symptomatic bullous keratopathy.32

The purpose of this study was to determine the effect of human amniotic membrane grafts on PEDs of the cornea with or without stromal ulcers and to compare the efficacy between inlay and overlay techniques.

PATIENTS AND METHODS

Thirty patients (30 eyes) who underwent AMT for PED with or without stromal ulceration between 1997 and 1999 were studied (Table 1). The duration of corneal epithelial defects varied from 1 to 6 weeks. We used a progressively staged approach in the management of PED. Thus, all patients were initially treated with removal of toxic topical antibiotics, lubrication, punctum occlusion if appropriate, and then with a bandage contact lens. If these techniques were unsuccessful, tarsorrhaphy was performed. Amniotic membrane transplantation was reserved for patients in whom all other measures were unsuccessful. In patients who refused to have tarsorrhaphy, mostly for cosmetic reasons, AMT was performed after treatment with bandage contact lenses failed.

Human amniotic membrane grafts were prepared and preserved as previously described.31 An informed consent was obtained from each patient before the surgery. After peribulbar or topical anesthesia, the base of the epithelial defect or stromal ulcer was debrided with a microsponge, and the poorly adherent epithelium surrounding the defect or ulcer was removed. The amniotic membrane was placed on the surface of the cornea in overlay (group A) or inlay (group B) fashion (Figure 1). After each AMT, a bandage contact lens was applied and 0.35% ciprofloxacin hydrochloride eyedrops 4 times a day and 1% rimexolone eyedrops 4 times a day were administered in the postoperative period. The amniotic membrane dissolved under the bandage contact lens during a period of 4 weeks after surgery. The bandage contact lens was removed when the epithelial defect had healed.

GROUP A: OVERLAY AMT

Patients with large epithelial defects with or without stromal ulcer with clinically deficient limbal stem cell function were treated with overlay AMT. Overlay grafts approximately 12 to 14 mm in diameter covered the entire corneal, limbal, and perilimbal surfaces. The overlay AMT was placed with the epithelial BM side up and secured by interrupted 10-0 polyglactin sutures to the surrounding conjunctiva. In some cases, a running 10-0 polyglactin suture was placed in the midperipheral cornea.

GROUP B: INLAY AMT

Patients with localized PED (<20% of corneal surface) with or without stromal ulceration received inlay AMT. Inlay grafts were cut to fit the size of the epithelial defect or stromal ulceration as described by Lee and Tseng.31 These grafts were placed with the epithelial BM side up and secured to the edge of the defect by interrupted 10-0 polyglactin sutures.

After each AMT, a bandage contact lens was applied and 0.35% ciprofloxacin hydrochloride eyedrops 4 times a day and 1% rimexolone eyedrops 4 times a day were administered in the postoperative period. The amniotic membrane dissolved under the bandage contact lens during a period of 4 weeks after surgery. The bandage contact lens was removed when the epithelial defect had healed.

RESULTS
OVERALL OUTCOMES

The overall results for all 30 cases are summarized in Table 2. The mean age of patients was 55.3 years (range, 9-78 years). The male-female ratio was 2:1. The mean follow-up time after AMT was 8.2 months(range, 1-32 months). The mean visual acuity before and after the surgery was 0.04 (range, 0.01-0.13) and 0.05 (range, 0.01-0.20), respectively (P = .45). The PEDs healed within an average of 25.5 days(range, 5-68 days) after surgery. The epithelial defect healed after the first AMT in 21 eyes (70%). In 9 eyes (30%), the defect persisted after the first AMT. The epithelial defect recurred after the first AMT in 6 (29%) of 21 eyes. The average time to recurrence of the defect was 5.2 weeks (range, 2-9 weeks). Thus, the PED did not heal or recurred after the first AMT in 15 (50%) of 30 eyes.

During follow-up, AMT was repeated in 5 patients, and in 1 case the recurrence was successfully treated with a bandage contact lens. The first AMT was accompanied by additional surgical procedures in 18 eyes. These included tarsorrhaphy (16 eyes), superficial keratectomy (2 eyes), and lamellar keratoplasty(1 eye). Among the 16 patients in whom AMT was performed along with tarsorrhaphy, 12 defects (75%) healed; of these, 4 (33%) recurred after the first AMT. Interestingly, we observed similar results in patients who were treated with AMT alone. In 9 (64%) of 14 patients the defect healed, and in 2 (22%) of the 9 it recurred.

