Use of various bone graft substitutes are advised to prevent bone loss, periodontal problems, and enhance bone formation after surgical removal of the mandibular third molar. Choice of graft substitute depends on biological properties and the cost of the material. So, a preliminary study was planned to evaluate and compare the effectiveness of eggshell-derived nano-hydroxyapatite as an emerging graft substitute for the enhancement of bone regeneration.
Materials and methods
Twelve patients (out of 20 enrolled) were finally assessed for bone healing after surgical removal of bilateral mandibular third molars in a split-mouth randomized controlled clinical study. All of them were assessed and compared at baseline, first, third, and sixth month. Clinically wound healing and probing depth were assessed. Radiographically the changes in density, bone formation characteristics, and bone level were evaluated. The observers were blinded for the surgical procedure and follow-up duration. The study protocol was approved by Institutional Ethics Committee and registered with National clinical trial registry.
Results
Wound healing was uneventful in all 24 extraction sites of 12 patients. Trabecular bone pattern with increased bone density was observed indicating complete bone healing in the graft group at third month. Probing depth was gradually decreased over a follow-up period and remained within normal limits during the third-month follow-up. These changes in the graft group were significant compared to the control group. The grafting with eggshell-derived nano-hydroxyapatite showed better bone regeneration properties without any infection or undue reactions.
Conclusion
Eggshell-derived nano-hydroxyapatite showed enhancement of bone regeneration compared to the control group. Grafting maintained bone height and prevented periodontal problem emergence. Eggshell-derived nano-hydroxyapatite is a safe synthetic graft substitute because it is derived from eggshell without any diseases transfer risks, unlike allografts. The process of preparation is environment-friendly. The beneficial effects of eggshell-derived nano-hydroxyapatite may be extrapolated to develop an ideal economic graft substitute.
DamienCJParsonsJR.Bone graft and bone graft substitutes: a review of current technology and applications. J Appl Biomater1991;
2: 187–208.
2.
KattimaniVSKondakaSLingamaneniKP.Hydroxyapatite – past, present, and future in bone regeneration. Bone Tissue Regen Insights2016;
7: BTRI.S36138.
3.
JoosUWiesmannHPNeunzehnJ. Chapter 10. Applications of biomaterials in alveolar and maxillofacial bone reconstruction. In: Preprosthetic and maxillofacial surgery biomaterials, bone grafting and tissue engineering. Cambridge: Woodhead Publishing Limited, 2011, pp.175–185.
4.
GreenwaldASBodenSDGoldbergVM, et al.
Bone-graft substitutes: facts, fictions, and applications. J Bone Joint Surg Am2001;
83-A: 98–103.
5.
HaugenHAvardJPeraleG, et al.
Bone grafts : which is the ideal biomaterial ?J Clin Periodontol2019;
46: 92–102.
6.
LeeS-WKimS-GBalazsiC, et al.
Comparative study of hydroxyapatite from eggshells and synthetic hydroxyapatite for bone regeneration. Oral Surg Oral Med Oral Pathol Oral Radiol2012;
113: 348–355.
7.
KumarGSThamizhavelAGirijaEK.Microwave conversion of eggshells into flower-like hydroxyapatite nanostructure for biomedical applications. Mater Lett2012;
76: 198–200.
8.
KumarGSGirijaEK.Flower-like hydroxyapatite nanostructure obtained from eggshell: a candidate for biomedical applications. Ceram Int2013;
39: 8293–8299.
9.
KugelbergCFAhlströmUEricsonS, et al.
Periodontal healing after impacted lower third molar surgery: a retrospective study. Int J Oral Surg1985;
14: 29–40.
FarinaRTrombelliL.Wound healing of extraction sockets. Endod Top2011;
25: 16–43.
12.
LeeC-THumLChenY-W.The effect of regenerative periodontal therapy in preventing periodontal defects after the extraction of third molars: a systematic review and meta-analysis. J Am Dent Assoc2016;
147: 709–719.e4.
13.
ThrondsonRRSextonSB.Grafting mandibular third molar extraction sites: a comparison of bioactive glass to a nongrafted site. Oral Surg Oral Med Oral Pathol Oral Radiol Endod2002;
94: 413–419.
14.
NathaniDBSequeiraJRaoB.Comparison of platelet rich plasma and synthetic graft material for bone regeneration after third molar extraction. Ann Maxillofac Surg2015;
5: 213–218.
15.
KimSHKimWChoJH, et al.
Comparison of bone formation in rabbits using hydroxyapatite and β-tricalcium phosphate scaffolds fabricated from egg shells. Adv Mater Res2008;
47–50: 999–1002.
16.
ParkJBaeSSuhJ, et al.
