Reviews of Complications from Lateral and Crestal Sinus Lifts · Sinus elevation surgery is today considered one of the most predictable preprosthetic site-development bone augmentation

The Journal of Implant & Advanced Clinical Dentistry

Volume 8, No. 7 NoVember 2016

Histologic Analysis of Various Sinus Grafts

Reviews of Complications from Lateral and

Crestal Sinus Lifts

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The Journal of Implant & Advanced Clinical DentistryVolume 8, No. 7 • NoVember 2016

Table of Contents

6 Sinus Augmentation Complications: Part-I Associated with Lateral Technique (Direct Approach): A Review Dr. Pranav S Patil, Dr. M. L. Bhongade

14 Sinus Augmentation Complications: Part-II Associated with Crestal Technique (Indirect Approach): A Review Dr. Pranav S Patil, Dr. M. L. Bhongade

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The Journal of Implant & Advanced Clinical Dentistry • 3


Table of Contents

22 Histologic Analysis of theOutcomes of Split-Mouth Maxillary Sinus Augmentation with Allograft and Xenograft Grafting Mediums Edward Ruvins, Mark Stein,

34 Temperature Changes DuringImplant Osteotomies Utilizing Three Different Implant Systems: A Pilot Study Dr. Nikolaos Soldatos, Dr. David Gozalo, Dr. Kerri Font, Dr. David Moreno, Dr. Charles Powell


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Patil et al

Maxillary sinus augmentation pro-cedures using crestal or lateral approach are the predictable treat-

ment modalities for placing the implant in atro-phic maxillary posterior area. Like any other

dental procedures there is always risk of encountering the intra or postsurgical com-plications. This review article illustrates the complication, prevention and management associated with the lateral (Direct) technique.

Sinus Augmentation Complications: Part-I Associated with Lateral Technique

(Direct Approach): A Review

Dr. Pranav S Patil1 • Dr. M. L. Bhongade2

1. Post graduate student, Department of Periodontology & Implantology, Sharad Pawar Dental College and Hospital, Sawangi, Wardha, Maharashtra, India

2. Professor and Head, Department of Periodontology & Implantology, Sharad Pawar Dental College and Hospital, Sawangi, Wardha, Maharashtra, India

Abstract

KEY WORDS: Schneiderian membrane, septa, sinus infection, sinusitis.

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Patil et al

INTRODUCTIONSinus elevation surgery is today considered one of the most predictable preprosthetic site-development bone augmentation procedures.1 This high level of predictability has been shown in two ways. The first is that the outcome of lateral wall sinus elevation surgery, as mea-sured by implant survival in evidence-based reviews, has been shown to be highly predict-able.1-3 By making the appropriate evidence-based decisions regarding grafting materials, implant surfaces, and the use of barrier mem-branes over the lateral window, one can expect implant survival rates to be above 95%. The second is that complications are infrequent and those that occur during and after sinus grafting procedures are for the most part local-ized and readily remedied.4-7 This Review will discuss the major intraoperative and postop-erative complications and present both recom-mendations for complication prevention and treatment options should complications occur.

INTRAOPERATIVE COMPLICATIONS

Intraoperative complications are primarily the result of surgical difficulties encountered dur-ing the course of the procedure. These may be the result of the presence of complex ana-tomic situations (thin membranes, septa, thick or convex lateral walls), the choice of less pre-dictable treatment options, inadequate sys-temic or local diagnosis, or operator error. The most common intraoperative complication is Schneiderian membrane perforation. Other complications include intraoperative bleed-ing, perforations in the buccal flap and, much less frequently, injury to the infraorbital nerve.

SCHNEIDERIAN MEMBRANE PERFORATION

Perforation of the Schneiderian membrane is the most common intraoperative com-plication in sinus elevation surgery.8 The reported incidence in the literature varies from lows of 11% and 14%9 to a high of 56%10 when rotary window preparation is used.

In a CT study by Cho et al.,11 the perfo-ration rate was shown to be related to sinus width or, to be more specific, the angle made by the medial and lateral walls at the crest of the alveolus. The perforation rates were 62.5% for the narrow anterior part of the sinus (angle < 30°), 28.6% for the wider middle part of the sinus (angle 30-60°), and 0% for the wid-est posterior portion (angle > 60°). There are numerous maneuvers that are performed dur-ing sinus elevation surgery that place the Schneiderian membrane at risk. These include:l flap elevation (placing an elevator through a thin

crest or lateral wall or through a previous oroan-tral fistula that has healed with soft tissue only)

l preparation of the lateral window (specifically with rotary instrumentation)

Figure 1: Pre-operative radiograph.

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l elevation of the Schneiderian membrane with hand instrumentation (especially medially and in close proximity to septa

l placement of graft material (excessive pressure against membrane).

PREVENTIONA thorough knowledge of the 3D anatomy of the sinus is essential if the perforation rate is

to be kept to a minimum. A CT analysis will give information relating to the thickness of the crest and lateral walls, presence of discontinui-ties in the bony walls, width of the sinus, slope of the anterior sinus wall, membrane thickness, and the presence, size, and location of septa.

When septa are known to be present, it is advisable to lengthen the window in the antero-posterior direction so that the window is located

Figure 2: Perforation of Schneiderian membrane.

Figure 4: Placement of resorbable membrane into sinus.

Figure 3: Membrane elevated around membrane perforation.

Figure 5: Membrane in position within sinus.


Patil et al

both anterior and posterior to the septum. This allows for a lateral to medial elevation of the membrane from both sides of the septum. It must be realized that it is extremely difficult to elevate a membrane from a sharp septum in a mesial to distal direction while keeping the eleva-tor on the bony surface at all times. While mak-ing two separate windows has been proposed for this task,12 some explanation is required. It is

likely that the two separate windows will be so decreased in size that access and vision will be made even more difficult. In practice, the two win-dows are joined at the septum, creating one large window with improved access to both sides of the septum. A useful piezoelectric surgery tech-nique is to perform a full osteoplasty of the lat-eral window. This will readily reveal the location of a septum and allow for its removal and sub-

Figure 6: Bone graft placement.

Figure 8: Clinical view of Underwood Septa.

Figure 7: Post-operative radiograph showing graft containment.

Figure 9: Clinical view of Underwood Septa (alternative view).

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sequent membrane elevation from both sides.Piezoelectric surgery again proves itself to

be a valuable adjunct in sinus surgery in that its use has been shown by most authors and clinicians to result in decreased membrane perforation rates. Wallace et al.13 reported a membrane perforation rate of 7%. In this series all perforations occurred when com-pleting the elevation via hand instrumentation, with no perforations occurring when using the piezoelectric inserts. Blus et al.14 reported two perforations in 53 sinus elevations for a 3.8% perforation rate using two different piezoelec-tric devices. In a report of 56 consecutive sinus elevations, Toscano et al.15 reported a 3.6% perforation rate using piezoelective surgery.

Piezoelectric and conventional rotary surgi-cal techniques should differ depending on the thickness and shape of the lateral sinus wall. If the window is thin, a diamond insert can be used to make a superior hinge or a free-floating bone island attached to the membrane. This is then elevated horizontally. If the lateral wall is thick or it becomes convex in the malar emi-nence area, the entire lateral wall in the win-dow area can be eliminated via osteoplasty.

The most common means of repairing a per-forated Schneiderian membrane is to use a bioabsorbable collagen barrier membrane as a patch. Other techniques involve the use of sutures (difficult), platelet-poor plasma (PPP) spray or plasma rich in growth factors (PRGF) applications (if available at the time of perfo-ration), and the use of lamellar bone sheets.

The following generalizations should be helpful when attempting repairs:-l Very small perforations may self-repair by

membrane fold-over or clot formation

l Large perforations will require large repairs for stability

l Large repairs tend to tent apically when grafts are placed.

l Repair membranes placed next to the lateral wall tend to shift medially when graft is placed.Therefore, management of Schnei-

derian membrane perforations must be accompanied with the following: 1. Perform pre-surgical diagnosis with CT scans

to disclose difficult anatomy. 2. Make the window in the best location (3 mm

from the floor and anterior wall).3. Use piezoelectric surgery for lateral oste-

otomy and initial membrane elevation.4. Elevate the membrane from lateral to medial,

keep the instrument on bone at all times.5. Use a repair membrane that remains rigid

when wet to achieve the most stable repair. 6. All repairs must be stable.

INTRA-OPERATIVE BLEEDINGIntraoperative bleeding results from sev-

ering or damaging branches of the vascu-lar supply to the lateral wall of the sinus and the surrounding soft tissues. This bleeding is usually minor and of relatively short dura-tion, but in some instances it can be pro-fuse and difficult to control in a timely manner.

Solar et al.16 described the blood supply to the lateral wall of the maxillary sinus in cadaver specimens. It consists of the intraosseous and extraosseous branches of the posterior superior alveolar artery which form an arterial cascade with the infraorbital artery. Bleeding may occur either from the soft tissue (extraosseous branch) during flap elevation or directly from the lateral bony wall (intraosseous branch) during prepara-


Patil et al

tion of the lateral window via rotary instrumenta-tion. There is also the possibility of bleeding from the medial wall of the sinus if the posterior lateral nasal artery is damaged.17 The posterior superior alveolar, infraorbital, and posterior lateral nasal artery are all branches of the maxillary artery.

Solar16 showed the internal branch of the posterior superior alveolar artery to be pres-ent in 100% of cadaver specimens. Elian et al.18

showed that this artery can be located in the lateral wall in cross-sectional computed tomo-graphic (CT) images in 52% of sinuses. Further, in 20% of these cases, the artery is in a posi-tion in which it is likely to be cut when creating a lateral window. Once it is anticipated that the possibility of a bleeding complication exists, it is prudent to locate the position of the artery on the cross-sectional CT images and then use a window preparation method that can respect the integrity of vascular and other soft tissues while still creating the window in the ideal location for access to and elevation of the sinus membrane.

If rotary instrumentation is used, diamond burs are preferable to carbide burs as they are less likely to catch and tear the membrane. Piezo-surgery, a concept of bone surgery developed by Vercellotti and specifically adapted for sinus elevation surgery,19 provides a means of avoid-ing this complication almost entirely. Piezoelectric surgery uses low frequency ultrasonic vibrations (range of 24—32 kHz for the various systems) to perform cutting (osteotomy) and grinding (osteoplasty) procedures on bone. This low fre-quency, selective cutting action provides safety for soft tissues as it is incapable of cutting either blood vessels or the Schneiderian membrane.

Many techniques exist to control vascular bleeding in sinus elevation surgery, these include:

l Direct pressure on the bleeding pointl Use of a localized vasoconstrictorl Bone waxl Crushing the bone channel around the vessell Use of electrocautery (with care near

membranes)l Suturing of the vessel proximal to the

bleeding point.Therefore, it is some precautions

must be taken to prevent the bleed-ing from operative site which include:1. Obtain preoperative CT images to locate

the vessel2. Visualize the vessel clinically.3. Avoid the vessel when designing the window.4. Use piezoelectric surgery to avoid trauma

to the vessel.5. Have materials on hand to control bleeding

(electrocautery, local with 1:50 000 epinephrine, bone wax).

