bone regeneration in the maxillary sinus using an autologous

Bone Regeneration in the Maxillary SinusUsing an Autologous Fibrin-Rich Block With

Concentrated Growth Factors AloneDong-Seok Sohn, DDS, PhD,* Jeung-Uk Heo, DDS, PhD,† Dong-Ho Kwak, DDS, PhD,‡

Dong-Eung Kim, DDS, PhD,§ Ji-Min Kim, DDS,� Jee-Won Moon, DDS,¶ Ju-Hyoung Lee, DDS,¶and In-Sook Park, DDS, PhD¶

The atrophic posterior maxilla isa challenging site for oral reha-bilitation with dental implants

due to insufficient bone volume to ac-commodate dental implants. Crestalapproaches or lateral window ap-proaches for sinus augmentation arethe most common surgical techniquesto overcome vertical deficiencies ofthe atrophic posterior maxilla.1–5 Forthe past several decades, bone graftshave been considered a prerequisitefor the success of sinus augmentation.Thus, variable bone grafts, such asautografts, allografts, xenografts, allo-plasts, or combinations of differentgraft materials, have been used widelyto augment the maxillary sinus. Asspace makers, all bone grafts are con-sidered highly predictable for newbone formation in the sinus.6–11 How-ever, successful bone augmentation inthe maxillary sinus without bone graft-

ing and osseointegration of implantshave been reported in human and an-imal studies.12–15 In addition, bone ref-ormation in the maxillary sinus, usingpatients’ own venous blood alone andabsorbable gelatin sponges alone asalternatives to bone grafts, has beenreported in clinical studies.16,17

Platelet aggregates, such asplatelet-rich plasma and platelet-richgrowth factors, have been used to ac-celerate new bone formation associ-ated with guided bone regenerationand sinus grafts.18–20 However, the ef-fect of platelet-rich plasma on newbone formation is debatable.21 The ex-pression of growth factors from col-

lected platelet aggregates is variable.22

Recently, successful bone reformationin the sinus using fibrin-rich blockswith concentrated growth factors(CGFs) as an alternative to bone graft-ing has been reported with limiteddata.23 To date, there have been nostudies indicating implant survivalrate on bone formation using fibrin-rich blocks with CGFs alone. The aimof this study was to verify the bonereformation by the application of onlyfibrin-rich blocks with CGFs in thenew compartment between the ele-vated sinus membrane and the sinusfloor in terms of radiologic, histologic,and clinical results.

*Chairman and Professor, Department of Dentistry and Oraland Maxillofacial Surgery, Catholic University Hospital ofDaegu, Republic of Korea.†Private Practice, President, Goodwill Dental Hospital, Pusan,Republic of Korea.‡Private Practice, President, Kwak’s Dental Hospital, Daegu,Republic of Korea.§Private Practice, President, Dr. Kim’s Dental Clinic, Daegu,Republic of Korea.�Resident, Department of Dentistry and Oral and MaxillofacialSurgery, Catholic University Hospital of Daegu, Republic ofKorea.¶Instructor, Department of Dentistry and Oral and MaxillofacialSurgery, Catholic University Hospital of Daegu, Republic ofKorea.

Reprint requests and correspondence to: Dong-SeokSohn, DDS, PhD, Department of Oral andMaxillofacial Surgery, Catholic University Hospital ofDaegu, 3056-6 Daemyung-4 Dong, Namgu, Daegu705-718, Republic of Korea, Phone: �82 53-6504288,Fax: �82 53-6227067, E-mail: [email protected]

ISSN 1056-6163/11/02005-001Implant DentistryVolume 20 • Number 5Copyright © 2011 by Lippincott Williams & Wilkins

DOI: 10.1097/ID.0b013e31822f7a70

Purpose: The purpose of thisstudy was to evaluate the predict-ability of new bone formation in themaxillary sinus using an autologousfibrin-rich blocks with concentratedgrowth factors (CGFs) alone as analternative to graft material.

Materials and Methods: A totalof sixty-one sinus grafts were consec-utively performed using the lateralwindow approach. After making re-placeable bony window, the sinusmembrane was elevated to make anew compartment. After 113 implants(average 13 mm high) with 11 differ-ent systems were placed simultane-ously, the collected fibrin-rich blockswith CGFs alone were inserted in thesinus. To seal the lateral window, thebony window was repositioned. Radi-

ographic, clinical, and histologicevaluation was performed to verifysinus augmentation.

