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Jop060142 231.238

Effect of Autogenous Cortical BoneParticulate in Conjunction With EnamelMatrix Derivative in the Treatment ofPeriodontal Intraosseous DefectsLuigi Guida,* Marco Annunziata,* Salvatore Belardo,* Roberto Farina,† Alessandro Scabbia,†and Leonardo Trombelli† Background: The aim of the present study was to assess the additional clinical benefit of autogenous cortical bone particu-late (ACBP) when added to enamel matrix derivative (EMD),compared to EMD alone, in the treatment of deep periodontalintraosseous defects.
Methods: A total of 28 intraosseous lesions in 27 patients with advanced periodontitis were included in this controlledclinical trial and randomly assigned to the EMD group (14 de- fects) or to the EMD + ACBP group (14 defects). Immediately before surgery (baseline) and after 6 and 12 months, probing depth (PD), clinical attachment level (CAL), and gingival re- cession (REC) were recorded. Radiographic depth of the de- fect (DEPTH) was also measured at baseline and 12 months Results: At 6 and 12 months, PD and CAL significantly im- proved from baseline in both groups (P <0.000). No significant differences in terms of CAL gain and PD reduction were de- tected between groups. However, defect distribution according to CAL gain was significantly different between groups (P <0.05). DEPTH significantly decreased from baseline to 12 months in both groups (P <0.000); between-group differences were not significant. At 12 months, a significantly greater REC increase in the EMD group (1.1 – 0.7 mm) compared to the EMD + ACBP group (0.3 – 0.8 mm) was observed (P <0.05).
Conclusions: Both EMD and EMD + ACBP treatments led tial, which may potentially affect its re- to a significant improvement in clinical and radiographic pa- rameters at follow-up with respect to presurgery condition. The combined approach resulted in reduced post-surgery recession and increased proportion of defects with substantial CAL gain (‡6 mm). J Periodontol 2007;78:231-238.
erative treatment is addressed to deep,non-contained intraosseous defects.14 Autograft; enamel matrix proteins; periodontitis; randomized clinical trial; regeneration; treatment/surgery.
such as bovine porous bone mineraland demineralized freeze-dried bone al-lograft, has the potential to enhance the * Department of Odontostomatological, Orthodontic and Surgical Disciplines, Second University of Naples, Naples, Italy.
† Research Center for the Study of Periodontal Diseases, University of Ferrara, Ferrara, Italy.
EMD alone in terms of clinical attach-ment level gain15,16 or bone fill.17,18 Autogenous Bone Graft and EMD Versus EMD in Intraosseous Defects Among the different available graft materials, search Centre for the Study of Periodontal Diseases, autogenous bone graft meets several ideal character- University of Ferrara, Italy, from November 2003 istics, because it is potentially osteoinductive, bio- to May 2004. Adult patients with advanced chronic absorbable, low-cost, and easy to handle. It may be or aggressive periodontitis21 were consecutively en- speculated that the combined use of EMD and autog- rolled for this study. Informed consent was obtained enous bone graft could be advantageous, resulting in a from the patients after explaining the nature of the synergistic reconstructive effect. In this respect, the investigation being conducted. Informed consent autogenous bone graft may enhance the osteogenic and research protocol were institutionally approved.
potential of the healing site, act as an effective space- Exclusion criteria were: 1) systemic diseases that maintaining scaffold for bone regeneration, and limit contraindicated periodontal surgery; 2) medications the collapse of supracrestal soft tissues into the defect.
affecting periodontal status; 3) pregnancy or lacta- On the other hand, EMD may exert its biologic poten- tion; and 4) full-mouth plaque score22 and full-mouth tial at root level, inducing the biologic mechanisms bleeding score >20% at the time of surgical procedure.