OTHER INTRAOPERATIVE COMPLICATIONS

Complications such as tears in the buccal flap and injury to the infraorbital nerve generally result from poor surgical technique. Buccal flap tears may result from attempts to release the flap to achieve primary closure. This is usually an unnec-essary procedure in a typical sinus elevation. Since there is no change in external dimensions, the flap will close tension free without release. This is more often a problem when simultaneous ridge augmentation is performed. Be aware of the possibility that the flap may be thin in the area of release and that the direction of the bone sur-face changes in the area of the malar eminence.

Blunt or pressure injury to the infraorbital nerve may result during flap retraction. If the flap

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extends superiorly to this position, the exit of the nerve from the bone should be visualized and retraction placed distal to it. It is also possible to injure this nerve during sharp dissection to release the flap for primary closure. The exit-point of the nerve from the skull is just below the infra-orbital notch. Location of this anatomic structure is crucial before performing these procedures.

POSTOPERATIVE COMPLICATIONS

Postoperative edema, ecchymosis, mild to moderate discomfort, minor nosebleed, minor bleeding at the incision line, and mild conges-tion are within the scope of expected patient responses to this procedure. Some are due to manipulation of the facial flap and others to the manipulation of the sinus membrane.

Major postoperative complications after sinus elevation surgery are relatively uncommon. They include graft infections, sinus infections, postoperative sinusitis, profuse postopera-tive bleeding, flap dehiscence, oroantral fistula formation, formation of inadequate graft vol-ume for implant placement, loss of graft mate-rial containment as a result of either sinus membrane rupture or exfoliation of graft mate-rial through the sinus window, maxillary cyst formation.20,21 migration of dental implants into the sinus graft or into the sinus cav-ity proper, and the failure of dental implants.

Zijderveld et al.7 reported an 11% incidence of membrane perforations and a 2% incidence of bleeding as intraoperative complications. The postoperative complications listed in order of most frequent occurrence were loss of implants (4%), wound dehiscence (3%), graft infections (2%), postoperative maxillary sinusitis (1%),

and loss of or inadequate graft volume (1%).The incidence of postoperative sinus

graft infections has not been separately doc-umented but, by inference, the incidence is approximately 2-5%. The most common symptoms may include tenderness, nasal obstruction, pain, swelling, fistulation, puru-lent discharge, flap dehiscence, and suppura-tion. Sinus graft infections may be caused by:l pre-existing sinus infection (should not treat

symptomatic patient)l contamination of the surgical site:- sali-

vary/bacterial contamination of the graft material, instruments, or membrane, untreated periodontal disease, adjacent periapical pathology, lapses in the chain of sterility, extended surgical time

l infected simultaneous lateral ridge augmentation procedures

LOSS OF GRAFT MATERIAL THROUGH THE WINDOW

An increase in intrasinus pressure which may be caused by postoperative inflammation or bleeding from within the sinus can result in loss of graft material through the window. This is likely to occur if a membrane was not placed over the window or if the membrane was not stabilized. The displaced graft mate-rial is likely to cause an elevation, in the buc-cal mucosa. This can be removed with a small flap entry (not over window or membrane) or left in place and addressed at the time of implant placement. Some clinicians stabi-lize bio-absorbable barrier membranes with resorbable tacks or a mattress suture. The incidence of this complication is so low that this may be considered unnecessary therapy


Patil et al

INFECTIONThe following recommendations are given as measures to reduce the inci-dence of postoperative infection:1. Proper case selection.2. Use proper prophylactic antibiotics.3. Use chlorhexidine and/or betadine prepara-

tion of the mouth and face for surgery.

4. Use sterile draping with an infection control protocol.

5. Periodontal and endodontic problems should be attended to before surgery.

6. Keep incision lines distant from window and barrier membrane.

7. Prevent contamination of graft and barrier membrane with saliva.

8. Ensure the sterility of all instruments being used.

9. Keep the surgical time as short as possible.10. Use postoperative chlorhexidine rinses.

CONCLUSIONMaxillary sinus augmentation procedures are getting worldwide acceptance for plac-ing the dental implant with sufficient length. Still large gap exist between the research-ers and clinicians that how much amount of grafting material is required to augment the maxillary sinus. Pre-selection of suitable can-didates for maxillary sinus augmentation will undoubtedly help reduce the incidence rate. The surgeon must be aware of the various intraoperative and postoperative complica-tions that may occur and their management. l

Correspondence:Dr. Pranav S. Patil, Sharad Pawar Dental CollegeSawangi (M), Wardha – 442005Maharastra (INDIA)Phone numbers – 9420349157E-mail address – [email protected]

DisclosureThe authors report no conflicts of interest with anything in this article.

References1. Aghaloo TL, Moy PK. Which hard tissue augmentation techniques are the

most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants 2007; 22 (Suppl): 49-70.

2. Wallace SS, Froum SJ. Effect of maxifiary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol 2003; 8: 328-43.

3. Del Fabbro M, Testori T, Francetti L, Weinstein R. Systematic review of survival for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent 2004; 24: 565-77.

4. Ziccardi VB, Betts NJ. Complications of maxillary sinus augmentation. In: Jensen OT, ed. The sinus bone graft. Chicago, IL: Quintessence, 1999: 201-8.

5. Misch CE. Contemporary implant dentistry, 3rd edn. St Louis, MO: Mosby, 2008: 905-74.

6. Pikos MA. In: Jensen OT, ed. The sinus bone graft, 2nd ed. Chicago, IL: Quintessence, 2006: 103-14.

7. Zijderveld SA, van den Bergh, JPA, Schulten EAJM, ten Bruggenkate CM. Anatomical and surgical findings and complications in 100 consecutive maxillary sinus floor elevations. J Oral Maxillofac Surg 2008; 66: 1426-38.

8. Schwartz-Arad D, Herzberg R, Dolev E. The prevalence of surgical complications of the sinus graft procedure and their impact on implant survival. J Periodontal 2004; 75: 511-16.

9. Krekmanov L. A modified method of simultaneous bone grafting and placement of implants in the severely resorbed maxilla. Int ] Oral Maxillofac Implants 1995; 10: 682-8.

10. Kasabah S, Krug J, Simunek A, Lecaro MC. Can we predict maxillary sinus mucosa perforation? Acta Med 2003; 46: 19-23.

11. Cho S-C, Wallace SS, Froum SJ, Tarnow DP. Influence of anatomy on Schneiderian membrane perforations during sinus elevation surgery: three-dimensional analysis. Pract Proced Aesthet Dent 2001; 13: 160-3.

12. Betts MJ, Miloro M. Modification of the sinus lift procedure for septa in the maxillary antrum. ] Oral Maxillofac Surg 1994; 52: 332-3.

13. Wallace SS, Mazor Z, Froum SJ, Cho SC, Tarnow DP. Schneiderian membrane perforation rate during sinus elevation using Piezosurgery: clinical results of 100 consecutive cases. Int J Periodontics Restorative Dent 2007; 27: 413-19.

14. Blus C, Szmukler-Moncler S, Salama M, Salama H, Garber D. Sinus bone grafting procedures using ultrasonic bone surgery: 5-year experience. Int J Periodontics Restorative Dent 2008; 28: 221-9.

15. Toscano NJ, Holtzclaw D, Rosen PS. The effect of piezoelectric use on open sinus lift perforation: A retrospective evaluation of 56 consecutively treated cases from private practices. J Periodontol 2010; 81: 167-71.

16. Solar P, Geyerhofer U, Traxler H, Windish A, Ulm C, Watzak G. Blood supply to the maxillary sinus relevant to sinus floor elevation procedures. Clin Oral Implants Res 1999; 10: 34-14.

17. Flanagan D. Arterial supply of maxillary sinus and potential for bleeding complication during lateral approach sinus elevation. Implant Dent 2005; 14: 336-8

18. Elian N, Wallace S, Cho SC, Jalbout ZN, Froum S. Distribution of the maxillary artery as it relates to sinus floor augmentation. Int J Oral Maxillofac Implants 2005; 20: 784-7.

19. Vercellotti T, De Paoli S, Nevins M. The piezoelectric bony window osteotomy and sinus membrane elevation: introduction of a new technique for simplification of the sinus augmentation procedure. Int J Periodontics Restorative Dent 2001; 21: 561-7.

20. Misch CM, Misch CE, Resnik RR, Ismael YH, Appel B. Postoperative maxillary cyst associated with a maxillary sinus elevation procedure: a case report. ] Oral Implantol 1991; 17: 432-7.

21. Lockhart R, Ceccaidi J, Bertrand JC. Postoperative maxillary cyst following sinus bone graft: report of a case. Int J Oral Maxillofac Implants 2000; 15: 583-6.

Patil et al

Treatment of the posterior edentulous maxilla can be complicated by atrophy of the eden-tulous ridge or by an aging-related increase

in the pneumatization of the maxillary sinus. The technique of sinus floor elevation has expanded the prosthetic rehabilitation options for this region through the placement of dental implants.

However, this technique can be quite aggres-sive and often patients would prefer an option that stresses minimalism. A less invasive alter-native to the lateral window approach for sinus elevation was introduced by Summers in 1994. This review article illustrates the complications associated with the crestal i.e. indirect sinus lift.

Sinus Augmentation Complications: Part-II Associated with Crestal Technique

(Indirect Approach): A Review

Dr. Pranav S Patil1 • Dr. M. L. Bhongade2

1. Post graduate student, Department of Periodontology & Implantology, Sharad Pawar Dental College and Hospital, Sawangi, Wardha, Maharashtra, India

2. Professor and Head, Department of Periodontology & Implantology, Sharad Pawar Dental College and Hospital, Sawangi, Wardha, Maharashtra, India

Abstract

KEY WORDS: Schneiderian membrane, sinus infection, sinusitis, vertigo, dental implants

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INTRODUCTIONCrestal (indirect) technique for maxillary sinus aug-mentation, also known as bone-added osteotome sinus floor elevation (BAOSFE), proposes that a bone replacement graft be used simultaneous to the placement of the dental implant. The BAOSFE procedure attempts to augment the existing crestal bone under the sinus with graft materials, elevating the sinus floor and increasing osseous support for an implant. The combined mass of the native bone with the bone replacement graft material acts like a hydraulic plug to elevate the sinus floor. Implants are placed after the tenting of the sinus membrane with their apical end fur-ther facilitating the elevation of the sinus mem-brane. Implant stability initially relies on the host bone present at the created osteotomy site, while future additional support is potentially gained by the consolidation and amalgamation of the grafted material with newly formed host bone. Several case series reports1-5 attest to the success of this procedure, furthering its popularity among clini-cians. Nedir et al.6 demonstrated that a success rate of better than 90% can be achieved with this procedure in sinuses where preoperative bone height averaged approximately 5.5 mm (range 6-9 mm) without the use ofa bone replacement graft.

