Bone Density: Its Influence on Implant Stability After Uncovering Open Access

BONE DENSITY: ITS INFLUENCE ON IMPLANTSTABILITY AFTER UNCOVERINGRESEARCHHarold F. Morris, DDS, MSShigeru Ochi, PhDPatricia Crum, DDS, MPAIra Orenstein, DDSRichard Plezia, DDS, MSKEY WORDSDental implantsBone densityImplant stabilityPeriotestOsseointegrationHarold F. Morris, DDS, MS, is codirector atthe DVA Dental Clinical Research Center andstaff prosthodontist at the VA Medical Center,2215 Fuller Road, Ann Arbor, MI 48105.Shigeru Ochi, PhD, is codirector andbiostatistican at the DVA Dental ClinicalResearch Center and VA Medical Center, AnnArbor, MI.Patricia Crum, DDS, MPA, is chief of dentalservice at the VA Medical Center, Ann Arbor,MI, and associate professor in the Departmentof Periodontics, Prevention, and Geriatrics atthe University of Michigan, Ann Arbor, MI.Ira Orenstein, DDS, is staff dentist at the VAMedical Center, Bronx, NY, and ColumbiaUniversity School of Dental and Oral Surgery,New York, NY.Richard Plezia, DDS, MS, is chief of dentalservice at the John Dingell VA Medical Center,4646 John R Street, Detroit, MI.Primary implant stability and bone density are variables that have long beenconsidered to be essential to achieving predictable osseointegration and longtermclinical survival. Although the dentist can control most factors associatedwith implant survival, bone density is the one factor that cannot be controlled.Measuring implant stability would assist in determining if an implant hasintegrated and is ready for the fabrication of the final prosthesis. Changes inimplant stability in each type of Bone Quality (BQ-1, -2, -3, and -4), which mayoccur with time, have not been studied. Such information could help identifywell-integrated implants and identify changes associated with impendingimplant failure. Several studies have used the Periotest instrument to studyimplant stability. Use of the Periotest implant stability will be studied duringeach phase of implant treatment for each bone density, and a range for clinicallysatisfactory integration will be suggested. Implant stability changes over time,and the changes are different for each bone density as the bone surrounding thenonhydroxyapatite implant becomes denser. This is clearly demonstrated in apostmortem histological specimen. The changes in implant stability (PeriotestValues [PTVs]) are more apparent in BQ-1 and BQ-2 bone and less apparent inBQ-3 and BQ-4 bone. The Periotest is capable of providing valuable informationconcerning favorable or unfavorable changes in the bone-implant interface afteruncovering. In addition, it can help identify when an implant is ready to beloaded. A new range of PTVs (25 to 22) is suggested for monitoring the statusof implants. Implants with PTVs more positive than 22 would indicate a boneimplantcomplex that may be marginal.of the bone-implant interfaceand (2) the density of the surroundingbone (ie, the bone-implantcomplex). Implant stability, as measurementsof stability would assist theclinician in determining implant integrationbefore fabrication of the finaldental restoration. After delivery andloading of the final restoration, reliable I sta e th rs: cto f e c adosseoouplusoimfaplants(1)is relatedtusto bone-implant complex. Reliable methis o tus sta e th ects refl u e ted osseointegra f o successNTRODUCTION In general, the long-term clinicalnsuredes (PTVs),by the Periotest as PeriotestfVala-Journal of Oral Implantology 263BONE DENSITY AFTER IMPLANT UNCOVERYFIGURE 1. Periotest instrument for measuring implant stability. The plunger rod within thehandpiece is electrromagnetically accelerated; when it strikes a firm object, the plungerrebounds into the handpiece. The time that the plunger remains in contact with the objectis returned to the Periotest, and the central processing unit converts this time into a PeriotestValue (PTV). PTV calibration ranges from 28 to 150 PTVs. The more rigid the object,the more negative the PTVs, and flexible objects provide more positive values. Range forintegrated implants is 25 to 22 PTVs. Between 22 and 12, implant may appear clinicallystable but suggests a marginal bone-implant complex.measurements may well be equally importantin monitoring the status of thebone-implant complex to identify earlysigns of