Restricted accessResearch articleFirst published online 2017-01
Acceleration of Healing of Traumatic Tympanic Membrane Perforation in Rats by Implanted Collagen Membrane Integrated with Collagen-Binding Basic Fibroblast Growth Factor
Traumatic tympanic membrane (TM) perforation is very common in clinical practice. Several biomaterials have been reported to play a role in TM reparation, whereas their functional recovery is limited when used alone. Meanwhile, the administration of biofactors could promote functional recovery, but rapid distribution and short half-time obstruct their application. To study the effect of traumatic TM regeneration, we prepared collagen membrane (CM) integrated with collagen-binding basic fibroblast growth factor (CBD-bFGF) and implanted into the injury site of perforated TM in Sprague-Dawley rats. The study on CBD-bFGF in vitro showed that CBD-bFGF accelerated the proliferation of human fibroblast cell HS-865 biologically and was released from CM gradually. In vivo study, through the gross anatomy, auditory brainstem responses assay, histological staining, and transmission electron microscopy observation at d7, d14, and d28 after the acute TM perforation, we found that CBD-bFGF-integrated CM promoted the healing rate at an early stage (∼7 days), reduced the healing time of perforated TM, and notably retrieved the structure and hearing of TM. These findings suggest that CM modified with CBD-bFGF could be therapeutically appropriate for the treatment of TM perforation.
Get full access to this article
View all access options for this article.
References
1.
TehB.M., MaranoR.J., ShenY., FriedlandP.L., DilleyR.J., and AtlasM.D.Tissue engineering of the tympanic membrane. Tissue Eng Part B Rev, 19, 116, 2013.
2.
KnutssonJ., Bagger-SjobackD., and von UngeM.Collagen type distribution in the healthy human tympanic membrane. Otol Neurotol, 30, 1225, 2009.
3.
LaidlawD.W., CostantinoP.D., GovindarajS., HiltzikD.H., and CatalanoP.J.Tympanic membrane repair with a dermal allograft. Laryngoscope, 111, 702, 2001.
4.
KimJ.H., ChoiS.J., ParkJ.S., LimK.T., ChoungP.H., KimS.W., et al.Tympanic membrane regeneration using a water-soluble chitosan patch. Tissue Eng Part A, 16, 225, 2010.
5.
MerwinG.E., and BoiesL.R.Jr.Paper patch repair of blast rupture of the tympanic membrane. Laryngoscope, 90, 853, 1980.
6.
CamnitzP.S., and BostW.S.Traumatic perforations of the tympanic membrane: early closure with paper tape patching. Otolaryngol Head Neck Surg, 93, 220, 1985.
7.
KimJ.H., BaeJ.H., LimK.T., ChoungP.H., ParkJ.S., ChoiS.J., et al.Development of water-insoluble chitosan patch scaffold to repair traumatic tympanic membrane perforations. J Biomed Mater Res Part A, 90, 446, 2009.
8.
KimJ., KimS.W., ChoiS.J., LimK.T., LeeJ.B., SeonwooH., et al.A healing method of tympanic membrane perforations using three-dimensional porous chitosan scaffolds. Tissue Eng Part A, 17, 2763, 2011.
9.
HottM.E., MegerianC.A., BeaneR., and BonassarL.J.Fabrication of tissue engineered tympanic membrane patches using computer-aided design and injection molding. Laryngoscope, 114, 1290, 2004.
10.
HakubaN., IwanagaM., TanakaS., HiratsukaY., KumabeY., KonishiM., et al.Basic fibroblast growth factor combined with atelocollagen for closing chronic tympanic membrane perforations in 87 patients. Otol Neurotol, 31, 118, 2010.
11.
JangC.H., ChoY.B., YeoM., LeeH., MinE.J., LeeB.H., et al.Regeneration of chronic tympanic membrane perforation using 3D collagen with topical umbilical cord serum. Int J Biol Macromol, 62, 232, 2013.
12.
SeonwooH., KimS.W., KimJ., ChunjieT., LimK.T., KimY.J., et al.Regeneration of chronic tympanic membrane perforation using an EGF-releasing chitosan patch. Tissue Eng Part A, 19, 2097, 2013.
13.
KimJ., KimC.H., ParkC.H., SeoJ.N., KweonH., KangS.W., et al.Comparison of methods for the repair of acute tympanic membrane perforations: silk patch vs. paper patch. Wound Repair Regen, 18, 132, 2010.
14.
GuneriE.A., TekinS., YilmazO., OzkaraE., ErdagT.K., IkizA.O., et al.The effects of hyaluronic acid, epidermal growth factor, and mitomycin in an experimental model of acute traumatic tympanic membrane perforation. Otol Neurotol, 24, 371, 2003.
15.
OzturkK., YamanH., Cihat AvundukM., ArbagH., KelesB., and UyarY.Effectiveness of MeroGel hyaluronic acid on tympanic membrane perforations. Acta Otolaryngol, 126, 1158, 2006.
16.
RamalhoJ.R., and BentoR.F.Healing of subacute tympanic membrane perforations in chinchillas treated with epidermal growth factor and pentoxifylline. Otol Neurotol, 27, 720, 2006.
17.