Similarly to any other procedure, BAOSFE has received innovative modifications7 in an effort to achieve greater simplicity or greater success with reduced complications. Some of these modifications have included using medi-cal devices and instruments that are specific to their particular technique.8 Although these tech-niques have all demonstrated high rates of suc-cess, insufficient evidence exists in the form of prospective studies to validate their inclusion

in clinical practice. Therefore, techniques such as localized management of the sinus floor,9-

10 hydraulic sinus lift,11 minimally invasive antral membrane balloon elevation (MIAMBE)12-13 and several others are not included in this review.

DETERMINING THE INCIDENCE OF COMPLICATIONS ASSOCIATED WITH

CRESTAL TECHNIQUEOne must first look at implant failures with BAOSFE. However, most studies and case reports have focused on successful outcomes. When evaluating the body of literature regard-ing BAOSFE, meta-analysis is the most dispas-sionate and extensive way to gain this clinically valuable information. In 2005, Emmerich et al.14 published the first meta-analysis report that strictly reviewed the use of osteotomes for sinus floor elevation. Their analysis revealed over 44 articles for evaluation, of which eight15-21 met their rigor-ous inclusion criteria. All of these studies did not include criteria for success, so survival rate was calculated with a minimum of 6 months of load-ing. In total, 1,139 implants were appropriate for meta-analysis and the percentage of implants

lost was 1.8%, 2.5%, 4.3%, and 9.1%, after 6, 12, 24, and 36 months respectively. Emmerich14 enumerates some of the complicating factors that may have caused the implants to fail that include lack of primary stability, type IV bone qual-ity, and occlusal traumatic forces from either a partial denture or parafunction. The most consis-tent fact about implant failures associated with BAOSFE is that they usually occur before loading.

A second meta-analysis on osteotome use was published by Shalabi et al.22 These authors

estimated the 4.5-year survival rate of implants


16 • Vol. 8, No. 7 • November 2016

that were placed using the osteotome tech-nique. Their inclusion criteria were different from the former meta-analysis.14 Shalabi et al.22 in their literature search, revealed five studies23-24 for inclusion of the 164 that were reviewed. The combined data of 349 implants revealed a failure probability of 2% before loading and 1% after 56 months of loading. At the end of the observation period, 41 implants in 18 patients were still at risk.

One additional prospective study, by Ferri-gno et al.25 was published since the time of these two meta analyses and should also be men-tioned. The 12-year cumulative loss rate based on their calculation of implant survival was 5.2%, which is slightly better than Emmerich,14 but well within the grouping of all of the included studies.

A third meta-analysis was published in 2008 by Tan et al.26 on transalveolar sinus elevation, which they termed an osteotome technique. This exhaustive literature search identified 19 studies which met the authors' inclusion cri-teria, of which ten studies reported on com-plications. The authors noted that these ten articles included a total of 1,776 implants and the most commonly reported complication was sinus perforation. Only eight of these ten stud-ies reported on this. There were a total of 1,621 implants from these studies with 61 membrane perforations noted, for an overall rate of 3.8% (range 0-21.4%). The most common postopera-tive complication was infection; only six of the studies reported on this. There were a total of 884 implants from these studies of which seven had infections, a rate of 0.8% (range 0-2.5%). Other complications found in this meta-analy-sis included postoperative hemorrhage, nasal bleeding, blocked nose, hematomas, and cover screw loosening that resulted in suppuration.

ETIOLOGY INFECTIONFirst and foremost among the list of etiologies for possible complications is infection. Site infec-tion may be related to poor oral hygiene, con-tamination of the implant surface at the time of insertion, or graft material contamination, or may be due to the sinus having underly-ing disease, particularly if a sinus membrane perforation were to occur during elevation of the sinus. Such events could lead to failure of the implant owing to a lack of osseointegra-tion or the development of peri-implantitis.

When performing BAOSFE strong con-sideration should be given to minimizing the bacterial load at the time of the surgery. Any active periodontal disease or endodontic infection, particularly in the area of the pro-cedure, should be addressed before pro-ceeding. The use of pre-surgical antiseptic rinses and systemic administration of antibi-otics will further decrease potential patho-genic bacteria. The same consideration might be given to using postsurgical antibiot-ics and an antiseptic mouth rinse to reduce the complication of postoperative infection.

Inadequate Primary Stability Related to Pre-treatment Bone Height/WidthImplant success and survival with BAOSFE rely on good primary stability of the implant at the time of placement. There can be several reasons why the implant is not well stabilized. Having enough vertical bone height, before place-ment with the BAOSFE procedure, appears to impact stability and implant success.5,15 Rosen et al.15 and Toffler5 provided case series data that demonstrated an almost 10-20% increase in failures when the subantral bone measured

Patil et al


4 mm or less at the time of implant placement. A narrower ridge width with diminished bone height below the sinus may also have a nega-tive impact on success since tapping the osteo-tomes in denser bone may cause the site to become overprepared, causing the implant to be placed without adequate primary stability.

Good primary stability for the implant can be achieved when elevating the sinus floor with osteotomes. Consideration might be given to selecting a tapered implant for use versus one with a straight-wall design. The taper of the implant will give some added stability related to the wedging that occurs when inserting this par-ticular design. A rough-surfaced implant is rec-ommended since it will aid in gaining optimal primary stability.27 Several authors5,15 have empha-sized the need for at least 5 mm of vertical bone height beneath the sinus wall at the site before surgery to ensure a higher chance of success.

Inadequate Primary Stability Related to Bone QualityHistorically, implant failures have increased par-ticularly when bone has been of type IV quality.28

Some clinicians feel that the use of osteotomes may condense the bone, thereby modifying type IV bone to type II or type III.29 This compression of the bed may increase the bone-to implant contact and allow for better stability and integra-tion. In situations where poorer bone quality is encountered, greater use of the osteotome might be considered versus drilling of the site with the hope that compression of the bed will lead to denser bone and greater implant stability. An alter-native to this might be to underprepare the site with the drill and use a substantially larger diam-eter implant to facilitate better primary stability.

Inadequate Primary Stability Related to Site PreparationOverpreparation of the site with BAOSFE is a concern when creating the osteotomy with the mallets. Biichter and colleagues30 dem-onstrated in an ex-vivo model significantly higher removal torque values for implants placed with a conventional technique com-pared to those with the osteotome. This find-ing of diminished primary stability has been further corroborated in vivo where at 28 days removal torque again was higher for conven-tional versus osteotome implant placement.31-32

Underpreparation can also be of con-cern. If the site were to be underprepared, irreversible damage might occur from exces-sive compression during implant placement with fracture of the bony trabeculae and poor recovery of vital bone. Without adequate sta-bility of the implant, there is a potential risk for migration of the implant into the sinus.14

Sinus Membrane Tears Related to Excessive Tapping, Anatomy, or Overzealous ElevationThe complication of a sinus membrane tear is more common than one might believe. Signs of membrane tear can be the develop-ment of sinusitis, epistaxis, or exfoliation of graft particles from the nose. Development of a sinus tear during BAOSFE is not always apparent and sometimes must be deter-mined by the Valsalva maneuver or more accu-rately by inspection with an endoscope8.Theincidence of membrane perforations ranges from 4 to 25% of osteotome cases.33

In reality, microscopic tears are, in many instances, impossible to diagnose and therefore their incidence is often underes-

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18 • Vol. 8, No. 7 • November 2016

timated. Causes for tearing of the mem-brane can be related to inserting the osteotome beyond the sinus border.34

This unfortunate occurrence can be related to difficulty in initial in-fracturing of the sinus floor. One possible cause for this could be angulation of the sinus floor at the site of preparation leading to dis-similar heights in the area where the osteo-tome encounters the inferior sinus wall.

Trying to elevate the Schneiderian mem-brane beyond its capacity to adapt can also cause the sinus membrane to tear. Pommer et al.35 reported from a human cadaver study that there was a limit to how far the sinus mem-brane could be stretched and that thicker mem-branes demonstrated significantly higher load limits. The clinician is constantly challenged in determining what a reasonable elevation of the membrane is since a wide variation has been reported. Komarnyckyj and London36 reported a range of 3-9 mm (average 5.4 mm), while Bau-mann and Ewers37 reported that 13 mm of eleva-tion was achieved in one case. These disparate differences make it difficult to determine what a reasonable goal is for a given individual who is to undergo osteotome sinus floor elevation.

Other possible causes for membrane tears may include the sharp nature of some of the particulate graft materials placed into the oste-otomy or too rapid elevation of the membrane. Another concern with sinus membrane perfo-ration is potential for the tear to lead to a pat-ent oral-antral communication. This would be more common in a patient with underlying sinus disease, which could diminish the pos-sibility for healing of a sinus membrane tear.

Osteotome Use Leading to Benign Paroxysmal Positional Vertigo or Poor Patient ExperienceIncidents of significant headache, labyrinthitis and, more recently, benign paroxysmal positional vertigo (BPPV) have been reported following the use of the osteotome for both internal sinus floor elevation38,39 and ridge widening.40,41 Symptoms of BPPV include dizziness or vertigo, imbalance, lightheadedness, and nausea. These symptoms are almost always caused by a change in the posi-tion of the head with respect to gravity. BPPV is not progressive, will occur suddenly and unpre-dictably, and can be temporarily incapacitating. Di Girolamo et al.39 postulated that the surgi-cal trauma, particularly the pressure exerted by the osteotomes, may cause the detachment of the otoliths known as otoconia from the utricular macula. These calcium carbonate crystals, while floating in the inner ear fluid, could strike against sensitive nerve endings within the balance appa-ratus at the end of each semicircular canal, cre-ating the position- or motion-induced vertigo. The patient's head position, hyperextended and tilted opposite to the side from where the opera-tor is working, favors the entry of these free-floating particles into the posterior semicircular canal of the implanted side. While in the major-ity of cases of BPPV the etiology is unknown, it may follow viral infection, vascular disorders, and head trauma. It is believed that BPPV may account for 50% of all dizziness in older indi-viduals.42 BPPV is self-limiting and symptoms subside or disappear within 6 months of onset.

Poor patient experience related to the mal-leting involved with the osteotome is the great-est single complaint of this procedure. Diserens and colleagues43 compared the responses of

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55 patients who had undergone sinus eleva-tion with the Summers osteotome technique34 to a group of patients who received implants in the same location during the same period using standard implant placement. A visual analogue score was used to help gauge patient responses. The groups did not differ in their perception of pain; however, the osteotome group judged the procedure more negatively. The biggest con-cern centered around the tapping, during which some patients expressed that they had experi-enced strong sensations and discomfort. How-ever, pain itself was not the primary complaint.