problems. Such informationwould also contribute to a better understandingof bone response to dentalimplants after uncovering. If earlysigns of problems within this complexcould be measured, they would permitearly intervention and research to developnew and innovative correctivetreatments.Some reports suggest that primaryimplant stability may be directly relatedto the bone quality and quantity, theimplant design, and the site preparation.1 Other reports speculate thatgreater contact between the implantand the bone may be more favorable,but this relationship is not well understood.2 Although bone density at thetime of implant placement is generally264 Vol. XXIX/No. Six/2003accepted as being important to immediateimplant stability, the influence ofeach of the 4 bone densities on earlyand long-term implant stability has notbeen well documented.One study reported that in densebone, implant stability decreasesslightly with time, despite clinical evidenceof osseointegration and increasedbone-implant contact.3 However,another study reported that insoft bone there is an increase in implantstability with time.4 Scientificdata from an independent clinicalstudy are needed to demonstrate anychanges in the stability measured withthe Periotest or other methods. Ideally,such research should include the testingof large numbers of implants andbe supported by postmortem specimensobtained from humans.The dental implant community haslong sought a noninvasive method thatcould assess implant stability. It shouldbe capable of providing a reliable, indirect,noninvasive measurement of thebone quality and quantity associatedwith this complex, as well as anychanges in this complex after clinicalloading. It is reasonable to assume thata change in implant stability representsmeasurable changes within the boneimplantcomplex. The stability data recordedover time may actually documentchanges in which the implant becomesincreasingly more stable or lessstable. Buser5 provided some insightinto the potential favorable or unfavorablebone responses around the implantto clinical loading when loadingis below, within, or exceeding normalphysiological limits. Loading the bonebelow physiological limits may resultin atrophy, whereas loading abovephysiological limits may precipitatefracture failures with eventual loss ofthe implant (ie, The Carter Hypothesis).Loading within acceptable limitsserves to stimulate bone, which can respondby becoming denser.To be of practical value, an instrumentused to measure implant stabilityshould be noninvasive, be nontraumatic,be easy to use in the clinical environment,exhibit a clinically meaningfullevel of sensitivity, and be reproducible.In 1986, Schulte6 described thePeriotest (Figure 1) in detail. It was developedinitially to assess bone atrophyand inflammatory periodontal conditionsaround natural teeth.7 It has beenused successfully to study changes intooth mobility and implants for largenumbers of implants and natural teethfor a period of 60 months.8The Periotest device consists of ametal case containing a central processingunit, a digital read-out screen,and artificial speech (Figure 1). Thecase is connected by a cord to a handpiecethat contains a percussion rod,which is electromagnetically acceleratedwhen the unit is activated. Whenthe rod comes into contact with a solidobject, it strikes the object and rebounds.The more rigid the bone-im-plant complex, the shorter the time theplunger remains in contact with it andthe faster it rebounds.The duration of contact betweenthe rod and the object being tested isreturned to the central processing unit(CPU) in the Periotest case. The CPUconverts the electrical output from thehandpiece into a PTV. The operatorgets both a digital readout and an audiblereadout of the PTVs. The instrumentis calibrated to a range of PTVsfrom 28 to 150, with the more negativevalues indicating greater stabilityand the more positive values indicatingless stability. Teerlinck et al9 reportedthat the PTVs for 30 patients with implantsthat were determined to be osseointegratedfell within a range from24 PTVs to 12 PTVs. Olive and Aparicio10also reported a similar range ofPTVs for osseointegrated implants.PTVs of 19 or greater were associatedwith implants that had failed and requiredremoval.In 1997, Meredith