underlying the periodontal regenerative process. How- Furthermore, third molars, teeth with Class III mobil- ever, limited data are available about the use of EMD ity, furcation involvement, inadequate endodontic treat- and autogenous bone graft in the treatment of intraos- Inclusion criteria were considered as follows: 1) at A histologic study19 on non-human primates has least one intraosseous defect in need of surgical treat- investigated this combined approach, reporting en- ment after initial periodontal treatment and reevalua- couraging results in terms of amount of new cemen- tion; 2) PD ‡6 mm; and 3) radiographic intraosseous tum and bone. Recently, we reported a consecutive series of cases where the effectiveness of a regenera- Patients were given a cause-related treatment con- tive procedure based on the preservation of supra- sisting of oral hygiene instructions and multiple scal- crestal soft tissue in association with an autogenous ing and root planing sessions, using both hand and cortical bone particulate (ACBP)-EMD combination ultrasonic instruments. At least 4 weeks elapsed from was investigated for the treatment of deep, 1- to 2-wall the completion of the non-surgical therapy until intraosseous defects.20 This approach resulted in sig- nificant clinical attachment gain and probing depth (PD) reduction and in a reduced marginal gingival re- Radiographs were performed at baseline and 1 year cession increase after 6 months of healing. To support after surgery. Radiographic measurements included the additional use of ACBP in conjunction with EMD, 1) the radiographic depth of the defect (DEPTH), mea- we designed a 12-month prospective randomized sured as the linear distance (in millimeters) from the clinical trial where the two procedures (EMD alone most coronal extension of the alveolar crest (as per- versus EMD + ACBP) were compared in the treatment pendicularly projected on the long axis of the tooth) of deep intraosseous periodontal defects.
to the most apical extension of the defect (i.e., wherethe periodontal ligament space was considered hav- ing a normal width);9 2) the radiographic defect fill (percentage), calculated as follows: (baseline DEPTH Two different approaches for the treatment of deep - 12-month DEPTH)/baseline DEPTH · 100; and 3) intraosseous defects were compared in a parallel the radiographic defect angle (ANGLE) at baseline, designed, randomized, controlled clinical trial. The determined in degrees as the angle formed between control group was treated by means of EMD‡ alone the lines that represent the root surface of the involved (EMD group), whereas the test group was treated with tooth and the bone defect surface.23 All radiographic EMD in association with an ACBP (EMD + ACBP measurements were performed by a single trained group). The same surgical procedures and the appli- and calibrated examiner (AS), who was masked as cation of EMD on the root surface were performed in both control and test groups. Grafting with ACBP was the only difference between the experimental groups.
The following clinical measurements were taken im- Clinical outcomes were measured at baseline and 6 mediately before surgery (baseline) and 6 and 12 months post-surgery: local plaque score (LPS) and lo- cal bleeding score (LBS), recorded dichotomously at Patients were recruited among those seeking care for surgical site as the presence or absence of supragin- periodontal disease at the Department of Odontosto- gival plaque and bleeding on probing, respectively; matological, Orthodontic and Surgical Disciplines,Second University of Naples, Italy, and at the Re- ‡ Emdogain Gel, Straumann, Basel, Switzerland.
Guida, Annunziata, Belardo, Farina, Scabbia, Trombelli clinical attachment level (CAL); PD; and marginal After flap reflection, all soft tissue was removed gingival recession (REC). Measurements were per- from the defect, and the root surface was scaled and formed at six sites (mesio-buccal, buccal, disto-buc- planed with hand and ultrasonic instruments. In all cal, mesio-lingual, lingual, and disto-lingual) around cases, the exposed root surfaces were conditioned the teeth presenting the defect; however, only the de- with 24% EDTA geli for 2 minutes. The defect was then fect-specific measurement presenting the highest thoroughly rinsed with saline to remove gel remnants.