CONCLUSIONWhen preparing to treat a patient with an osteo-tome approach to sinus elevation, there should be a minimum of 5 mm of bone beneath the sinus. The (2X - 2) rule,44 where ‘X’ is the dimension of bone beneath the sinus, should be used when determining what is a reasonable goal for sinus elevation. The site should initially be prepared just short of the sinus wall with an implant hand piece. Radiographic verification of this should be performed using a radiopaque calibrated measur-ing device inserted into the osteotomy. The oste-otomy should be undersized since the use of the osteotomes may widen the site, thereby reduc-ing the primary stability of the implant when it is placed. A piezoelectric hand piece with a round diamond ball should be considered to in-fracture the wall of the sinus initially. The advantage of this approach is avoiding the malleting that creates many of the adverse sequelae, while the piezo-electric tip helps to reduce the likelihood of tear-ing the membrane. Before placing the graft into the osteotomy, a collagen membrane/plug should be inserted into the osteotomy as Cavicchia et

al.45 recommended. This may help to avoid a per-foration preventing graft exfoliation and loss. If the amount of sinus lift may be less than 2 mm, consideration should be given to using the col-lagen alone without a graft. To avoid sinus perfo-ration, the osteotomes should not be tapped or advanced beyond the length of the final drill. Make sure that no loading forces are placed on the implant at the time of placement. Any provisional appliances should be checked in function to avoid loss of the implant owing to premature loading. l

Correspondence:

Dr. Pranav S. Patil,

Sharad Pawar Dental College

Sawangi (M), Wardha – 442005

Maharastra (INDIA)

Phone numbers – 9420349157

E-mail address – [email protected]

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20 • Vol. 8, No. 7 • November 2016


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3. Leonetti JA, Rambo HM, Throndson RR. Osteotome sinus elevation and implant placement with narrow size bioactive glass. Implant Dent 2000; 9: 177-82.

4. Saadoun AP, Le Gall MG. Implant site preparation with osteotomes: principles and clinical application. Pract Periodontics Aesthet Dent 1996; 8: 453-63.

5. Toffler M. Osteotome-mediated sinus floor elevation: a clinical report. Int J Oral Maxillofac Implants 2004; 19: 266-73.

6. Nedir R, Bischof M, Vazquez L, Szmukler-Moncler S,Bernard J-P. Osteotome sinus floor elevation without grafting material: a 1-year prospective pilot study with ITI Implants. Clin Oral Implant Res 2006; 17: 679-86

7. Li TF. Sinus floor elevation: a revised osteotome technique and its biological concept. Compend Contin Educ Dent 2005;26: 619-30.

8. Nkenke E, Schlebel A, Schultze-Mosgau S, Neukam FW, Wiltfang J. The endoscopically controlled osteotome sinus floor elevation: a preliminary prospective study. Int J OralMaxillofac Implants 2002; 17: 557-66.

9. Bruschi GB, Scipioni A, Calesini G. Bruschi E. Localized management of sinus floor with simultaneous implant placement: a clinical report. Int J Oral Maxillofac Implants1998; 13: 219-26.

10. Winter AA, Pollack AS, Odrich RB. Placement of implants inthe severely atrophic posterior maxilla using localized management of the sinus floor: a preliminary study. Int ] Oral Maxillofac Implants 2002; 17: 687-95.

11. Chen L, Cha J. Minimally invasive hydraulic sinus condensing technique. / Periodontal 2005; 76: 482-91.

12. Kfir E, Kfir V, Mijiritsky E, Rafaeloff R, Kaluski E. Minimally invasive antral membrane balloon elevation followed by maxillary bone augmentation and implant fixation. / Oral Implantol 2006; 32: 26-33.

13. Kfir E, Kfir V, Eliav E, Kaluski E. Minimally invasive antral membrane balloon elevation: report of 36 procedures./ Periodontal 2007; 78: 2032-5.

14. Emmerich D, Att W, Stappert C. Sinus floor elevation using osteotomes: a systematic review and meta-analysis. J Periodontal 2005; 76:1237-51.

15. Rosen PS, Summers R, Mellado JR, Salkin LM, ShanamanRH, Marks MH, Fugazzotto PA. The bone-added osteotomesinus floor elevation technique: multi-center retrospective report of consecutively treated patients. Int J Oral Maxillofac Implants 1999; 14: 853-8.

16. Coatoam GW, Krieger JT. A four-year study examining the results of indirect sinus augmentation procedures. J Oral Implant 1997; 23: 117-27.

17. Deporter D, Todescan R, Caudry S. Simplifying management of the posterior maxilla using short, porous-surfaced dental implants and simultaneous indirect sinus elevation. Int ] Periodontics Restorative Dent 2000; 20: 476-85.

18. Cavicchia F, Bravi F, Petrelli G. Localized augmentation of the maxillary sinus floor through a coronal approach for the placement of implants. Int J Periodontics Restorative Dent2001; 21: 475-85.

19. Fugazzotto PA, De Paoli S. Sinus floor augmentation at the time of maxillary molar extraction: success and failure rates of 137 implants in function for up to 3 years. J Periodontol 2002; 73: 39-44.

20. Fugazzotto PA. Immediate implant placement following a modified trephine/osteotome approach: success rates of 116implants to 4 years in function. Int J Oral Maxillofac Implants 2002; 17: 113-20.

21. Zitzmann NU, Schaerer P. Sinus elevation procedures inthe resorbed posterior maxilla. Comparison of the crestal and lateral approaches. Oral Surg Oral Med Oral Pathol OralRadiol Endod 1998; 85: 8-17.

22. Shalabi MM, Manders P, Mulder J, Jansen JA, Creugers NH.A meta-analysis of clinical studies to estimate the 4.5-yearsurvival rate of implants placed with the osteotome technique. Int J Oral Maxillofac Implants 2007; 22:110-16.

23. Rodoni LR, Glauser R, Feloutzis A, Hammerle CH. Implants in the posterior maxilla: a comparative clinical and radiologic study. Int J Oral Maxillofac Implants 2005; 20: 231-7.

24. Strietzel FP, Nowak M, Kuchler I, Friedmann A. Periimplantalveolar bone loss with respect to bone quality after use of the osteotome technique: results of a retrospective study. Clin Oral Implants Res 2002; 13: 508-13

25. Ferrigno N, Laureti M, Fanali S. Dental implants placement in conjunction with osteotome sinus floor elevation: a 12-year life-table analysis from a prospective study on 588 ITI implants. Clin Oral Implant Res 2006; 17:194-205

26. Tan WC, Lang NIP, Zwahlen M, Pjetursson BE. A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontal 2008; 35: 241-54.

27. Shalabi MM, Wolke JGC, Jansen JA. The effects of implant surface roughness and surgical technique on implant fixation in an in vitro model. Clin Oral Implants Res 2006; 17:172-8

28. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. / Periodontal 1991;62: 2-4.

29. Hahn J. Clinical uses of osteotomes. J Oral Implantol 1999; 25:23-9.

30. Biichter A, Kleinheinz J, loos U, Meyer U. Primary implant stability with different bone surgery techniques. An in-vitro study of the mandible of the minipig. Mund Kiefer Gesichtshir 2003; 7: 351-5

31. Biichter A, Kleinheinz J, Wiesmann HP, Jayaranan M, JoosU, Meter U. Interface reaction at dental implants inserted in condensed bone. Clin Oral Implants Res 2005; 16: 509-17.

32. Biichter A, Kleinheinz J, Wiesmann HP, Kersken J,Nienkemper M, von Weyhrother H, et al. Biological and biomechanical evaluation of bone remodeling and implant stability after using an osteotome technique. Clin Oral Implants Res 2005; 16: 1-8.

33. Reiser GM, Rabinowitz Z, Bruno J, Damoulis PD, Griffin TJ. Evaluation of the maxillary sinus membrane response following elevation with the crestal osteotome technique inhuman cadavers. Int J Oral Maxillofac Implants 2001; 16:833.

34. Summers RB. The osteotome technique: Part 3: Less invasive methods of elevating the sinus floor. Compend Contin Educ Dent 1994; 15: 698-708.

35. Pommer B, Unger, Siito D, Hack, Watzek G. Mechanical properties of the Schneiderian membrane in vitro. Clin OralImplant Res 2009; 20: 633-7.

36. Komarnyckyj OG, London RM. Osteotome single-stage dental implant placement with and without sinus elevation:a clinical report. Int J Oral Maxillofac Implants 1998; 13:799-804

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37. Baumann A, Ewers R. Minimally invasive sinus lift. Limits and possibilities in the atrophic maxilla. Mund KieferGesichtschir 1999; 3 (Suppl 1): S70-3.

38. Saker M, Ogle O. Benign paroxysmal positional vertigo subsequent to sinus lift via closed technique. / Oral Maxillofac Surg 2005; 63: 1385-17.

39. Di Girolamo M, Napolitano B, Arullani CA, Bruno E, DiGirolamo S. Paroxysmal positional vertigo as a complication of osteotome sinus floor elevation. Eur Arch Otorihnolaryngol2005; 262: 631-3.

40. Perez-Garrigues H, Mateos Fernandez M, Penarrocha M.Benign paroxysmal positional vertigo secondary to surgicalmaneuvers on superior maxilla. Acta Otorrinolaringo Esp2001; 52: 343-6.

41. Penarrocha-Diago M, Rambia-Ferrer J, Perez V, Perez-Garrigues H. Benign paroxysmal positional vertigo secondary to placement of maxillary implants using the alveolar expansion technique with osteotomes: a study of 4 cases. Int J Oral Maxillofac Implants 2008; 23: 129-32.

42. Oghalai JS, Mandolidis S, Barth JL, Stewart MG, Jenkins HA. Unrecognized benign paroxysmal positional vertigo in elderly patients. Otolaryngol Head Neck Surg 2000; 122:630-4.

43. Diserens V, Merickse E, Schappi P, Mericske-Stern R.Transcrestal sinus floor elevation: report of a case series. Int J Periodontics Restorative Dent 2006; 26: 151-9.

44. Yamada JM, Park HJ. Internal sinus manipulation (ISM) procedure: a technical report. Clin Implant Dent Relat Res2007; 9: 128-35.

45. Cavicchia F, Bravi F, Petrelli G. Localized augmentation ofthe maxillary sinus floor through a coronal approach for the placement of implants. Int J Periodontics Restorative Dent 2001; 21: 475-85.

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Patil et al

Ruvins et al

Background: This study was designed to pro-vide a histomorphometric evaluation of newly formed bone after bilateral concurrent maxil-lary sinus augmentation completed with two dis-tinctly different biomaterials. Allograft (AlloOssTM) and Xenograft (NuOss XC SinusTM Bone Composite) were used for maxillary sinus floor augmentation in a split-mouth design study.