et al11 introducedthe so-called Resonance FrequencyAnalysis technique. As are the Periotestand other methods for measuringstability, the device is based on the assumptionthat the amount of bone-toimplantcontact determines how theimplant vibrates when tested.Although bone density is consistentlyreferred to as being important tothe long-term clinical performance ofdental implants, limited scientific informationaddresses the influence ofeach bone density on long-term survival.And although the dental surgeoncan control most factors associatedwith improving the chances for clinicalsuccess, bone density is the one factorover which the surgeon has no control.Branemark and Zarb12 described 4Bone Qualities (BQ-1, -2, -3, and -4)found in the edentulous jawbone. BQ-1is composed of homogeneous compactbone, which has been described to belike hard wood, when preparing theimplant site. BQ-2 has a thick layer ofcompact bone surrounding a densecore of trabecular bone, which has beendescribed as having the quality of aTABLE 1Distribution of bone quality in implant sites by arch and research stratum14Q-1 Bone (%) Q-2 Bone (%) Q-3 Bone (%) Q-4 Bone (%) Implant Site0.51.520Maxillary anteriorMaxillary posteriorMandibular anterior8.8 Mandibular posteriorhard pine. BQ-3 has a thin layer ofdense cortical bone around a dense acore of dense trabecular bone and feelslike a soft wood (eg, balsa wood). BQ-4bone represents the less dense boneand has a thin layer of cortical bonearound a core of low-density trabecularbone, which feels like Styrofoam.Misch13 also defined the 4 bone typesrelative to the surgical protocol, healing,treatment plans, and progressiveloading time periods that were optimalfor each bone type. In 1997, Truhlar etal14 reported on the distribution of thebone quality (density) in which 2910implants (Table 1) were placed in arandomized, prospective, scientificclinical study. The percentage of eachbone density found in each jaw regionwas very similar to percentages reportedby others.15-17The purpose of this paper is to reportscientific clinical data related tothe following questions: (1) what PTVswould suggest that the implant is integrated,(2) are there changes in thebone-implant complex after a normalhealing period, (3) are there changeswithin the bone-implant complex in responseto stimulation during loading,(4) what is the influence of each bonedensity on implant stability and whatchanges in implant stability over timeare normal, and (5) are these data supportedby human postmortem histologicalspecimens? Currently, little informationexists concerning the influenceof bone density on the stability ofendosseous dental implants at uncoveringand after loading of the prosthesis.MATERIALS AND METHODSA total of 30 Periotest units were purchasedon the open market. Of theseHarold F. Morris et al16231.85953142423642.6 33 56instruments, 6 were randomly selectedfor testing to study the reproducibilitywithin the same instrument andamong the 6 instruments. A series ofstandardization test devices were fabricatedand tested in vitro. They consistedof 2 types: (1) blocks of wood ofdifferent densities in which 2 implantsof the same design were placed; and(2) a metal membrane, which consistedof various metal types and thickness toalter the flexibility of the membrane,was placed over a hollow section at theends of a metal cylinder. Each end wascovered with a similar metal membranebut with different thickness toproduce very different rigidity. Thewooden-block and metal-membranetest samples were all coded for futurereference.The dimensions of the 4 blocks ofwood that were the test specimenswere 5.0 cm in depth, 10.0 cm wide,and 10.0 cm long. The materials for theblocks were selected to simulate thevarious bone densities: simulated BQ-1bone was made from a dense hardwood, BQ-2 bone was made with aslightly less dense wood, BQ-3 bonewas a soft wood, and BQ-4 bone wasa very soft wood. Two actual implant-fixture sites were prepared in eachblock of wood 3.8 cm apart. One implantwas placed into the prepared site,which had been filled with a thin layerof epoxy cement (to simulate an implantthat was integrated), whereas theother implant was seated without anythingbetween the implant and thewood (to simulate nonintegration). Theinstrument was activated, and thePTVs