GROUP A

Among the 22 eyes treated with an overlay AMT, the mean age of patients was 53.1 years (range, 27-75 years). The male-female ratio was 7:4. The mean follow-up time was 6.8 months (range, 1-22 months) after AMT. The mean visual acuity before and after the surgery was 0.05 (range, 0.01-0.33) and 0.06 (range, 0.01-0.33), respectively (P = .54). The corneal epithelial defect healed within an average of 24.5 days (range, 5-68 days) after surgery. The epithelial defect healed after the first AMT in 14 eyes (64%). The epithelial defect recurred after the first AMT in 4 (29%) of 14 eyes. The average time to the recurrence of the defect was 4.5 weeks (range, 2-9 weeks). The PED did not heal or recurred after the first AMT in 4 patients (45%).

GROUP B

Among the 8 eyes treated with an inlay AMT, the mean age of patients was 61.1 years (range, 9-78 years). The male-female ratio was 3:1. The mean follow-up time was 12.2 months (range, 2-32 months) after AMT. The mean visual acuity before and after the surgery was 0.02 (range, 0.01-0.05) and 0.03 (range, 0.01-0.1), respectively (P = .35). The corneal epithelial defect healed within an average of 27.4 days (range, 7-41 days) after AMT, which did not statistically significantly differ from group A (P = .72). The epithelial defect healed after the first AMT in 7 eyes(88%). The epithelial defect persisted after the first AMT in 1 eye (12%). The epithelial defect recurred after the first AMT in 2 (29%) of 7 eyes. The PED did not heal or recurred after the first AMT in 3 (38%) of 8 eyes. There was not a statistically significant difference (P= .53) in the average time to the recurrence of epithelial defect between group B (6.5 weeks) and group A.

COMMENT

The epithelial defects healed after the first AMT in 70% (21/30) of all eyes in our study. By comparison, Lee and Tseng31 reported an initial success rate of 90% (10/11). In addition, we found a higher recurrence rate (29%) after the first AMT than that previously reported.31 Given the intrinsic diversity among PED cases, it might be hypothesized that differences in surgical techniques and/or causes of the epithelial defects might explain these outcome differences. Lee and Tseng31 did not observe any recurrence of epithelial defect when the amniotic membrane graft was placed into the stromal ulcer and secured by interrupted sutures to the edge of the defect. The corneal epithelium grew over the amniotic membrane graft. We used an identical technique in group B, yet the incidence of recurrences was 29%. Again, the difference in cause of the epithelial defects and extent of damage to the ocular surface might explain this higher rate of recurrences. Interestingly, our results show that there was no difference in recurrence rate between overlay and inlay techniques, although there was a slight difference in success rate after the first AMT when the inlay technique was used. In addition to using amnion in the inlay fashion, we used the amniotic membrane graft to cover the entire corneal surface and perilimbal conjunctiva in some cases, similar to a bandage contact lens. This technique has been used successfully by others in the treatment of patients with symptomatic bullous keratopathy,32 limbal stem cell deficiency of various causes,33 and stromal defects after photorefractive keratectomy.20

Among our patients, autoimmune diseases affecting the ocular surface were involved in the pathogenesis of epithelial defects and stromal ulcers in 3 of 6 patients with recurrence of epithelial defect. One patient had ocular cicatricial pemphigoid, 1 had toxic epidermal necrolysis, and the other had Sjögren syndrome. Tsubota et al29 treated a group of patients with ocular cicatricial pemphigoid or Stevens-Johnson syndrome with AMT and limbal stem cell transplantation. They demonstrated that the entire ocular surface with or without PED in this group of patients can be restored by AMT along with limbal allograft and tarsorrhaphy, followed by systemic immunosuppression and topical administration of artificial tears derived from autologous serum. The authors reported a stable ocular surface during the follow-up in 9 of 11 patients. However, final visual acuity remained less than 0.1 in all but 3 patients.