Materials and Methods: Three partially eden-tulous and two fully edentulous patients requiring bilateral sinus augmentation were selected for this study. The patients were informed of the objec-tives of the study. Simultaneous bilateral sinus augmentations were completed on five subjects with utilization of a buccal open window approach. Six months after grafting core bone specimens were obtained from the recipient sites prior to den-tal implant placement. Core specimens were pre-served in Formalin, prepared into cytology blocks and underwent histomorphometric analyses.

Results: A histomorphometric analysis deter-mined presence of good regenerative results in both groups. Presence of vital bone in the spec-imens was observed on the average of 97% (by the area of examination). Structural composition of the specimens indicated that on average 45% of the area observed under the microscope was filled with newly formed bone. Clinical analysis of the pre-augmentation and post-augmentation measurements established that in all augmented sites a consistent and statistically measurable increase of the bone structure was achieved. No clinical failures of the grafts were observed bringing the success rate of the study to 100%. Conclusion: This analysis demonstrated close quantitative similarities of histologic composition between newly formed bone specimens obtained after maxillary sinus aug-mentation regardless of the biomaterial used.

Histologic Analysis of the Outcomes of Split-Mouth Maxillary Sinus Augmentation with Allograft and Xenograft Grafting Mediums

Edward Ruvins, DDS, MS, MBA, MSF1 • Mark Stein, DDS, MD2

Susanna Kayserman, DDS3

1. Spectrum Dental Group, Private Practice, Denver, Colorado2. Board Certified Oral & Maxillofacial Surgeon, Private Practice, New York City, New York

3. Private Practice, Warren, New Jersey

Abstract

KEY WORDS: Maxillary sinus augmentation, allograft, xenograft, histology

22 • Vol. 8, No. 7 • November 2016

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INTRODUCTIONSurgical placement of implant fixtures in the pos-terior maxilla is frequently associated with dif-ficulties in the management of enlarged maxillary sinuses. The success of the surgical manage-ment of the osseous maxillary deficiency was traditionally achieved by effective and predict-able maxillary sinus augmentation procedures. The search for the optimal grafting medium to maintain the space formed after elevation of the Schneiderian membrane consumed interests of many clinicians dedicating their clinical skills and resources to the search for an “ideal” graft-ing material. Clinical protocol makes it difficult to obtain any samples of a newly formed osse-ous tissue after the healing process takes place. As a result, overwhelming studies relied on the radiographic evidence of new bone formation to assess the success of the sinus augmentation. This split-mouth study was designed to provide an objective assessment of the histological com-position of the newly formed bone tissue and compare outcomes of traditional sinus augmen-

tation procedure completed with two distinctively different bone grafting materials completed with utilization of identical surgical technique. Lastly, this research was designed to assess the vital-ity of the newly formed osseous tissue formed in the opposite recipient sites after completion of the augmentation with different grafting mediums.

MATERIALS AND METHODSThis split-mouth study included five edentulous patients (three partially and two fully) diagnosed with maxillary alveolar ridge deficiency caused by enlarged maxillary sinus impeding adequate implant placement. Four female and one male subjects were included in this study; the average age of the subject was 43. All patients required bilateral sinus augmentation to subsequently facili-tate placement of dental implants replacing teeth #3 and #14. The patients were selected and agreed to bilateral and concurrent maxillary sinus augmentation with two distinctly different bioma-terials. Bilateral maxillary sinus augmentation was completed on each subject concurrently. An open

Figure 1a: Open Window Access into the Maxillary Sinus (Right).

Figure 1b: Open Window Access into the Maxillary Sinus (Left).

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24 • Vol. 8, No. 7 • November 2016

window approach was utilized to obtain a surgical access to the recipient site Figure 1. Right max-illary sinus of each subject was grafted with an allograft (Figure 2), subsequently the left maxillary sinus of each subject was grafted with a compos-ite xenograft graft (Figure 3). None of the surgical sites had a history of previous bone augmentation. No implant fixtures were placed concurrently with the augmentation procedure. All selected patients

were informed on the nature of the study, pre-sented with alternatives and had consented to the treatment and postoperative follow up protocol.

Six-month post-augmentation, a CBCT scan was taken to evaluate the healing of the sinus augmentation and plan the implant surgery. Then endosseous implants were placed in the first maxillary molar sites on the left and the right side of each study participant. These sites cor-

Figure 2a: Post graft placement; Allograft. Figure 2b: Post graft placement; Xenograft.

Figure 3a: Fixation of Resorbable Collagen Barrier Membrane on the Right.

Figure 3b: Fixation of Resorbable Collagen Barrier Membrane on the Left.

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responded directly to the recipient sites of the earlier augmentation. After surgical site prepa-ration a 2mm inside diameter and 2.8mm out-side diameter head trephine bur was used to extract cylindrical bone core specimens for his-tological analysis. All osteotomies and all implant fixtures were placed with flapless approach.

Extracted specimens were preserved in 10% Formaldehyde (Formalin) solution to fix the tis-

sue for preparation of cytology cell blocks. Specimens were prepared with utilization of Donath technique with subsequent histomor-phometric analysis. Analysis was completed by the Hard Tissue Research Laboratory at The University of Minnesota School of Dentistry.

The following bone grafting materials were used in this study: 1) AlloOss™. AlloOss is a par-ticulate mineralized human bone allograft material.

Figure 4a: Preoperative CT Scan; (Subject A). Figure 4b: Postoperative CT Scan (6 Month Postaugmentation); (Subject A).

Figure 5a: Preoperative CT Scan; (Subject B). Figure 5b: Postoperative CT Scan (6 Month Postaugmentation); (Subject B).

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26 • Vol. 8, No. 7 • November 2016

Figure 6a: Preoperative CT Scan of Allograft Site. (Subject A).

Figure 6b: Postoperative CT Scan of Allograft Site. (Subject A).

Figure 7a: Preoperative CT Scan of Xenograft Site. (Subject B).

Figure 7b: Postoperative CT Scan of Xenograft Site (6 Month Postaugmentation). (Subject B).

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Large size (1000-2000 mic.) particles of this can-cellous bone particulate were used for the graft-ing of the right maxillary sinus of each subject; 2) NuOss XC SinusTM. NuOss is an expanding com-posite material comprised of mineralized de-pro-teinated bovine granules and purified type I bovine collagen. When placed into a bleeding recipi-ent site, NuOss, activated by contact with blood, expands to fill an available recipient space to the

extent of the material dimensions. NuOss is avail-able in both socket and sinus forms. Sinus form material was used for this study utilized for the grafting of the left maxillary sinus of each subject.

RESULTSDuring the course of the study ten specimens (five of each allograft and xenograft) were obtained. Subsequently, ten cytology blocks prepared out

Figure 8: Evidence of Osteoblastic Activity Adjacent to the Allograft Particles. Lower Magnification.

Figure 9: Evidence of Osteoblastic Activity Adjacent to the Allograft Particle. Higher Magnification.

Figure 10: Evidence of Osteoblastic Activity in Xenograft Specimen. Lower Magnification.

Figure 11: Evidence of Osteoblastic Activity in Xenograft Specimen. Higher magnification.

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28 • Vol. 8, No. 7 • November 2016

of ten specimens collected in the course of the study underwent a histomorphometric analysis. No clinical complications or failures of the grafts were observed bringing the success rate of the study to 100%. This analysis demonstrated closely related outcomes of the bone regenera-tion completed bilaterally and concurrently as a part of the sinus augmentation procedure. The results of the analysis were summarized and pre-sented in the Tables 1 and 2. Presence of vital

bone in the specimens was observed on the aver-age of 97% (by the area of examination) of the total sample leaving 3% to the non-vital bone. Seven out of ten specimens were composed of 100% vital bone (as a percent of the speci-men). Out of seven specimens four were grafted with xenograft vs. three with allograft medium.

Structural composition of the specimens indicated that the average of 45% (by the area observed under the microscope) of the speci-

Fibrous Tissue Non Bone Non Vital Total Area Vital Bone Non Vital Bone or Marrow as a Percent Vital Bone as Bone as a Specimen Graft of the Area of the Area of the -Percent of the of the a Percent of the Percent of ID Site Speciment Specimen Specimen Specimen Specimen of the Specimen Specimen

1 24/13-01 #3 345417 202783 0 41 0 100 0

2 24/13-02 #14 191762 117110 0 39 0 100 0

3 24/13-03 #3 883119 400920 0 54 1 100 0

4 24/13-04 #14 778471 390858 41493 44 1 90 10

5 6/13/2001 #3 524993 142870 24740 53 15 85 15

6 6/13/2002 #14 267037 83325 0 63 6 100 0

7 26/13-01 #3 303833 88410 0 68 3 100 10

8 26/13-02 #14 660107 291136 0 56 0 100 0

9 26/13-03 #3 675221 299712 17036 51 2 95 5

10 26/13-04 #14 1249338 587893 0 53 0 100 00

Table 1: The Summary of the Histomorphometric Analysis

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Fibrous Tissue Non Bone Non Vital Total Area Vital Bone Non Vital Bone or Marrow as a Percent Vital Bone as Bone as a Specimen Graft of the Area of the Area of the -Percent of the of the a Percent of the Percent of ID Site Speciment Specimen Specimen Specimen Specimen of the Specimen Specimen

1 24/13-01 #3 345417 202783 0 41 0 100 0

2 24/13-02 #14 191762 117110 0 39 0 100 0

3 24/13-03 #3 883119 400920 0 54 1 100 0

4 24/13-04 #14 778471 390858 41493 44 1 90 10

5 6/13/2001 #3 524993 142870 24740 53 15 85 15

6 6/13/2002 #14 267037 83325 0 63 6 100 0

7 26/13-01 #3 303833 88410 0 68 3 100 10

8 26/13-02 #14 660107 291136 0 56 0 100 0

9 26/13-03 #3 675221 299712 17036 51 2 95 5

10 26/13-04 #14 1249338 587893 0 53 0 100 00

Table 1: The Summary of the Histomorphometric Analysis

mens was filled with newly formed bone. While the average of 42.4% was observed in the Allograft specimens, the average of 47.8% was seen in the Xenograft specimens. A simi-lar trend was observed upon observation and analysis of the vital bone within the samples.