were recorded with the test specimen'sreference code.The clinical investigators weretrained in the intraoral use of the Per-Journal of Oral Implantology 265BONE DENSITY AFTER IMPLANT UNCOVERYTABLE 2Mean PTVs for each bone density at each follow-up visit*BoneQuality 3 mo 6 mo 9 mo 12 mo 18 mo 24 mo 36 mo 48 mo TotalBQ-1BQ-2BQ-324.6723.5722.5724.1723.6222.6224.3423.2822.7723.5123.4023.23BQ-4 22.88 22.20 21.70 21.55*PTVs indicates Periotest values; BQ, bone quality. There is an increase in the density ofthe bone surrounding the endosseous implant in response to functional stresses. Thischange in density is different for each of the bone densities. BQ-1 shows the greatest increasein stablity (negative PTVs 5 greater stability, the more negative the PTV the greaterthe stability of the bone-implant complex); BQ-2 shows a similar change, but it takes longerfor the final stability to develop; BQ-3 shows little or no negative (increase in stability overtime) change in PTVs; and BQ-4 shows the least change in implant stability.iotest device during a three-day trainingmeeting before activation of thestudy. A total of 3006 implants wereplaced during the study.18 For all clinicalmeasurements of implant stability,the tip of the plunger rod from the Periotest'shandpiece was carefully positionedabove the soft-tissue margin,and the Periotest was activated (Figure2A). Implant stability was tested 3months after uncovering and at 6, 9,12, 18, 24, 36, and 48 months. BQ foreach implant was determined duringthe placement of the implant by usingradiographs and tactile sensations. Althoughsome subjectivity was involvedin assessing a BQ at the time of implantplacement, the PTVs for the implantscorrelated well with the BQ classificationfor the bone in that area.19POSTMORTEM HISTOLOGICALSPECIMENThe comprehensive clinical study designallowed for the opportunity to obtainpostmortem specimens for histologicalanalysis to support clinicalfindings. One patient, who was enteredinto the study, had a fixed partial denturerestoration planned and fabricatedfor the mandibular posterior jaw region.The patient was later diagnosedwith cancer after the implants hadbeen in place and functioning for a periodof 24 months. At the time of entryinto the study, the patient signed a con-266 Vol. XXIX/No. Six/200324.3423.6122.7824.3423.6122.6224.3423.7622.7824.7924.0022.7624.4222.6722.8822.04 22.18 22.18 21.89 22.47sent form that permitted donation ofbone-implant complex for histologicalanalysis in the event of his death. Thebone quality in this area was recordedas BQ-2.RESULTS AND DISCUSSIONThe mean PTVs were pooled for all implantsplaced in all bone densities andwere tested. The PTVs varied slightly(range 23.06 PTVs to 23.40) duringthe 48-month observation period (Figure2C) at each evaluation visit. Thegreater the negative number, the betterthe stability of the bone-implant complex,whereas any trend toward positivevalues would indicate a less stablebone-implant complex. At 3 months afteruncovering, the mean PTV for allimplants was 23.2, indicating that allimplants exhibited good stability. At 6months, their stability had changedslightly to 23.1 PTVs; at 12 months,23.2 PTVs; at 18 months, 23.3 PTVs;at 24 months, 23.4 PTVs; at 36 months,23.3 PTVs; and at 48 months, 23.2PTVs. These variations in stabilitywereneither clinically nor statistically significant.Bone is a viable, living tissue thatresponds to stimulation by developinga more dense bone structure when thestimulation remains within normalphysiological limits.19 The histologicalspecimen obtained during this study(Figure 2B) provides a rare opportunityto view what appears to be a favorablebone response in a human histologicalspecimen. This specimen wasobtained as part of the same study thatwas gathering clinical implant stabilityand survival data. It clearly shows adense bone formation around the peripheryof the implant in response tomicrostrains that occurred during a 20-month period of normal clinical function.Restoring and functionally loadingthe implant involves stimulatingthe bone surrounding the dental implant,which should lead to a gradualincrease in the density of the bone-implantcomplex. The concept of ''progressiveloading'' capitalizes on thisphysiological response to increase thebone density and improve