The growth of new epithelium, particularly in patients with multiple causative factors involved in the pathogenesis of epithelial or stromal defects, may be altered by the absence of direct contact with BM. Tseng et al33 recently showed that AMT alone is superior to AMT with limbal allotransplantation in patients with partial limbal stem cell deficiency, whereas limbal allotransplantation with AMT is needed for patients with total limbal stem cell deficiency.

Active conjunctival inflammation can complicate the postoperative period after ocular surface reconstruction,34 with resultant failure of the ocular surface. Keratoprosthesis may then be the procedure of last resort in such cases.35

Shimazaki et al19 claimed that the epithelium of the amniotic membrane may survive up to 70 days after cryopreservation. Their study showed that living epithelium of amnion produces basic fibroblast growth factor, hepatocyte growth factor, and transforming growth factor β.19 Whether cryopreserved transplanted amniotic membrane confers such benefit is uncertain. Because the epithelium of amnion expresses neither HLA class I nor II antigens,3638 the use of systemic immunosuppressive therapy in AMT is not required.

Amniotic membrane transplantation can improve visual acuity by both corneal surface restoration and improvement of corneal transparency.31 In our study, the average visual acuity improved after AMT, but the difference between the preoperative and final visual acuities was not statistically significant (P = .45). A statistically significant difference between visual acuity before AMT and final visual acuity was not observed in either group A (P = .54) or group B (P = .35). These results suggest that the effect of AMT on vision rehabilitation is very limited and is unrelated to the technique used.

In summary, our study confirms the results of previous reports that AMT can be helpful in the treatment of epithelial defects and stromal ulcers in which all other conventional management has failed. However, the success rate in our study was not as high as that previously reported, and our results showed a high incidence of recurrences of epithelial defects.

We therefore believe that AMT for PED, with or without stromal ulceration, should not be used as first- or even second-line therapy. The use of AMT for PED should be reserved for cases in which removal of medications toxic to the epithelium, aggressive lubrication and ocular surface protection (eg, bandage contact lens and tarsorrhaphy), and control of inflammation have failed to promote closure of the defect. We did not find any difference between overlay and inlay techniques in terms of healing time, recurrence rate, and effect on vision rehabilitation. Further studies are required to confirm our results, to compare AMT with other strategies in treatment of PEDs and stromal ulcers, to compare the results after different techniques of transplantation, and to estimate the outcomes in various groups of patients.

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Article Information

Accepted for publication December 15, 2000.

Corresponding author and reprints: C. Stephen Foster, MD, Immunology Service, Massachusetts Eye and Ear Infirmary, 243 Charles St, Boston, MA 02114(e-mail: fosters@uveitis.org).