While the average of 97.0% (by the area observed under the microscope) of newly formed bone was vital, the average of 96.0% was observed in the Allograft specimens, the aver-

age of 98.0% was seen in the Xenograft speci-mens. The highest percentage of non-vital bone observed was 15 % in the Allograft specimen fol-lowed by 10.0% in the Xenograft specimen. The average of 4.0% (by the area) of non-vital bone was observed in the Allograft samples and this was contrasted by 2.0% of vial bone (by the area) observed in Xenograft samples. While 53.4% of allografts areas of specimens were comprised of fibrous tissue or marrow, only 51% of the xeno-

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30 • Vol. 8, No. 7 • November 2016

Table 2: The Summary of the Histomorphometric Analysis by the Sites

Bone as Vital Bone as Non Vital Bone Percent of the a Percent of the as a Percent of Specimen ID Recipient Site Specimen Specimen the Specimen

Allograft Used

1 24/13-01 #3 59 100 0

2 24/13-03 #3 45 100 0

3 6/13/2001 #3 32 85 15

4 26/13-02 #3 29 100 0

5 26/13-03 #3 47 95 5

Average 42.4 96 4

Std. Deviation 12.16 6.52 6.52

XenograftUsed

6 24/13-02 #14 61 100 0

7 24/13-04 #14 56 90 10

8 6/13/2002 #14 31 100 0

9 26/13-02 #14 44 100 0

10 26/13-04 #14 47 100 0

Average 47.8 98 2

Std. Deviation 11.61 4.47 4.47

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graft areas of specimens were occupied by the fibrous tissue and marrow. Clinical analysis of the pre-augmentation and post-augmentation measurements established that in all augmented sites a consistent and statistically measurable increase of the bone structure was achieved.

DISCUSSIONThe imperative goal of any bone regenerative and reconstructive procedure is that regener-ated bone can in fact bear functional loads as well as maintain sustainable bone architecture around the implant fixture. The results of the study proved that the regeneration of the deficient bone after maxillary sinus augmentation with utilization of distinctly different biomaterials generally pro-duces statistically measurable positive outcomes.

Due to the non-invasive nature and limitations of traditional clinical protocols obtaining of the specimens from human subjects for the histologi-cal studies is exceptionally difficult. Historically, many previously conducted clinical research proj-ects were limited to the measurements obtained by means of computed tomography (CT). Com-parisons of pre- and postoperative CT radiography results clearly demonstrated new bone formation of the sinus floors. Even though the radiologic evidences of new bone were clearly observed, no study was designed to obtain any conclusive histological evidence of the new bone formation.

Perhaps one of the first histological evi-dence that effectively verified the formation of new bone were presented by Palma et al.1 as a result of animal experiments. The design of the study was to determine a difference between autograft assisted and no grafting mate-rial sinus augmentations. Palma et al. recog-nized no histological differences between newly

formed bone samples obtained after healing. First histological composition of newly

formed human bone was presented in the study by Sohn et al.2 The experiment pre-sented both radiographic and histologic evi-dence of the newly formed maxillary bone adjacent to the implants placed 6 months prior. Sinus elevation was completed by eleva-tion of the maxillary membrane and without use of any biomaterials to assist the healing.

Recent clinical evidence-based practice sug-gests that graftless sinus augmentation is as effective as traditional maxillary membrane eleva-tion with utilization of biomaterials to maintain the volume formed inferiorly to the membrane to allow a formation of new bone. Historical find-ings certainly support this clinical concept.

Research by Boyne et al.3 described contralat-eral (graft biomaterial vs. graftless) maxillary sinus augmentation in monkeys with subsequent implant placement. Radiographic evidence of newly formed bone was observed bilaterally even around the implant placed into graftless environment with evident perforations into the sinus space.

This clinical approach was extensively researched by Lundgren et al.4 investigating graft-less maxillary implant placement. The technique involved an open window approach and mem-brane elevation with concurrent implant place-ment and no biomaterial use to maintain the volume. The study that included ten patients, twelve sinus augmentation procedures and 19 implants demonstrated an excellent fixture stability and radiographically evident new bone formation.

An additional study by Sohn et al.5 presented conclusive evidence of new maxillary bone for-mation after utilization of absorbable gelatin as a graft medium. This study focused on seven

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patients and included eighteen implants placed under elevated membrane with subsequent graft-ing of the space with resorbable gelatin material. Six months’ evaluation presented strong radio-graphic evidence of the new bone formation.

A similar study by Chen et al.6 was designed to perform a graftless sinus augmentation with uti-lization of venous blood only. Thirty-three patients were included with forty-seven implants concur-rently placed. Two year follow up demonstrated a 100% of implant survival and radiographic evidence of increases in bone height rang-ing from 3 mm to 9 mm with 4.5 mm. average.

Earlier research lead to a deeper understand-ing of the osteogenic potential of the Schnei-derian membrane, particularly of its periosteal side. Even though the evidences of the graft-less bone regeneration after membrane eleva-tion speak for themselves, the specifics of the regenerative mechanism are very well known.

Additional and perhaps revolutionary contribu-tion to the study of the osteogenic potential of the Schneiderian membrane was conducted by Srouji et al.7 The study was conducted on humans both in vitro and in vivo aiming to clarify the cel-lular mechanism of the bone formation and to test the osteogenic potential of the Schneiderian membrane. In this study specimens of the sinus membrane were histologically examined with uti-lization of the flow cytometry analysis. The analy-sis was designed to establish and further analyze mesenchymal progenitor cell markers. The study established that the Schneiderian membrane cells capabilities to induce various osteogenic markers such as osteopontin, osteocalcin, osteo-nectin and bone morphogenic protein-2. Addi-tionally, the study established a cellular potential to induce and extracellular matrix mineralization.

Perhaps the most exciting part of the experiment was conducted in in vivo environment. Srouji et al. implanted cultured cells consisted of HA/β-TCP and a fibrin clot under the skin of a mice. Re-examination of the specimen after 8 weeks provided histologic evidence of new bone forma-tion. The study clearly established a strong osteo-genic potential of the Schneiderian membrane.

Further research by Srouji et al.8 provided a great contribution to the entire Schneide-rian membrane research. Srouji et al. con-ducted in vivo experiments to test whether the sinus membrane has its own inherent biologic osteogenic capacity. The experiment involved encapsulation of the fibrin clot into the speci-men of the human maxillary sinus membrane with subsequent subcutaneous implanta-tion into mice. The results demonstrated new bone formation proving intrinsic osteogenic potential of the Schneiderian membrane.

The attention of many clinicians was directed at the factual findings confirming an adequate of vitality of the newly formed bone. Hatano et al.9 conducted a study with venous blood clot acting as a graft medium with con-current maxillary implant placement. Six month postoperative histomorphometric examina-tion established the vitality of newly formed bone to be at 38.7%. Comparatively, this study’s histomorphometric analysis estab-lished new bone vitality at 97.0% (average).

The results of histomorphometric analy-sis conducted for this study established a very high level of newly formed bone vitality indicat-ing good regenerative results in both groups of the specimens. All specimens revealed an ade-quate presence of mature bone in both groups.

As many retrospective studies, this study

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has inherent limitations. Certain degree of vari-ability may be present within the data due to the nature of the sampling and specimen collection procedure. Subjective imperfection may, to a cer-tain degree affect the data collected. Utilization of prefabricated intraoral surgical stent minimizes inaccuracies while collecting specimen samples and help to re-establishing a reference position to assure that histologic specimen was collected exactly at the at the point of original augmentation.

CONCLUSIONSThis analysis demonstrated close quantitative sim-ilarities of histologic composition between newly formed bone specimens obtained after maxillary sinus augmentation regardless of the biomate-rial used. The results indicated that both Allograft and Xenograft biomaterials allow regeneration of fully vital osseous tissue within six months post augmentation. These results most probably could be attributed to the osteogenic properties of the Schneiderian membrane. Grafting materials, satu-rated with host’s blood play the role of a volume preserver, are biocompatible and promoted osteo-conduction, acting as a matrix for bone formation. Notwithstanding nature of the grafting mate-rial, graft assisted maxillary sinus augmentation is a safe and predictable treatment modality. l

Correspondence:Dr. Edward Ruvins9450 East Mississippi AvenueSuite # ADenver CO 80247303-368-0777 Fax: 303-484-4024Email: [email protected]

AcknowledgementsThe authors gratefully acknowledge a contribution of Dr. Hari Prasad of Hard Tissue Research Laboratory of the University of Minnesota School of Dentistry for the completion of histological analysis of the specimens obtained for this research project.


References1. Palma VC, Magro-Filho O, de Oliveria JA, Lundgren S, Salata LA, Sennerby L.

Bone reformation and implant integration following maxillary sinus membrane elevation: an experimental study in primates. Clinical Implant Dentistry and Related Research. 2006;8(1):11-24.

2. Sohn DS, Lee JS, Ahn MR, Shin HI. New bone formation in the maxillary sinus without bone grafts. Implant Dentistry. 2008 Sep;17(3):321-31.

3. Boyne PJ. Analysis of performance of root-form endosseous implants placed in the maxillary sinus. Journal of Long Term Effects of Medical Implants. 1993;3(2):143-59.

4. Lundgren S, Andersson S, Gualini F, Sennerby L. Bone reformation with sinus membrane elevation: a new surgical technique for maxillary sinus floor augmentation. Clinical Implant Dentistry and Related Research. 2004;6(3):165-73.

5. Sohn DS, Moon JW, Moon KN, Cho SC, Kang PS. New bone formation in the maxillary sinus using only absorbable gelatin sponge. Journal of Oral Maxillofacial Surgery. 2010 Jun;68(6):1327-33.

6. Chen TW, Chang HS, Leung KW, Lai YL, Kao SY. Implant placement immediately after the lateral approach of the trap door window procedure to create a maxillary sinus lift without bone grafting: a 2-year retrospective evaluation of 47 implants in 33 patients. Journal of Oral Maxillofacial Surgery. 2007 Nov;65(11):2324-8.

7. Srouji S, Kizhner T, Ben David D, Riminucci M, Bianco P, Livne E. The Schneiderian membrane contains osteoprogenitor cells: in vivo and in vitro study. Calcified Tissue International Journal. 2009 Feb;84(2):138-45.

8. Srouji S, Ben-David D, Lotan R, Riminucci M, Livne E, Bianco P. The innate osteogenic potential of the maxillary sinus (Schneiderian) membrane: an ectopic tissue transplant model simulating sinus lifting. International Journal of Oral Maxillofacial Surgery. 2010 Aug;39(8):793-801.

9. Hatano N, Sennerby L, Lundgren S. Maxillary sinus augmentation using sinus membrane elevation and peripheral venous blood for implant-supported rehabilitation of the atrophic posterior maxilla: case series. Clinical Implant Dentistry and Related Research. 2007 Sep;9(3):150-5.

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Soldatos et al

Background: Bone overheating may lead to failure of dental implant osseointegration. The purpose of this study was to compare three dif-ferent implant drill designs in order to evaluate the temperature changes over the osteotomy area.

Methods: Three different designs were included: a tapered design (D1), a self-tapping tapered design (D2) and a parallel wall design (D3). A polyurethane foam block 125 x 87 cm was used as an alternative medium to human mandible and was soaked in a water bath at 37ºC. The temperature was measured at the end of each drilling sequence through the use of a thermocouple device. For each implant system, the drills were used with and with-out external irrigation, at 800 (control group), 1000 (test group 1) and 1200 revolutions per minute (RPM) (test group 2), respectively.