Results: No significant postoper-ative complications developed. Newbone consolidation in all augmentedmaxillary sinus was observed alongthe implants on plain radiographs andon cone-beam computed tomograms.The success rate of implant was98.2% after an average of 10 monthsloading.

Conclusion: Fibrin-rich blockswith CGFs act as an alternative to bonegrafting and can be a predictable pro-cedure for sinus augmentation. (ImplantDent 2011;20:1–000)Key Words: maxillary sinus augmenta-tion, fibrin, growth factor, platelet ag-gregate, replaceable bony window

IMPLANT DENTISTRY / VOLUME 20, NUMBER 5 2011 1

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MATERIALS AND METHODSPatient Selection

The present study populationcomprised 61 consecutive sinus graftsin 53 patients, 30 men and 23 women,ranging from 27 to 75 years of age(mean age, 51.3 years). The surgerywas performed at the Department ofOral and Maxillofacial Surgery, Cath-olic University Medical Center, and at2 private practices in Daegu, Korea,from September 2008 to October2009. All patients were informedabout the treatment procedure, andoral and written consent was obtained.Before the sinus graft procedure wasperformed, patients’ medical historieswere carefully evaluated, and patientswith disease known to affect bone me-tabolism were excluded. Smokerswere not excluded from the study butwere informed that smoking couldcompromise the quality of the sinuslift and reduce the success rate of im-plants. Preoperative plain panoramicradiograms and cone-beam computedtomograms (Combi; Pointnix Co.,Seoul, Korea, or i-Cat; Imaging Sci-ences, Hatfield, PA) were taken toevaluate preoperative sinus conditionsand residual bone heights and later toassess postoperative bone gain. Theresidual bone heights at the implantsites were between 0.5 mm and 10 mm(average � SD: 3.9 � 2.1 mm). Theresidual bone heights at the implantsites were between 0.5 and 5 mm in75% of sinuses, and 25% of sinusesshowed bone heights of 6 to 10 mm.Huge cysts (ranging from 17 mm to 30mm wide) were observed in 6 maxil-lary sinuses. One maxillary sinusshowed thickened sinus membrane(�5 mm) (Table 1).

Preparation of Fibrin-Rich BlocksWith CGFs

Fibrin-rich blocks were preparedaccording to Sacco’s protocol.24 Be-fore sinus grafting, 20 to 60 mL ofpatient’s venous blood was taken from

the patient’s forearm, and the venousblood was divided into 2 to 8 glass-coated test tubes without anticoagu-lants. The blood in the test tubes wascentrifuged at 2400 to 2700 rpm usinga specific centrifuge with a rotor turn-ing at alternated and controlled speedsfor 12 minutes (Medifuge; Silfradentsrl, Sofia, Italy); 2 to 6 pieces offibrin-rich blocks were prepared usingthis specific centrifuge. The collectedfibrin-rich blocks were characterizedby 4 phases. The uppermost layer wasrepresented by the serum (bloodplasma without fibrinogen and coagu-lation factors), and the second layerwas the fibrin buffy coat layer repre-sented by a very large and dense po-lymerized fibrin block. The third layerwas a liquid phase containing theCGFs, white line cells, and stem cellswaiting for stimulation and to differ-entiate into specialized cell types. Thelowest red layer represented platelet-rich coagulation. The red phase con-sisted of concentrated red and whiteblood cells, platelets, and clotting fac-tors (Fig. 1, a). In this study, the sec-ond layer with the fibrin buffy coatand the third liquid phase were used asalteratives to bone substitutes for sinusaugmentation.