Evaluation of bone healing with eggshell-derived bone graft substitutes in rat calvaria: a pilot study. J Biomed Mater Res A2008;
87: 203–214.
17.
CaiY-DWangS-MChouAHK, et al.
Zinc-coated carbonate apatite derived from avian eggshell for potential use as bone substitute. Part I: preparation and properties. Implant Dent2012;
21: 230–235.
18.
KattimaniVSChakravarthiPSKanumuruNR, et al.
Eggshell derived hydroxyapatite as bone graft substitute in the healing of maxillary cystic bone defects: a preliminary report. J Int Oral Health2014;
6: 15–19.
19.
KattimaniVLingamaneniKPChakravarthiPS, et al.
Eggshell-derived hydroxyapatite: a new era in bone regeneration. J Craniofac Surg2016;
27: 112–117.
20.
KattimaniVSLingamaneniKP.Natural bioceramics: our experience with changing perspectives in the reconstruction of maxillofacial skeleton. J Korean Assoc Oral Maxillofac Surg2019;
45: 34–42.
21.
KattimaniVLingamaneniKPEkG, et al. Eggshell derived nanohydroxyapatite(nHA) with platelet-rich fibrin (PRF) as a barrier membrane – a new technique for socket preservation. J Korean Assoc Oral Maxillofac Surg 2019. Epub ahead of print 2019, http://www.jkaoms.org/journal/view.html?uid=2929&vmd=Full (accessed 20 June 2019).
22.
MunhozEAFerreira JuniorOYaeduRYF, et al.
Radiographic assessment of impacted mandibular third molar sockets filled with composite xenogenic bone graft. Dento Maxillo Facial Radiol2006;
35: 371–375.
23.
MunhozEABodaneziAFerreira JuniorO, et al.
Bone crestal height and bone density after third-molar extraction and grafting: a long-term follow-up study. Clin Oral Invest2011;
15: 123–126.
24.
de MeloDGde Santana SantosTSehnFP, et al.
Evaluation of inorganic bovine bone graft in periodontal defects after third molar surgery. Ann Maxillofac Surg2015;
5: 198–202.
25.
KattimaniVSBajantaiNVSriramSK, et al.
Observer strategy and radiographic classification of healing after grafting of cystic defects in maxilla: a radiological appraisal. J Contemp Dent Pract2013;
14: 227–232.
26.
MarmaryYBrayerLTzukertA, et al.
Alveolar bone repair following extraction of impacted mandibular third molars. Oral Surg Oral Med Oral Pathol1986;
61: 324–326.
27.
RakprasitkulSPairuchvejV.Mandibular third molar surgery with primary closure and tube drain. Int J Oral Maxillofac Surg1997;
26: 187–190.
28.
BlumIR.Contemporary views on dry socket (alveolar osteitis): a clinical appraisal of standardization, aetiopathogenesis and management: a critical review. Int J Oral Maxillofac Surg2002;
31: 309–317.
29.
DodsonTBPetersonLJ.Reconstruction of alveolar bone defects after extraction of mandibular third molars: a pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol Endodontol1996;
82: 241–247.
30.
KanKWLiuJKSLoECM, et al.
Residual periodontal defects distal to the mandibular second molar 6-36 months after impacted third molar extraction. J Clin Periodontol2002;
29: 1004–1011.
31.
SivakumarMKumarTSShanthaKL, et al.
Development of hydroxyapatite derived from Indian coral. Biomaterials1996;
17: 1709–1714.
32.
WuS-CTsouH-KHsuH-C, et al.
A hydrothermal synthesis of eggshell and fruit waste extract to produce nanosized hydroxyapatite. Ceram Int2013;
39: 8183–8188.
33.
KaurPMariaA.Efficacy of platelet rich plasma and hydroxyapatite crystals in bone regeneration after surgical removal of mandibular third molars. J Maxillofac Oral Surg2013;
12: 51–59.
34.
PandayVUpadhyayaVBerwalV, et al.
Comparative evaluation of G bone (hydroxyapatite) and G-graft (hydroxyapatite with collagen) as bone graft material in mandibular III molar extraction socket. J Clin Diagn Res JCDR2015;
9: ZC48–52.
35.
GholamiGA.Clinical, histologic and histomorphometric evaluation of socket preservation using a synthetic nanocrystalline hydroxyapatite in comparison with a bovine xenograft: a randomized clinical trial. Clin Oral Implants Res2012;
23: 1198–1204.
36.
GötzWGerberTMichelB, et al.
Immunohistochemical characterization of nanocrystalline hydroxyapatite silica gel (NanoBone(r)) osteogenesis: a study on biopsies from human jaws. Clin Oral Implants Res2008;
19: 1016–1026.
37.