CAL at the time of presurgery recordings was consid- For the EMD + ACBP group, an adequate amount of ered for the analysis. Measurements were performed cortical bone particulate was harvested from the buc- by trained and calibrated examiners (SB and AS) with cal cortical plate by means of a bone scraper.¶ The a manual sensitive probe (at approximately 0.3 N bone graft was collected from the surgical site adja- force) with 1-mm increments§ and rounded up to cent to the intraosseous defect. A first layer of EMD the nearest millimeter. Examiners were not masked was injected to condition the bone defect and the more apical portion of the root surface. ACBP was posi-tioned to fill only the intrabony component of the defect, avoiding any packing of the graft. Finally, a Intrasurgical measurements, recorded immediately second layer of EMD was injected to cover the grafted after defect debridement, included probing bone level, autogenous bone particles and to condition the por- as the distance from the cemento-enamel junction tion of the root surface coronal to the bone crest.
(CEJ) to the apical end of the defect; and intrabony Therefore, a ‘‘sandwich’’ technique was adopted to component of the defect, as the distance from the treat the defect (i.e., apical layer of EMD, ACBP, most coronal extension of the interproximal bone crest to the apical end of the defect.
For the EMD group, the EDTA-treated root surface and surrounding bony walls were conditioned with the amelogenin gel according to the manufacturer’s Two operators (LG and LT) performed all surgeries.
Each defect was randomly assigned to either EMD Finally, flaps were positioned at the presurgery group (14 defects) or EMD + ACBP group (14 defects).
level or slightly coronal to achieve primary closure After local anesthesia, buccal and lingual sulcular in- of the interdental area without any tension. Monofila- cisions were made and mucoperiosteal flaps were ele- ment non-resorbable 5-0 or 6-0# or polypropylene** vated. Maximum care was exercised to preserve the suturing material was used. Selection of the suturing marginal and interdental tissues. Flap design in the in- terdental area consisted of one of the following alterna- tives: 1) sulcular incisions with the split of buccal and The patients received systemic antibiotic therapy,†† lingual papilla;24 2) incision with the preservation of 2 g/day for 6 days, and 0.12% chlorhexidine mouth- the buccal papilla, according to the simplified papilla rinses,28 twice a day for 6 weeks. Mechanical tooth preservation technique;25 3) incision with the preser- cleaning was not allowed in the surgical area for the vation of the buccal papilla, according to the modified first 6 postoperative weeks. Sutures were removed papilla preservation technique;26 or 4) incision with at least 14 days following surgery. Patients were then the preservation of the lingual-palatal papilla, accord- placed on monthly recall visits, including professional ing to interproximal tissue maintenance procedure.27 tooth cleaning, during the first 6 months, and every 3 Selection of flap design was based on: 1) width of the months thereafter. Probing and subgingival instru- interdental space, evaluated as the distance from mentation was not performed £6-month reevaluation.
the CEJ of the tooth presenting the bone defect tothe CEJ of the adjacent tooth; 2) distance from the con-tact point or area to the bone crest, as radiographically assessed; 3) apico-coronal width of interdental kerati- Statistical software‡‡ was used for data analysis. Be- nized tissue in the area of intraosseous defect; and 4) cause no differences were observed whether the pa- location and morphology of the bone defect, as deter- tient or the defect was regarded as statistical unit, mined with bone sounding. The gingival tissue was in- we reported our data based on the number of defects.
cised at least one tooth mesial and distal to the defect Measurements from each group were expressed as site to provide access for visualization and instrumen-tation of the defect and, in the test group, for the follow- ing phase of bone harvesting. Vertical incisions were Micross, Meta C.G.M., Reggio Emilia, Italy.
placed mesial or distal to the treated defect, if they were # Gore-Tex Suture, W.L. Gore & Associates, Flagstaff, AZ.
considered necessary for better access or primary clo- ** Perma Sharp Suture, Hu-Friedy.
†† Augmentin, SmithKlineBeecham, Milan, Italy.
‡‡ NCSS-PASS, Number Cruncher Statistical Systems, Kaysville, UT.