Surgical and Prosthetic Procedures

Prophylactic oral antibiotics,Cefditoren pivoxil (Meiact; BoryungParm., Seoul, Korea), 300 mg threetimes per day, were used routinely,beginning 1 day before the procedureand continuing for 7 days. Surgerywas performed under local maxillaryblock anesthesia using 2% lidocainewith 1:100,000 epinephrine. Flomoxefsodium (Flumarin; Ildong Pharmaceu-tical Co., Korea, 500 mg intrave-nously) was administered 1 hourbefore surgery. Maxillary sinus floorelevation via the lateral approach wascompleted on all patients. The fullthickness of mucoperiosteal flap waselevated to expose the lateral wall of

the maxillary sinus. The piezoelectricsaw, with a thin blade (S-Saw; BukbooDental Co., Daegu, Korea), connectedto piezoelectric device (Surgybone; Sil-fradent srl), was used with copious sa-line irrigation to create the replaceablerectangular bony window at the lateralwall of the maxillary sinus. The ante-rior vertical osteotomy was made 2mm distal to the anterior vertical wallof the maxillary sinus and the distalosteotomy was made approximately20 mm away from the anterior verticalosteotomy. The height of the verticalosteotomy was approximately 10 mm.The anterior and inferior osteotomylines were tilted to the inside of themaxillary sinus lateral wall, and thensuperior and posterior osteotomiesperpendicular to the sinus wall weremade. This design of osteotomy facil-itated the precise replacement of thebony window as a barrier over theinserted fibrin-rich blocks in the max-illary sinus (Fig. 1, b and c). The bonywindow was detached carefully to ex-pose the sinus membrane. The sinusmembrane was carefully dissectedfrom the sinus floor walls with a flatblunt-edged sinus membrane elevator.Dissection of the sinus membrane wascontinued to reach the anterior andmedial walls of the sinus cavity. Theheight of exposed medial wall wasparallel to the superior osteotomy lineof the lateral window.

After elevation of sinus mem-brane, a 1-step, undersized osteotomywas used to obtain initial stability ofthe implant at implant sites with lowbone height. To verify the effect of thefibrin-rich block with CGFs, and toexclude the effect of the implant sys-tem, 11 kinds of implant systems with4 different implant surfaces wereplaced in this study. A total of 113implants with 4 different surfaced im-plant systems were placed. Twenty-eight resorbable blast media-surfacedimplants (10 Dentis Implants [DentisInc., Daegu, Korea] and 18 SybronPro

Table 1. Summary of Characteristics and Findings of Patients

No. ofPatient

AverageAge (y)

No. ofSinusGraft

AverageBone Height(mm � SD)

No. ofImplant

AverageHealing Time

(wk � SD)

Average VerticalBone Gain(mm � SD)

AverageLoading Period

(wk � SD)

SuccessRate(%)

53 51.3 61 3.9 � 2.1 113 21.4 � 5.6 9.53 � 2.64 40 � 15.5 98.2

2 BONE REGENERATION AS AN ALTERNATIVE TO BONE GRAFTING • SOHN ET AL

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XRT implants [Sybron Implant Solu-tions, Grendore, CA]) were placed.Forty-seven hydroxylapatite-coatedimplants (14 Tapered screw vent im-plants [Zimmer Dental Inc., Carlsbad,CA]; 31 Legacy implants [Implant Di-rect LLC, Calabasas Hills, CA]; and 2Bio-tite implants [Dio Implant Co.,Busan, Korea]) were placed. Thirty-four sand-blasted, large grit, acid-etched surface implants (MIS ImplantsTechnologies Ltd., Shlomi, Israel)were placed. Four sintered porous-surfaced implants (Endopore im-plants; Sybron Implant Solutions)were placed.

Two to six pieces of fibrin-richblocks with CGFs were inserted in thenew compartment between the ele-vated sinus membrane and the sinusfloor (Fig. 1, d). The bony portion ofthe lateral window was repositioned toprevent soft tissue sinus cavity in-growths and to promote new bone for-mation from the lateral wall of themaxillary sinus (Fig. 1, e). Flaps weresutured using interrupted mattressPTFE sutures (Cytoplast; OsteogenicBiomedical, TX) to achieve passiveprimary closure. Patients were in-structed not to blow their noses for 2weeks after surgery and to cough or