ArtziZTalHDayanD.Porous bovine bone mineral in healing of human extraction sockets. Part 1: histomorphometric evaluations at 9 months. J Periodontol2000;
71: 1015–1023.
38.
LeeJSBaekSDVenkatesanJ, et al.
In vivo study of chitosan-natural nano hydroxyapatite scaffolds for bone tissue regeneration. Int J Biol Macromol2014;
67: 360–366.
39.
ParkJWJangJHBaeSR, et al.
Bone formation with various bone graft substitutes in critical-sized rat calvarial defect. Clin Oral Implants Res2009;
20: 3728.
40.
OliveiraHLDa RosaWLOCuevas-SuárezCE, et al.
Histological evaluation of bone repair with hydroxyapatite: a systematic review. Calcif Tissue Int2017;
101: 341–354.
41.
MorjariaKRWilsonRPalmerRM.Bone healing after tooth extraction with or without an intervention: a systematic review of randomized controlled trials. Clin Implant Dent Relat Res2014;
16: 1–20.
42.
AraújoMGSilvaCOMisawaM, et al.
Alveolar socket healing: what can we learn?Periodontol 20002015;
68: 122–134.
43.
RipamontiU.Osteoinduction in porous hydroxyapatite implanted in heterotopic sites of different animal models. Biomaterials1996;
17: 31–35.
44.
GosainAKSongLRiordanP, et al.
A 1-year study of osteoinduction in hydroxyapatite-derived biomaterials in an adult sheep model: part I. Plast Reconstr Surg2002;
109: 619–630.
45.
PilloniAPompaGSaccucciM, et al.
Analysis of human alveolar osteoblast behavior on a nano-hydroxyapatite substrate: an in vitro study. BMC Oral Health2014;
14: 22.
46.
KasajAWillershausenBReichertC, et al.
Ability of nanocrystalline hydroxyapatite paste to promote human periodontal ligament cell proliferation. J Oral Sci2008;
50: 279–285.
47.
KasajARöhrigBZafiropoulosG-G, et al.
Clinical evaluation of nanocrystalline hydroxyapatite paste in the treatment of human periodontal bony defects–a randomized controlled clinical trial: 6-month results. J Periodontol2008;
79: 394–400.
48.
HeinzBKasajATeichM, et al.
Clinical effects of nanocrystalline hydroxyapatite paste in the treatment of intrabony periodontal defects: a randomized controlled clinical study. Clin Oral Invest2010;
14: 525–531.
49.
HaghighatAHekmatianEAbdinianM, et al.
Radiographic evaluation of bone formation and density changes after mandibular third molar extraction: a 6 month follow up. Dent Res J2011;
8: 1–5.
50.
DuttaSRPassiDSinghP, et al.
A randomized comparative prospective study of platelet-rich plasma, platelet-rich fibrin, and hydroxyapatite as a graft material for mandibular third molar extraction socket healing. Natl J Maxillofac Surg2016;
7: 45–51.
51.
DurmuŞlarMCAlpaslanCAlpaslanG, et al.
Clinical and radiographic evaluation of the efficacy of platelet-rich plasma combined with hydroxyapatite bone graft substitutes in the treatment of intra-bony defects in maxillofacial region. Acta Odontol Scand2014;
72: 948–953.
52.
Arenaz-BúaJLuaces-ReyRSironvalle-SolivaS, et al.
A comparative study of platelet-rich plasma, hydroxyapatite, demineralized bone matrix and autologous bone to promote bone regeneration after mandibular impacted third molar extraction. Med Oral Patol Oral Cir Bucal2010;
15: e483–489.
53.
SinghMBhateKKulkarniD, et al.
The effect of alloplastic bone graft and absorbable gelatin sponge in prevention of periodontal defects on the distal aspect of mandibular second molars, after surgical removal of impacted mandibular third molar: a comparative prospective study. J Maxillofac Oral Surg2015;
14: 101–106.
54.
PengKYTsengYCShenEC, et al.
Mandibular second molar periodontal status after third molar extraction. J Periodontol2001;
72: 1647–1651.
55.
FariaAIGallas-TorreiraMLópez-RatónM.Mandibular second molar periodontal healing after impacted third molar extraction in young adults. J Oral Maxillofac Surg2012;
70: 2732–2741.
56.
VenkatesanJKimS-K.Nano-hydroxyapatite composite biomaterials for bone tissue engineering – a review. J Biomed Nanotechnol2014;
10: 3124–3140.
57.
SalmasiSNayyerLSeifalianAM, et al.
Nanohydroxyapatite effect on the degradation, osteoconduction and mechanical properties of polymeric bone tissue engineered scaffolds. Open Orthop J2016;
10: 900–919.
58.
RicciardiBFBostromMP.Bone graft substitutes: claims and credibility. Semin Arthroplasty2013;
24: 119–123.