KanemaruS., UmedaH., KitaniY., NakamuraT., HiranoS., and ItoJ.Regenerative treatment for tympanic membrane perforation. Otol Neurotol, 32, 1218, 2011.
18.
RoosliC., von BurenT., GassmannN.B., and HuberA.M.The impact of platelet-derived growth factor on closure of chronic tympanic membrane perforations: a randomized, double-blind, placebo-controlled study. Otol Neurotol, 32, 1224, 2011.
19.
AbeM., YokoyamaY., and IshikawaO.A possible mechanism of basic fibroblast growth factor-promoted scarless wound healing: the induction of myofibroblast apoptosis. Eur J Dermatol, 22, 46, 2012.
20.
Skaletz-RorowskiA., EschertH., LengJ., StallmeyerB., SindermannJ.R., PulawskiE., et al.PKC delta-induced activation of MAPK pathway is required for bFGF-stimulated proliferation of coronary smooth muscle cells. Cardiovasc Res, 67, 142, 2005.
21.
ZhangQ., and LouZ.Impact of basic fibroblast growth factor on healing of tympanic membrane perforations due to direct penetrating trauma: a prospective non-blinded/controlled study. Clin Otolaryngol, 37, 446, 2012.
22.
ZhaoW., ChenB., LiX., LinH., SunW., ZhaoY., et al.Vascularization and cellularization of collagen scaffolds incorporated with two different collagen-targeting human basic fibroblast growth factors. J Biomed Mater Res Part A, 82, 630, 2007.
23.
ShiC., ChenW., ZhaoY., ChenB., XiaoZ., WeiZ., et al.Regeneration of full-thickness abdominal wall defects in rats using collagen scaffolds loaded with collagen-binding basic fibroblast growth factor. Biomaterials, 32, 753, 2011.
24.
ShiQ., GaoW., HanX., ZhuX., SunJ., XieF., et al.Collagen scaffolds modified with collagen-binding bFGF promotes the neural regeneration in a rat hemisected spinal cord injury model. Sci China Life Sci, 57, 232, 2014.
25.
ShenY., RedmondS.L., TehB.M., YanS., WangY., ZhouL., BudgeonC.A., et al.Scaffolds for tympanic membrane regeneration in rats. Tissue Eng Part A, 19, 657, 2013.
26.
AbbenhausJ.I.The use of reconstituted bovine collagen for tympanic membrane grafting. Otolaryngology, 86, Orl485, 1978.
27.
MaY., ZhaoH., and ZhouX.Topical treatment with growth factors for tympanic membrane perforations: progress towards clinical application. Acta Otolaryngol, 122, 586, 2002.
28.
LouZ.C., LouZ.H., LiuY.C., and ChangJ.Healing human moderate and large traumatic tympanic membrane perforations using basic fibroblast growth factor, 0.3% ofloxacin eardrops, and gelfoam patching. Otol Neurotol, 37, 735, 2016.
29.
LouZ., HuangP., YangJ., XiaoJ., and ChangJ.Direct application of bFGF without edge trimming on human subacute tympanic membrane perforation. Am J Otolaryngol, 37, 156, 2016.
30.
CuiY., LuC., MengD., XiaoZ., HouX., DingW., et al.Collagen scaffolds modified with CNTF and bFGF promote facial nerve regeneration in minipigs. Biomaterials, 35, 7819, 2014.
31.
LiQ., TaoL., ChenB., RenH., HouX., ZhouS., et al.Extrahepatic bile duct regeneration in pigs using collagen scaffolds loaded with human collagen-binding bFGF. Biomaterials, 33, 4298, 2012.
32.
LiX., SunH., LinN., HouX., WangJ., ZhouB., et al.Regeneration of uterine horns in rats by collagen scaffolds loaded with collagen-binding human basic fibroblast growth factor. Biomaterials, 32, 8172, 2011.
33.
CassanoM., and CassanoP.Retraction pockets of pars tensa in pediatric patients: clinical evolution and treatment. Int J Pediatr Otorhinolaryngol, 74, 178, 2010.
34.
SomeyaT., TamuraY., and TsutsuiT.Cytological and cytogenetic effects of the fluoroquinolone ofloxacin on human periodontal ligament fibroblasts. J Periodontal Res, 35, 352, 2000.
35.
OuedraogoG., MorliereP., SantusR., Miranda, and CastellJ.V.Damage to mitochondria of cultured human skin fibroblasts photosensitized by fluoroquinolones. J Photochem Photobiol B, 58, 20, 2000.
36.
O'ConnorK.N., TamM., BlevinsN.H., and PuriaS.Tympanic membrane collagen fibers: a key to high-frequency sound conduction. Laryngoscope, 118, 483, 2008.
37.
JesicS.D., DimitrijevicM.V., NesicV.S., JoticA.D., and SlijepcevicN.A.Temporalis fascia graft perforation and retraction after tympanoplasty for chronic tubotympanic otitis and attic retraction pockets: factors associated with recurrence. Arch Otolaryngol Head Neck Surg, 137, 139, 2011.
38.
SchillerA., and WormaldP.J.Malleomyringoplasty using a silicone prosthesis. J Laryngol Otol, 106, 205, 1992.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