the ability ofthe implant to withstand functionalstresses and promote long-term clinicalsurvival.This response, however, does notoccur to the same degree for all implantsin all bone densities as shownby PTVs recorded for each bone densityover time (Table 2, Figure 2D). Thedenser the bone surrounding the implantsite at the time of implant placement,the greater the contact betweenthe implant surface and the trabecularbone. During loading, the functionalmicrostrains will stimulate the trabecularbone. If this falls within a physiologicallyacceptable range for thatbone density, the bone responds by increasingits density.5 Roberts20 has referredto this response as microremodeling.The extent of this favorablebone response for each bone density isreflected in the PTVs recorded over the48 months. Favorable bone responseover time is indicated by the PTVs becomingmore negative, indicating anincrease in the rigidity of the bone-implantcomplex.The most dense BQ (BQ-1) appearsto reach an optimal PTV between 6and 12 months (Table 2) after uncovering.The mean PTV for BQ-1 was24.3 PTVs. BQ-2 is less dense thanBQ-1 and had a mean PTV of 23.6PTVs for all evaluations during the 48months. Stability of the bone-implantcomplex in BQ-2 reached an optimalPTV over a slightly longer period ofFIGURE 2. (A) Periotest instrument: The plunger rod from the handpiece is positioned slightly above the soft tissue, and the Periotestis activated. (B) Postmortem specimen: The implant is a titanium alloy and was loaded clinically for a period of about 20 months. Notethe dense cortical bone at the crest of the specimen and surrounding the dental implant around most of its periphery. This dense layerof bone can be explained by The Carter Hypothesis, which states that bone responds to loading within normal physiological limits byforming increased density of bone. This increase in bone density occurs over a period of time and is documented by the changes inthe PTVs recorded for each bone density at each follow-up visit. Roberts20 refers to this as microremodeling of bone. (C) All implantsplaced: Mean Periotest Value (MPTV); confidence interval (CI) 5 95% for Periotest Values (PTVs). For each follow-up visit: At 3 months,MPTV 5 23.21; at 6 months, MPTV 5 23.06; at 12 months, MPTV 5 23.22; at 18 months, MPTV 5 23.40; at 24 months, MPTV 523.40; at 36 months, MPTV 5 23.33; and at 48 months, MPTV 5 23.21. Differences are not statistically significant. (D) Changes inPTVs over time for each of the 4 bone densities. CI 5 95% for PTVs. The 95% CIs are shown above for each of the visits and for eachBone Quality (BQ). BQ-1 is shown in red. At 3 months after uncovering, the mean is about 23.8 PTVs (rigid), and it gradually decreasesover time to about 24.5 PTVs (more rigid) at 48 months. BQ-2 is shown in green. At 3 months, the mean is about 23.5 PTVs (rigid),which also gradually decreases over time to 23.8 PTVs but at a slower rate than the increased in rigidity noted for BQ-1. Dark bluerepresents BQ-3. At 3 months, the mean is about 23.2 PTVs, which appears to become less rigid until the mean at 48 months is about2.8 PTVs. BQ-4 is shown in pink. At 3 months, after uncovering, the mean is about 22 PTVs and remains around 22 over the 48-month period.time. The mean PTV recorded for BQ-3over the 48-month period was 22.8PTVs. The optimal PTV for BQ-3 wasreached between 6 and 18 months. Thechanges in the PTVs over time do notsuggest a major increase in the densityof the bone surrounding the implant orthat the stability of bone-implant complexis decreasing. The PTVs for BQ-4are significantly less negative thanthose of the other bone densities,which suggests that the bone-implantcomplex does not improve (PTVs becomemore negative) with any appreciableamount and may, in fact, beslightly worsening (PTVs becomemorepositive) during long-term functionalloading. The optimal stability is evidentbetween 9 and 18 months. Thedifferences in the mean PTVs (stability)is statistically significant for each of thebone densities (Figure 2D).Harold F. Morris et alCONCLUSIONSThe conclusions that one can drawfrom these results in relation to thegoals of this study are the following:What PTVs would suggest that theimplant is integrated? PTVs for implantsthat appear to be clinically osseointegratedfall