Autogenous Bone Graft and EMD Versus EMD in Intraosseous Defects mean values – SD. The presence of any randomiza- All 27 patients completed the study, and complied tion imbalance between the two experimental groups with the 6- and 12-month reexaminations.
at baseline was tested by unpaired Student t test and x2 analysis. Within-group comparisons for outcome Incidence of LPS-positive defects was 21.4% at base- variables were performed by paired Student t test, line and remained unchanged (21.4%) at 12 months whereas between-group differences were evaluated in both groups (P >0.05). Incidence of LBS-positive by unpaired Student t test at 6- and 12-month obser- defects decreased from 71.4% at baseline to 7.1% at vation intervals. A power analysis indicated that 26 12 months in the EMD group (P <0.000), and from unpaired defects (13 in each group) would be suffi- 50% at baseline to 7.1% at 12 months in the EMD + cient to demonstrate statistical significance at the ACBP group (P <0.000). No statistically significant P <0.05 level with a power of 0.85. In our study, 14 differences were detected between groups in terms defects for each experimental group were treated.
of incidence of LPS- and LBS-positive defects at 6 Clinical and radiographic measurements at base- Study Population and Defect Characteristics line and 6 and 12 months are summarized in Table 2.
A total of 27 patients (13 men and 14 women, 30 At 6 months, CAL and PD significantly improved to 65 years old; mean age: 46.3 – 8.7 years) with from baseline (P <0.000) in both groups. The 12-month 28 intraosseous defects were selected and treated.
CAL and PD measurements did not significantly Twenty-six patients contributed one defect, one pa- change from the 6-month measurements, remain- tient contributed two defects. Fourteen defects in ing significantly improved with respect to baseline 14 patients were treated with EMD, 14 defects in 13 (P <0.000). In the EMD group, REC varied from patients were treated with EMD + ACBP. All defects 1.7 – 0.7 mm at 6 months to 2.1 – 0.9 mm at 12 showed a predominant 1- to 2-wall component. Mean months, whereas REC remained almost unchanged age in the EMD + ACBP and EMD groups was 44.1 – in the EMD + ACBP group. No significant differences 6.9 years and 48.4 – 9.9 years, respectively. There in CAL gain and PD reduction were detected between were seven females and two smokers in each group.
groups at 6 and 12 months. At 12 months, a signifi- An analysis of defect characteristics at baseline cantly greater REC increase in the EMD group com- revealed no significant differences between groups pared to the EMD + ACBP group was observed with respect to baseline REC (P <0.05). A significantly dif-ferent distribution of defects according to 12-month CAL gain was observed between groups (P <0.05)(Table 3): 50% of defects showed a CAL gain of ‡6 mm and 21% showed a CAL gain of 4 to 5 mm inthe EMD + ACBP group compared to 21% and 57%, DEPTH significantly decreased from baseline to 12 months in both groups (P <0.000). DEPTH gain was 4.3 – 2.4 mm corresponding to a radiographic defectfill of 64.8% – 24.1% for the EMD group, and 4.3 – 1.3 mm corresponding to a radiographic defect fill of 68% – 17.3% for the EMD + ACBP group. No signif-icant differences were detected between groups at 12 months (P >0.05). Defect distribution, according to DEPTH gain, was similar between groups (P >0.05;Table 4).
The clinical effect of EMD to achieve the reconstruc-tion of lost periodontal tissues has been extensively revised and confirmed. Available data from sys- tematic reviews10,12,29 indicate that all EMD re-constructive treatment produces a more favorable clinical improvement in hard and soft tissue param- I = incisors; C = canine; P = premolars; M = molars; PBL = probing bone eters of healing response (i.e., clinical attachment level; IBD = intraosseous component of the defect; NS = not significant(P >0.05).
gain, pocket reduction, and bone fill) compared to Guida, Annunziata, Belardo, Farina, Scabbia, Trombelli Clinical and Radiographic Measurements at Baseline and 6 and 12 Months (mean – SD) D0-6 = difference between baseline and 6 months; D0-12 = difference between baseline and 12 months; NS = not significant (P >0.05).
* P <0.05.
† P <0.01.