Results: The highest temperature was found with D1 initial drills (65.0±6.90C). The lowest temper-ature was noted with D2 initial drills (47.3±2.90C). For the D1 system, the use of irrigation resulted in statistically significant lower maximum tem-perature by 8.70C. For the D2 system, irrigation was found to significantly decrease the average maximum temperature by 7.10C. For the D3 sys-tem there was not sufficient evidence to conclude there was a relationship between speed and irri-gation on maximum temperature. Spaghetti plots showed that the D2 system has more variabil-ity in maximum temperature than that observed for D1 and D3. As the drill size increases, maxi-mum temperature tends to decrease and this pattern was more obvious with the D1 system.

Conclusions: Within the limitations of this pilot study, it can be concluded that differ-ent implant designs have different thermody-namic behavior. This study supports the use of irrigation during dental implant placement.

Temperature Changes During Implant Osteotomies Utilizing Three

Different Implant Systems: A Pilot Study

Dr. Nikolaos Soldatos1,3 • Dr. David Gozalo2 • Dr. Kerri Font3 Dr. David Moreno2 • Dr. Charles Powell3

1: Department of Periodontics and Dental Hygiene, School of Dentistry, University of Texas, Health Science

Center at Houston

2: Division of Restorative Dentistry, Department of Surgical Dentistry, University of Colorado School of Dental Medicine

3: Division of Periodontics, Department of Surgical Dentistry, School of Dental Medicine, University of Colorado,

University of Colorado School of Dental Medicine

Abstract

KEY WORDS: Dental implants, adverse effects, mandibular osteotomy, heat generation

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INTRODUCTIONLiterarure supports the use of dental implants to restore partially of fully edentulous patients.1,2 Jung et al., in a systematic review found that the five-year survival rate of single implant supported crowns is 94.5% and that of implant supported fixed partial dentures (FPD’s) is 95.2%.3 In addi-tion, the ten-year survival rate of single implant supported crowns and implant supported FPD’s is 89.4% and 86.7%, respectively.1 The suc-cess of dental implants is based primarily on the extent of osseointegration. Reasons that may lead to failure of osseointegration or/and implant failure are: (i) previous infection of the site, (ii) peri-implantitis, (iii) systemic factors, (iv) implant fracture, (v) immediate or functional over-loading, (vi) compression necrosis, (vii) reverse torque testing, and (viii) bone overheating.4,5

Bone overheating or thermonecrosis have been reported in the literature and may be caused at the time of implant placement or the time of surgical exposure of implant. Among the factors which can contribute to heat stress are drill speed, drill sharpness, drill force, drill depth, drill design, drill diameter, bur wear, bur geometry, cortical thickness, use of surgical drill guides and lack of insufficient irrigation.6-8

At the time of implant placement, lack of irriga-tion increases the risk of bone overheating. Spe-cifically, small diameter drills may generate more heat than larger diameter drills and they need to be irrigated when used in dense bone.9 Con-temporary larger diameter drills may not gener-ate the detrimental heat and may incrementally remove any heat damaged bone from the previ-ous drilling.9 Heat stress during drilling is one of the causes for osseointegration failure when tem-perature exceeds 47ºC during osteotomy prepa-

ration, causing a temperature-dependent delay in bone formation.10 Albrektsson and Eriksson found that setting the temperature between 47 - 50ºC for one minute significantly reduced bone forma-tion around implants, while they found no signifi-cant effects when the temperature stayed below 47ºC for one minute.11 Furthermore, Eriksson et al following on their initial research, found that the maximum temperature should not exceed 30.3°C for five seconds.12 Other studies support Albrekts-son’s findings, showing that 48°C heat stress does not obstruct bone formation. Maximum tem-perature during drilling is higher without irrigation than with irrigation, therefore it is easier to reach the critical threshold without it.13 Some stud-ies have even shown that temperature might rise up to 130.1ºC without the use of irrigation.8 An increase in the temperature causes an increase of the area of dead osteocytes which hinders the regeneration of the periosteal membrane.10

In vitro studies have looked into drilling speed profiles in addition to the necessity of irriga-tion during implant placement. When irrigation is applied, Lavelle et al. found that internal irrigation reduces heat more than external irrigation.14 Bris-man et al. reported that increasing speed and load results in efficient cutting with less heat,15 and Spatz et al., reported that high-speed drill-ing produces earlier, more rapid cutting with-out significant necrosis and is better than the conventional drilling speed.16,17 Other studies have shown no difference between conven-tional and high-speed cutting18 and an additional advantage in using external irrigation in com-bination with internal in reducing the heat on the site.19 Tehemar et al. found that atraumatic preparation of the recipient site is an impor-tant factor influencing implant survival.20 Finally,

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bone overheating during drilling is one of the causes of an implant periapical lesion.21,22

The purpose of this study is to com-pare three different implant designs, in three different drilling protocols (800, 1000 and 1200 RPM), with and without exter-nal irrigation, in order to compare the tem-perature stress over the osteotomy area.

MATERIALS AND METHODSThree different implant drill designs were used for this study. For each implant system, the drills were used per the manufacturer’s rec-ommended sequence, with and without exter-nal irrigation, at 800 (control group), 1000 (test group 1) and 1200 RPM (test group 2), respectively (18 groups). The groups with-out irrigation were used as reference groups. For each drill sequence of the three implant systems, all drills were used, from the initial through the final drill. Maximum temperature along with time spent at maximum tempera-ture and time to return to 370C were recorded.

The implant designs included a tapered design (D1)*, a tapered self tapping design

(D2)#, and one parallel wall design (D3)^. A polyurethane foam block~ (125 x 87cm) with closed cell content ranging from 96.0 to 99.9% was used as an alternative test medium substituting for human mandibular bone. The mechanical properties of the selected block were similar to those of mandibular bone23 (Table 1). In an attempt to duplicate the clini-cal conditions, the block was soaked in a water bath§ at 37ºC. The criteria, used in this pilot study, were: (i) use of new drills for each implant system, (ii) all procedures were per-formed by the same surgeon (N.S.), (iii) use of the same implant motor† and the same hand-piece¥ for all implant systems, (v) use of the same surgical room with standardized 250C room temperature, (vi) the use of external irriga-tion of 0.9% sodium chloride solution in room temperature, and (vii) no use of a spear drill.

The temperature was measured at the end of each drilling sequence through the use of a ther-mocouple∞. The thermocouple was attached to the water bath allowing for its wires to measure the temperature directly in the osteotomy walls from the most coronal to the most apical part.

Table 1: Mechanical Properites of the Block, in Comparison of the Mandibular Base

Misch 199925 Saw Boney®

Elastic Modulus (MPa) 24.9-240 210 (cortical plates present) (mean value 96.2)

Elastic Modulus (MPa) 3.5-125.6 N/A (cortical plates not present) (mean value 56.0)

Compressive Strength (MPa) 0.22-10.44 9.4 (mean value 3.9)

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STATISTICAL ANALYSISData analysis was done using the R version 3.1.2 (2014-10-31).24 This analysis considered only the maximum temperature achieved. Descriptive figures and statistics were evaluated to assess patterns in the data and identify potential mea-surement errors. To evaluate the association between RPM and temperature at the pilot drill and to compare the two test groups, one-way ANOVA models were created for each drill type. If results indicated a significant association between RPM and temperature, individual linear regres-sion models for each drill type were used to esti-mate the effect sizes. Parameter estimates for the change in mean maximum temperature between 1000 RPM and 1200 RPM compared to the ref-erence group of 800 RPM is reported along with 95% confidence intervals and pairwise compari-son p-values. To assess the overall effect of irri-gation for a given drill, maximum temperature for the pilot drill was modeled by whether irrigation was used in univariate regression analyses. The estimate for the change in mean maximum tem-

perature for irrigation compared to no irrigation was reported along with 95% confidence interval and p-value. Finally, maximum temperature for the pilot drills was modeled using multiple regression models including both RPM and use of irrigation to assess the effect of one variable while keeping the other constant. Estimates for RPM represent the mean change in maximum temperature while keeping irrigation use constant, where estimate for irrigation represent the mean change in maxi-mum temperature at a constant RPM. Similar to univariate results, the parameter estimates for the multivariable model are reported along with 95% confidence intervals and p-values. Spear-man correlation was used as it is less sensitive to non-normality in distributions where the rela-tionship between maximum temperature and drill number appears to follow a quadratic trend.

RESULTSAll three initial drills have an excess portion on the most apical aspect, which measures 1.2 mm for D1, 1.1 mm for D2 and 0.7 mm for D3 respec-

Figure 1: D1, D2 and D3 systems’ initial drills. All three initial drills have an excess portion on the most apical aspect, which measures 1.2 mm for D1, 1.1 mm for D2 and 0.7 mm for D3 respectively.

Figure 2: D1 and D2 system drills transferred the excess portion of 1.2 and 1.1 mm respectively, to the final depth of the osteotomy. D3 system drills did not transfer the excess portion to the final depth of the osteotomy.

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38 • Vol. 8, No. 6 • June 2009

tively (Figure 1). D3 drills, compared to D1 and D2, did not transfer the excess portion of 0.7 mm to the final depth of the osteotomy (Figure 2). D1 and D3 drills at the final depth of the osteotomies left space for air and water to cool the osteot-omy. On the contrary, D2 drills did not leave any space for the same purpose (Figures 3, 4, 5).

The critical temperature point used in this study was 47ºC based on the Eriksson et al. stud-

ies.12 The initial drill sites of the test groups 1, 2 (with and without irrigation) were analyzed in a single ANOVA model (Table 2). The initial pilot drill, which raised the temperature at 65.0±6.90C was from the D1 system, when it was used with-out irrigation at 1200 RPM. The lowest tem-perature was noted with the D2 system at 1000 RPM with irrigation (47.3 ± 2.90C). These results were found to be statistically significant (Table 2).

Figure 3: D1 system drill. Figure 4: D2 system drill.

Figure 5: D3 system drill. Figure 6: The semi partial correlation analysis.

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The initial drill of D1, when irrigation was not applied, raised the temperature higher than the other systems (75.60C). The use of irrigation resulted in a significantly lower maximum tem-perature (8.70C, p < 0.01), irrespective of RPM. Speed did not significantly impact the maximum temperature for the initial drill when unadjusted for irrigation, however, it was found to be significant when irrigation was adjusted (p = 0.03). Speed of 1000 RPM compared to 800 RPM increased the average maximum temperature by 6.8 degrees (p = 0.01). The larger diameter drills of D1 and D3 systems with irrigation did not generate heat over 470C. For the D2 initial drill, the irrigation was found to significantly decrease the average maximum temperature. Maximum temperature was on average 7.1 degrees lower when using irrigation adjusting for speed (p < 0.01). With-

out irrigation, it took 17 minutes to return back to 370 C. For the D3 system, due to the high vari-ability in the initial drill measurements, there was no significant effect seen for speed or irrigation on maximum temperature. With the rest of the drills, no relationship was found between speed and irrigation on maximum temperature (Table 3).