References
1.
Tsai  RJFTseng  SCG Effect of stromal inflammation on the outcome of limbal transplantation for corneal surface reconstruction. Cornea. 1995;14439- 449Article
2.
Foster  CSZelt  RPMai-Phan  TKenyon  KR Immunosuppression and selective inflammatory cell depletion. Arch Ophthalmol. 1982;1001820- 1824Article
3.
Thoft  RAFriend  JMurphy  HS  et al.  Ocular surface epithelium and corneal vascularization in rabbits, I. Invest Ophthalmol Vis Sci. 1979;1885- 92
4.
Brown  SIHook  CW Isolation of stromal collagenase in corneal inflammation. Am J Ophthalmol. 1971;721139- 1142
5.
Kenyon  KRBerman  MRose  JGage  J Prevention of stromal ulceration in the alkali-burned rabbit cornea by glued-on contact lens. Invest Ophthalmol Vis Sci. 1979;18570- 587
6.
Terranova  VPLyall  RM Chemotaxis of human gingival epithelial cells to laminin: a mechanism for epithelial cell apical migration. J Periodontol. 1986;57311- 317Article
7.
Khodadoust  AASilverstein  AMKenyon  KRDowling  JE Adhesion of regenerating corneal epithelium. Am J Ophthalmol. 1968;65339- 348
8.
Sonnenberg  ACalafat  JJanssen  H  et al.  Integrin α6/β4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell–basement membrane adhesion. J Cell Biol. 1991;113907- 917Article
9.
Barcellos-Hoff  MHAggeler  JRam  TGBissell  MJ Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development. 1989;105223- 235
10.
Guo  MGrinnel  F Basement membrane and human epidermal differentiation in vitro. J Invest Dermatol. 1989;93372- 378Article
11.
Streuli  CHBailey  NBissell  MJ Control of mammary epithelial differentiation. J Cell Biol. 1991;1151383- 1395Article
12.
Tseng  SCGPrabhasawat  PLee  SH Amniotic membrane transplantation for conjunctival surface reconstruction. Am J Ophthalmol. 1997;124765- 774
13.
Boudreau  NSympson  CJWerb  ZBissell  MJ Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science. 1995;267891- 893Article
14.
Boudreau  NWerb  ZBissell  MJ Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci U S A. 1996;933509- 3513Article
15.
Kurpakus  MAStock  ElJones  JCR The role of the basement membrane in differential expression of keratin proteins in epithelial cells. Dev Biol. 1992;150243- 255Article
16.
van Herendael  BJOberti  CBrosens  I Microanatomy of the human amniotic membranes. Am J Obstet Gynecol. 1978;131872- 880
17.
Fukuda  KChikama  TNakamura  MNishida  T Differential distribution of subchains of the basement membrane components type IV collagen and laminin among the amniotic membrane, cornea, and conjunctiva. Cornea. 1999;1873- 79Article
18.
Polzin  WJLockrow  EGMorishige  WK A pilot study identifying type V collagenolytic activity in human amniotic fluid. Am J Perinatol. 1997;14103- 106Article
19.
Shimazaki  JShinozaki  NTsubota  K Transplantation of amniotic membrane and limbal autograft for patients with recurrent pterygium associated with symblepharon. Br J Ophthalmol. 1998;82235- 240Article
20.
Choi  YSKim  JYWee  WRLee  JH Effect of the application of human amniotic membrane on rabbit corneal wound healing after excimer laser photorefractive keratectomy. Cornea. 1998;17389- 395Article
21.
Wang  MGray  TPrabhasawat  P  et al.  Corneal haze is reduced by amniotic membrane matrix in excimer laser photoablation in rabbits [abstract]. Invest Ophthalmol Vis Sci. 1997;38suppl405
22.
Athayde  NEdwin  SSRomero  R A role for matrix metalloproteinase-9 in spontaneous rupture of the fetal membranes. Am J Obstet Gynecol. 1998;1791248- 1253Article
23.
Davis  JW Skin transplantation with a review of 550 cases at The Johns Hopkins Hospital. Johns Hopkins Med J. 1910;15307- 396
24.
Trelford  JDTrelford-Sauder  M The amnion in surgery, past and present. Am J Obstet Gynecol. 1979;134833- 845
25.
De Roth  A Plastic repair of conjunctival defects with fetal membrane. Arch Ophthalmol. 1940;23522- 525Article
26.
Batlle  JFPerdomo  FJ Placental membranes as a conjunctival substitute [abstract]. Ophthalmology. 1993;100107Abstract 9A.
27.
Kim  JCTseng  SCG Transplantation of preserved human amniotic membrane for surface reconstruction in severely damaged rabbit corneas. Cornea. 1995;14473- 484Article
28.
Shimazaki  JYang  HYTsubota  K Amniotic membrane transplantation for ocular surface reconstruction in patients with chemical and thermal burn. Ophthalmology. 1997;1042068- 2076Article
29.
Tsubota  KSatake  YOhyama  M  et al.  Surgical reconstruction of the ocular surface in advanced ocular cicatricial pemphigoid and Stevens-Johnson syndrome. Am J Ophthalmol. 1996;12238- 52
30.
Prabhasawat  PBarton  KBurkett  GTseng  SCG Comparison of conjunctival autografts, amniotic membrane grafts, and primary closure for pterygium excision. Ophthalmology. 1997;104974- 985Article
31.
Lee  SHTseng  SCG Amniotic membrane transplantation for persistent epithelial defects with ulceration. Am J Ophthalmol. 1997;123303- 312
32.
Pires  RTTseng  SCPrabhasawat  P  et al.  Amniotic membrane transplantation for symptomatic bullous keratopathy. Arch Ophthalmol. 1999;1171291- 1297Article
33.
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