sneeze with an open mouth. Antibiotictherapy was continued postoperativelyfor 7 days, and the sutures were re-moved 10 days postoperatively. Aftersinus augmentation, plain panoramicradiographs and cone-beam computedtomograms (Combi; Pointnix Co., andi-Cat; Imaging Sciences) were madeimmediately after surgery. An average21.4 weeks (SD: �5.6) healing periodwas allowed for new bone consolida-tion and the osseointegration of im-plants. Plain panoramic radiogramsand dental cone-beam computed to-mograms were obtained to assess thenew bone formation around the im-plants before the implants were uncov-ered (Fig. 1, f). Bone biopsies weretaken in 5 cases through the reposi-tioned lateral window to verify newbone formation in the sinus during theuncovering. Implants were loadedwith provisionals for an average 6weeks to contour the soft tissue profilearound the implant before the finalprosthesis was delivered. In the max-illary sinuses with huge cysts, cysticfluid was aspirated with a syringe orsuctioned through the stab incisionarea made by the surgical blade in thesinus membrane. And the same sinusaugmentation procedure using fibrin-rich blocks with CGFs was performedafter removal of cysts (Fig. 2, a–i).

Histologic Preparation

Five bone biopsies were harvestedfrom the repositioned lateral windowduring the uncovering procedure afteran average of 5 months healing period.Biopsy specimens were immediatelyfixed in 4% formaldehyde for 24 hoursat 4°C and decalcified in 10% formicacid for 3 days. After dehydration inan ascending alcohol series, the biop-sies were embedded in paraffin, and5-�m thick sections, parallel to thelongitudinal axis of the biopsy speci-men, were prepared using a mi-crotome. Sections were stained withMayer’s hematoxylin and eosin stainand Masson’s Trichrome stain, and thespecimens were evaluated to verifynewly formed bone and soft tissuechanges under light microscopy. Thespecimens were photographed usingthe AxioCam MRc5 (Carl Zeiss, Ger-

Fig. 1. a, A fibrin-rich block with concentrated growth factors made by a specific centrifugation(Medifuge, Silfradent srl). The second and third layers were utilized for sinus augmentation. b,Cone-beam computed tomogram showing 1 to 2 mm bone height at the right maxillary second(left) and first molar (right), respectively (from patient number 50). c, The piezoelectric saw,connected to piezoelectric device (Surgybone, Silfradent srl), was used to create the replace-able lateral window of maxillary sinus in all cases. d, After careful elevation of the sinusmembrane, 4 pieces of fibrin-rich block were inserted into the new compartment between theelevated membrane and the sinus floor. Two tapered design implants (Dentis Implants; DentisInc.) were placed simultaneously after a 1-step down osteotomy. The initial stability was good.e, The bony window was repositioned with stability to seal the window. f, Cone-beam com-puted tomographic scans revealed new bone consolidation along the implant body at the rightmaxillary second (left) and the first molar (right), respectively, after 18 weeks healing. Implantswere uncovered at this stage. g, Radiogram after 5 months loading. Note the newly formedbone in the sinus.


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many) interfaced with the AxiophotPhotomicroscope (Carl Zeiss).

RESULTS

After sinus grafting, no significantpostoperative complications devel-oped in any augmented sinus duringthe healing period. After an average of5 months healing period, plain pan-oramic radiograms and cone-beamcomputed tomograms showed newlyformed bone along implant bodies and

around implant apices in all cases ex-cept for 1 augmented sinus that ob-tained a large membrane perforationduring sinus membrane elevation.

Membrane perforation occurred in10 cases (16.4% of perforation rate).One perforation was made during os-teotomy with the saw insert, and theothers developed during the elevationof the sinus membrane. Eight perfora-tions showed small perforations (�5mm wide). Five small perforated

membranes were repaired with colla-gen membrane (CollaTape; ZimmerDental Inc.) before fibrin-rich blocksinsertion. The other 3 small perforatedsites were not repaired with collagenmembrane. No radiographic differ-ence on new bone augmentation wasseen between the 2 groups after anaverage of 5 months healing period.Large membrane perforations (�10mm wide) were observed in 2 cases.One perforated sinus membrane wasrepaired with collagen membrane be-fore inserting the fibrin-rich blocks.The postoperative cone-beam com-puted tomogram showed favorablebone reformation around the implantbody in this patient. The other largeperforation developed because the si-nus membrane was fused to the peri-osteum in the extraction socket. Thisperforation site was not repaired withcollagen membrane before the 2pieces of fibrin-rich block with CGFswere inserted. The sinus showed par-tially formed new bone along theimplant in radiograms. The new com-partment between the elevated sinusmembrane and sinus floor could notcontain a blood clot or fibrin-richblocks in this case, so only partialbone augmentation was achieved.However, clinically, implant prosthe-ses have been stable up to 9 months infunction.