With D1 system and following the initial drill, there was a difference between the groups with and without irrigation. Without irrigation at 1000 and 1200 RPM, four drills out of seven, were over the threshold of 470 C. With the use of irri-gation at 800, 1000 and 1200 RPM, only the initial drill increased the temperature over 470 C. The D1 system had a clear pattern, as the drill size increased the maximum temperature tended to decrease. D2 system had more variability and no clear pattern and consistency in maximum

Table 2: Test Groups 1, 2 with and without Irrigation Between the Three Implant Systems

*Statistical Initial Significant Results Drills p ≤ 0.05 D1 (°C) D2 (°C) D3 (°C)

Group 1 1000 RPM 54.9 ± 10.5* 47.3 ± 2.9* 55.6 ± 2.4* w/irrigation*

Group 2 1000 RPM 62.2 ± 2.6* 54.6 ± 2.8* 55.1 ± 8.7* w/o irrigation*

Group 3 1200 RPM 60.2 ± 4.8* 54.3 ± 4.7* 52.9 ± 7.2 w/irrigation*

Group 4 1200 RPM 65.0 ± 6.9* 57.5 ± 6.0* 54.3 ± 3.6* w/o irrigation*

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temperature. This variability was most notable at 1000 RPM without irrigation and at 1200 RPM both with and without irrigation. D3 system at 1000 and 1200 RPM without irrigation, showed only the initial and the second drills being over the threshold of 470 C. Similar to D1 system, it had a clear pattern. As the drill size increased, the maximum temperature tended to decrease.

The semi partial correlation analysis confirmed the previous findings. It showed that the D2 sys-tem has more variability across the drill sizes compared to D1 and D3. The Spearman correla-tion coefficient was estimated as -0.273 for D2 compared to -0.663 and -0.718 for D3 and D1, respectively. The negative correlation indicates that as the drill size increases, maximum tem-

perature tends to decrease. The latter was more obvious with D1 and D3 systems (Figure 6).

DISCUSSIONBone remodeling to establish the biological width, takes place when second stage surgery is per-formed and/or when the implant is exposed to the oral environment. Crestal bone levels around non-platform switched implants are typically located approximately 1.5 to 2 mm below the implant-abutment junction (IAJ) at one year follow-ing implant restoration, but are dependent upon the initial location of the IAJ relative to the bony crest.25,26 A stable bone level around the implant neck is a prerequisite for achieving support and long-term optimal and stable gingival contours.25

Table 1: Univariate and Multivariable Logistic Regression Estimates with Corresponding 95% Confidence Intervals and

p-values by Drill Type for the Initial drill size

Implant Designs Multi-Variable Model (°C) p-value

D1 (RPM) 800 vs. 1000 6.79 0.01 800 vs. 1200 2.1 0.4 Irrigation -8.72 < 0.01

D2 (RPM) 800 vs. 1000 4.62 0.11 800 vs. 1200 1.52 0.11 Irrigation -7.09 < 0.01

D3 (RPM) 800 vs. 1000 1.47 0.73 800 vs. 1200 -0.25 0.83 Irrigation -0.41 0.083

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The rationale behind this study was based on clin-ical and radiographical observations from patients with implants which lost radiographically more than 3 mm of bone support around the implant shoulder before the second stage surgery took place. We attempted to imitate the thermodynami-cal properties of bone during osteotomy prepara-tion in an in vitro study. Three different implant drill designs were used to accommodate for the diver-sity found in clinical practice and to better study the thermodynamical changes during implant site preparation. According to Jochum & Reichart there is a 1.5° C difference in temperature between distances of 0.3 mm and 0.5 mm from the oste-otomy site.27 Therefore, any attempts to measure the temperature 0.5 mm and 1 mm away from the osteotomy site were inaccurate and were not applied. Furthemore, in this study we did not use spear drills since the use of a spear drill is known to increase thermal oscillation by 40 C degrees.28

Histologic analysis of implants that failled to osseointegrate revealed non-viable bony seques-tra with bacterial colonization.6 The findings from the histologic analysis suggested that the rea-son for the lack of osseointegration and implant failure was due to bone compression necrosis when the implants were placed with excessive torque.6 Similar findings were found by Piattelli et al.29 Their results revealed the same histology as that of Bashutski et al.6 Bacteria occupied all the marrow spaces, and the necrotic bone that surrounded the implant was demineralized. With the use of higher magnification the authors observed a gap between the implant and bone, which contained polymorphonuclear granulo-cytes. This indicated loss of osseointegration due to bone overheating at the time of implant place-ment. The study, however, did not give any infor-

mation about the drill sequence, drill RPM, type of implant placement, drill design, previous site infections, irrigation during implant placement, the extent of the necrotic bone or any thermal changes during implant osteotomy preparation.6

D1 and D3 system measurements showed that with irrigation only the temperature produced by the pilot drills was well over 470 C, but as the drill size increases, maximum temperature tends to decrease. The larger diameter drills of D1 and D3 systems with irrigation did not generate det-rimental heat, which is in accordance with the findings of Flanagan et al.9 Kim et al. used an animal in vitro model with pig ribs and utilized drilling at 50 RPM without irrigation. This did not produce overheating at the tip of the drills, indicating that there may be a direct relationship between drill diameter and bone temperature.30 The maximum temperature observed was 2.5º C and the minimum was 1.6º C, respectively. Even though pig ribs are weaker than human mandib-ular bone, they have excellent homogeneity of cortical bone thickness. Kim et al. in their study, used three different implant systems (Bicon®, Branemark®, Osstem®) to accommodate for the diversity found in clinical practice, something that we adapted in our study as well. Due to the low RPM used in this study, the maximum tem-perature did not exceed 470 C.30 The thermo-dynamical pattern noted in the Kim et al. study is juxtaposed to the results noted in our study. They found that the larger the drill diameter, the higher the bone temperature became due to the greater bone volume to be cut, and therefore cre-ated more friction during the drilling procedure.30

Santos et al. compared guided (GG) and clas-sic (CC) drilling protocols for bone heating, drill deformation and drill roughness after implant site

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preparation. in twenty male white rabbit tibiae. The method used was drilling at 1600 RPM in five subgroups (0, 10, 20, 30, 40 osteotomies), using a spear drill first to mark the position, then using in sequence a 2.0 mm, 3.0 mm, and 3.15 mm drill to a 4 mm depth with external irrigation. A statis-tically significant difference was found in thermal oscillation between the two drilling protocols, with bone heating three times higher with the guided drilling protocol. The tissue temperature and sur-face roughness increased with the number of times the drills were used.28 This is in accordance with findings from Misir et al who verified that after 35 drill reutilizations, the drills increased heating.4

As found in numerous studies, the best way to prevent bone from overheating during osteotomy preparation is irrigation of the surgical site and low RPM. Lavelle & Wedgwood affirmed that internal irrigation is more effective than external irrigation in reducing friction during osteotomy.31 Another factor that influences the cutting capacity of drills is the repetition of sterilization cycles by auto-clave.32 However, Jochum & Reichart found no statistically significant difference in bone heating between reused drills that were washed and ster-ilized than drills that were just washed.27 Implant site preparation protocols currently in use by dif-ferent implant systems involve drilling at speeds of 1,000 to 1,500 RPM. Higher RPM and the lack of irrigation of the surgical site may have as a result mechanical and thermal damage to the tissue and a destructive effect on the initial state of the cav-ity housing the implant.33 This mechanical and thermal damage can also activate the release of inflammatory mediators such as cytokines, oxygen radicals, and lysosomal enzymes that in their turn could produce a widening zone of necrosis with the presence of fibrous tissue at the interface.34

Yamada et al. in their study used the same polyurethane block we used in our study, in dif-ferent compressive strengths of 8 and 18 MPa, respectively. This compressive strength dif-fers from what has been reported by Misch et al. that the mandible has a range of compres-sive strength between 0.22 and 10.44 MPa.23 Yamada et al. placed the block in a water bath at 370 C, but it was only half way immersed; in our study the block was covered to the top, but not over the osteotomy sites. In addition, they used internal irrigation drills at 400, 800, 1200 and 1600 RPM in three different motions, with-out mentioning the design of the drill, which sys-tem they used, or how many drills were used for each osteotomy. The mean maximum temperature for the drill motion was 40.9° C when not inter-mittent, 32.8° C for intermittent motion without exposure of the drill tip, and 31.0° C for intermit-tent motion with exposure of the drill tip. Bone density and constant motion were more strongly correlated with maximum temperature than with speed or intermittent motion with or without expo-sure of the tip of the drill. They found no signifi-cant difference in temperature changes after 90 uses of the same drills, even though Santos et al recommend using the drills only 50 times.37

To our knowledge, this is the first study that compares three very characteristic implant designs in three different RPM, with and with-out irrigation, which showed different patterns for thermal changes at the time of the osteotomy preparation. Within the limitations of this study, clinicians should prepare the osteotomy and place implants with internal or/and external irri-gation. Clinicians should be very careful with the RPM used for the different implant designs and their pilot drills. Further histological stud-

Soldatos et al

ies should be performed, in order to validate our results and better evaluate the size and the cells of the necrotic bone area at the implant/bone interface, during implant site preparation.

CONCLUSIONDifferent implant design drills have different thermodynamical behavior during implant site preparation. This study shows the necessity of irrigation during implant lacement, therefore cli-nicians should always prepare the implant site and place implants under continuous irrigation. l

Corresponding author:Dr Nikolaos SoldatosDepartment of Periodontics and Dental Hygiene School of Dentistry, University of Texas, Health Science Center at Houston. 7500 Cambridge St, • Suite 6429, Houston, TX, 77054Office: 713-486-4361 • Fax: 713-486-4393 Email: [email protected].

AcknowledgementsThe authors report no conflict of interest related to this study. The authors would like to particularly thank Jeffrey Stansburry PhD, (Professor and Asso-ciate Dean for Research, University of Colorado, USA) for the mentorship and the lab equipment, Miranda Kroehl PhD and Rachel Blumhagen PhD candidate (statisticians, University of Colorado, USA) for the statistical analysis and Dr. Raymond Yukna, (Professor, University of Colorado, USA) for assistance with manuscript preparation.*BioHorizons Tapered Internal Plus (BioHorizons®, Birmingham, AL)#Nobel Active(Nobel Biocare®, Kloten, Switzerland)^Straumann Bone Level (Straumann®, Basel, Switzerland)~Saw Bones® §Whip-Mix†3i implant motor® (Zimmer Biomet 3i, Parsippany, New Jersey, USA) ¥W&H hand piece 20:1®∞Tecpel 322/K-type®

DisclosureThe authors report no conflicts of interst with anything mentioned in this article.

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