within 24 (very stable) and22 (stable and functional). This rangeis more critical than the range of 24 toJournal of Oral Implantology 267BONE DENSITY AFTER IMPLANT UNCOVERY12 PTVs reported by Teerlinck.9 Anyimplant with PTVs more positive than22, should be viewed with some concern,because the bone-implant complexmay be marginal and the longtermprognosis for implant survivalmay be questionable. This is particularlytrue if the implant is placed inpoor bone density or subjected to afunctional overload.What are the changes within the boneimplantcomplex after loading? Threemonths after uncovering of the implants,in BQ-1 and BQ-2 there is ageneral decrease in the PTVs (PTVs becomemore negative) when the implantis exposed to the oral environment andafter loading of the prosthesis. This indicatesa positive response (bone densityincreasing) of the bone to clinicalloading. There is a less evidence of thisfavorable bone response in BQ-3 andBQ-4. BQ-3 appears to remain relativelyconsistent, whereas there is an indicationthat the bone-implant complexchanges very little if the implants arenot overloaded.What is the influence of bone densityon implant stability, and what changeswould be considered to be normal responses?There is a correlation between thebone density in this study and themean PTVs recorded for each bonedensity. As the bone density increases,the PTVs become more negative (indi- This is government-supported recatinga more rigid bone-implant com- search, and there are no restrictions onplex). The PTVs for the 48-month pe- its use. The results and opinions preriodfor BQ-1 range from 23.51 to sented are those of the authors and do24.79 with a mean of 24.34 PTVs; for not necessarily reflect the opinion ofBQ-2, the mean was 23.61 PTVs; for the Department of Veterans Affairs orBQ-3, the mean was 22.78 PTVs; and the Office of Dentistry.for BQ-4, the mean was 22.04 PTVs.After loading, the stability of implantsin BQ-1 continues to become more neg- 1. Sennery L, Roos J. Surgical deativeuntil a PTV of about 24 is terminants of clinical success of osreached.Implants in BQ-2 show similarchanges in stability, whereas implantsin BQ-3 tend to show no significantpositive or negative changes. 2. Rompen E, DaSilva D, HockersPTVs associated with implants in BQ-4tend to become slightly more positive,which suggests possible early breakdownmay be starting within the bone-268 Vol. XXIX/No. Six/2003implant complex as a result of overloading.Are these observations supported byhistological specimens? The histologicalstructure around the implant in thepostmortem specimen provides graphicevidence that the bone around theimplant responds favorably by increasingits density when subjected to physiologicallyacceptable levels of loading.This is seen when comparing the boneimmediately surrounding the implantwith the bone that is farther from theimplant.The Periotest device appears torepresent an instrument capable of detectingchanges in the bone-implantcomplex over time in large, well-controlledclinical studies. This instrumentmay also be of particular value in monitoringthe performance of implantsthat are immediately functionally loaded,provided that the implants are testednumerous times and with onlyshort intervals between the tests. Detectingearly signs of a breakdownwithin the bone-implant complex earlyenough to allow the necessary interventionwould be problematic, becausethis would require almost weekly testingto provide the number of datapoints necessary to demonstratetrends.ACKNOWLEDGMENTSREFERENCESseointegrated oral implants: a reviewof the literature. Int J Prosthodontics.1998;11:408-420.T, et al. Influence of implant design onprimary fit and stability: an RFA andhistological comparison of MkIII andMkIV Branemark implants in the dogmandible. Appl Osseointegration Res.2001;2:9-11.3. Friberg B, Sennerby L, GrondahlK, Bergstrom C, Back T, Lekholm U.On cutting torque measurements duringimplant placemen: a 3-year clinicalprospective study. Clin Implant DentRelat Res. 1999b;1:75-83.4. Friberg B, Sennerby L, MeredithN, Lekholm U. A comparison betweencutting torque and resonance frequencymeasurements of maxillary implants.A 20-month study. Int J OralMaxillofac Surg. 1999a;28:297-230.5. Jensen OT. 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