All repositioned lateral bony win-dows were well healed and fixed to thelateral wall of sinus in all cases atuncovering. The repositioned lateralbony windows acted as homologousbarriers with stability to prevent softtissue ingrowth into the sinus cavity.The success rate of implant was98.2%, after an average of 10 monthspostloading. The criteria of Buseret al25 were used to evaluate theosseointegration of implants. Tworesorbable blast media-surfaced im-plants failed. One implant was re-moved at uncovering and anotherfailed 3 months after loading. Evenwhen implants failed, newly formedbone was evident in the sinus. Histo-logically, bone biopsies revealed noinflammatory reactions, all showedactive new bone formation. The spec-imens revealed well-organized andmature lamellar bone. Osteoblasts

Fig. 2. a, Cone-beam computed radiogram showing approximately 30-mm wide mucousretention cyst in the sinus. High septum is seen in the tomographic scan. The residual bonewas 3 mm and 2 mm at the left maxillary first and second molar respectively (from patientnumber 1). b, Approximately 15 mL of cystic fluid was aspirated with an 18-G needle andsyringe after making 2 replaceable bony windows. c, Two pieces of fibrin-rich block wereinserted into new anterior and posterior compartments, respectively, after membrane eleva-tion. Three tapered design implants (Tapered screw vent implant; Zimmer Dental Inc.) wereplaced. Two bony windows were replaced to seal the lateral window. d and e, Cone-beamcomputed tomographic scans showing new bone consolidation around implants after 4months of healing. Resized cyst and new bone formation is seen in the sinus. f, Bone biopsywas performed through the well-healed bony window after 4 months healing. Histologicexamination shows dense and mature new bone (asterisks) and osteoblasts (arrow) next to thereplaced bony window in hematoxylin and eosin stain. This indicates active new bone forma-tion in the sinus (magnification, �12.5 [left] and �100 [right]). g, Active new bone formation(blue color) is seen in Masson’s Trichrome stain (magnification, �12.5 [left] and �100[right]). hand i, Clinical and radiographic view of final prosthesis 7 months after loading.



were easily revealed at high magnifi-cation, and blood vessels were re-vealed in the marrow space (Fig. 3).

The residual bone height at theimplant sites were between 0.5 and 10mm (average � SD: 3.9 � 2.1 mm).The residual bone height at the im-plant sites were between 0.5 and 5 mmin 75% of the sinus grafts, and 25% ofthe sinuses showed 6 to 10 mm boneheights. Residual bone height did notaffect the success rate of implant.Huge cysts (ranging from 17 to 30 mmhigh) were observed in 6 maxillarysinuses. The cystic fluid was aspiratedor suctioned through the stab incisionmade in the sinus membrane beforemembrane elevation to facilitate mem-brane elevation. The cysts did not af-fect bone reformation in the maxillarysinus in this study.

DISCUSSION

Various studies have reportedbone reformation in the maxillary si-nus with bone grafting in humans andanimals.12–17 Palma et al13 reported nohistologic differences on bone refor-mation in the maxilla betweenmembrane-elevated and grafted sites,regarding implant stability, bone-implant contacts, and bone area withinand outside implant threads in ani-mals. Sohn et al14 reported favorablenew bone formation in the maxillary

sinus without bone grafting and clini-cal implant success with in vivo histo-logic evidence for the first time. Sohnet al17 also reported that the fast ab-sorbable gelatin sponge insertedloosely under the elevated sinus mem-brane acted as space maintainer fornew bone formation in the maxilla asan alternative to bone fillers. Plateletaggregates, such as platelet-richplasma and platelet-rich fibrin gel inCGFs, have been used to acceleratenew bone formation associated withguided bone regeneration and sinusgrafting for many years.18–20 However,the effect of platelet-rich plasma onnew bone formation in the sinus graftis debatable.21 Fibrin-rich block cankeep higher CGFs than platelet-richplasma and can induce faster.26,27 Youet al28 reported that platelet-rich fibringel can induce higher bone to implantcontact than can platelet-rich plasmain bony defects around dental im-plants. Fibrin-rich gel is known torelease growth factors, such as trans-forming growth factor-�1, platelet-derived growth factor, and vascularendothelial growth factor slowly, andaccelerates new bone formation whencombined with bone grafting in themaxillary sinus.27,29,30 In addition,fibrin-rich blocks with CGFs as thesole material acted as an alternative tobone grafting and induced fast new

bone formation in the sinus.23 Com-pared with platelet-rich plasma orplatelet-rich growth factors, fibrin-rich blocks with CGFs are simple tomake and do not require any synthet-ics or biomaterials, such as bovinethrombin and calcium chloride, tomake gel, so it is free from the riskof cross-contamination.

To our knowledge, studies on theeffect of fibrin-rich blocks with CGFsalone as an alternative to bone graftingand functional survival rate of implantwas not reported. Therefore, this studywas designed to evaluate the effect offibrin-rich blocks with CGFs alone onbone reformation in the maxillary si-nus by clinical, radiographic, and his-tologic analyses with expanded data.Fast new bone formation in all thesinuses was apparent radiographically,and dense and mature new bone wasseen in the sinus histology in thisstudy. The resorbable or nonresorb-able barrier membrane is necessary toprevent ingrowths of soft tissue intothe sinus cavity.31,32 Instead of resorb-able or nonresorbable barrier mem-branes, the replaceable bony windowwas used to seal the lateral bony win-dow in this study. According to thestudy by Sohn et al15, new bone for-mation begins from the inner surfaceof the repositioned bony window earlyin the healing stage, but new boneformation was not shown from thecollagen membrane over the bonywindow early in the healing phase.Replaceable bony windows offer moreadvantages over using resorbable ornonresorbable barrier membranes toseal the lateral bony window. Replace-able bony windows are not only ho-mologous bony windows free from therisk of cross-contamination but alsoacts as osteoinductive substrates foraccelerating new bone formation inthe sinus. The ultrasonic piezoelectricdevice was effective in making thereplaceable bony window. Comparedwith the rotary bur, piezoelectric bonecut provides highly controlled osteot-omy and reduces the possibility ofmembrane perforation and inducedminimal trauma to soft and hard tis-sue.33–37 When creating the replaceablelateral bony window, a tilted osteot-omy into the sinus cavity was required

Fig. 3. Histologic finding from patient number 14. Active new bone formation is seen inhematoxylin and eosin stain (magnification, �12.5 [a] and �100[b]) and in Masson’sTrichrome stain (�12.5 [c] and �100 [d]). Abundant osteoblasts (arrows) are shown alongnewly formed bone. Red blood cells are shown in newly formed blood vessels.


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to prevent the replaceable bony win-dow from dropping into the maxillarysinus cavity.38 The replaceable bonywindows made by the thin piezoelec-tric saw could be precisely reposi-tioned because of the combination ofthe tilted osteotomy into the sinus, thehighly controlled osteotomy, and theminimal bone loss during osteot-omy.38–41 Initial stability of implantwas important to have successful os-seointegration.42 Regardless, 75% ofimplant sites had bone heights be-tween 0.5 and 5 mm in this study, andthe initial stability of the implants wasstable. Initial stability of implants wasachieved by a 1-step down undersizedosteotomy and the placement of a ta-pered design implant. All implantswere stable for an average of 10months loading, thanks to stable initialstability.

CONCLUSION

According to this study, bonegraft material may not be a prerequi-site for sinus augmentation. Insertionof fibrin-rich blocks with CGFs as analternative to bone grafting and simul-taneous implantation showed success-ful new bone formation in the sinus,and this can be a predictable procedurefor sinus augmentation.

Disclosure

The authors claim to have no finan-cial interest in any company or any ofthe products mentioned in this article.

ACKNOWLEDGMENTS

This study was supported by aresearch fund from the Implant Insti-tute of Catholic University MedicalCenter of Daegu, Republic of Korea.

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bone regeneration in the maxillary sinus using an autologous

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