‡ P <0.000.
conventional open flap debridement procedure. How- ever, although all studies generally showed an addi- Defect Distribution According to CAL Gain tional benefit with the use of EMD, a high degree of variability in treatment outcomes (heterogeneity)was found in the included trials.29 This heterogeneity may be partly explained by differences in the patientand defect selection among studies. For instance, the use of a biomaterial with a gel-like consistency, such as EMD, in a non–self-supporting intraosseous defectmay result in a limited clinical outcome due to the col- lapse of the flap into the bone defect during the early healing phase, particularly in deep, non-containingintraosseous defects.14 These observations seem to * Significant difference between groups (P <0.05).
emphasize the clinical relevance to adapt the selec-tion of the reconstructive strategy to the anatomy ofthe treated area and the physical and biologic char- acteristics of the regenerative materials used.29,30 In this perspective, the present study was under- taken to evaluate whether and to what extent the ad- ditional use of ACBP in conjunction with EMD mayimprove the clinical effect of EMD alone when used in deep intraosseous defects, with a predominant1- to 2-wall component. The results indicate that both the EMD + ACBP and EMD procedures led to a statis- tically significant and clinically relevant CAL gain withrespect to presurgery condition, with more than 70% of the defects presenting a CAL gain of at least 4 mm for both treatment groups. No significant differences * No significant difference between groups.
were detected between treatment groups in terms of Autogenous Bone Graft and EMD Versus EMD in Intraosseous Defects average CAL gain, PD reduction, and defect bone fill.
benefit derived from the additional use of ACBP. Pre- However, EMD + ACBP treatment significantly in- vious reports where a similar surgical approach was creased the proportion of defects with substantial associated to EMD treatment resulted in comparably CAL gain (‡6 mm) and determined a smaller postop- erative REC increase with respect to EMD alone.
A significantly smaller REC increase was found in Recent studies indicated that the combination of the EMD + ACBP group compared to the EMD group EMD with bone substitutes, such as bovine porous at the 12-month reevaluation. ACBP may efficiently bone mineral and demineralized freeze-dried bone al- have sustained the soft tissue healing, avoiding col- lograft, has the potential to enhance the reconstruc- lapse into the bony defect, during the tissue matura- tive outcome compared to EMD alone in terms of tion phase. This result compared to those stemming clinical attachment level gain15,16 or bone fill.17,18 from clinical trials where EMD treatment was used The choice to use ACBP in addition to EMD was sup- in conjunction with slowly bioabsorbable biomate- ported by data from a randomized controlled trial rials, such as bovine porous bone mineral.16,17 These showing a greater CAL gain after an access flap pro- observations seem to suggest the additional use of cedure with autogenous bone graft compared to an ACBP in deep, non–self-supporting intraosseous de- access flap procedure alone, for the reconstructive fects, especially in areas of the dentition where the treatment of deep intraosseous defects.31 Further- esthetic outcome is considered of paramount im- more, we previously showed that the adjunctive ap- plication of ACBP with EMD resulted in clinically Our results indicate that both EMD and EMD + significant attachment gain and PD reduction in deep ACBP reconstructive procedures result in comparable intraosseous defects, with a predominant 1- to 2-wall outcomes in terms of attachment gain and bone fill.
intraosseous component.20 In our study, the lack of However, defect distribution according to CAL gain substantial additional benefits observed in the EMD + significantly differed between groups. In particular, a ACBP group compared to EMD seems to confirm higher prevalence of defects showing a CAL gain of the biologic potential of EMD per se to support the ‡6 mm was observed in the EMD + ACBP group com- clinical reconstruction of the lost attachment appara- pared to the EMD group (Table 3). In contrast, defect tus, and to limit the additional application of an autog- distribution according to DEPTH gain was similar be- enous bone particulate to enhance the EMD-induced tween groups (Table 4). These data suggest that part of the defects in the EMD + ACBP group showed a CAL The observed values for CAL gain, PD reduction, gain greater than the corresponding DEPTH gain, and REC increase in the EMD group compared to whereas in EMD-treated defects CAL gain substan- some studies,9,14,16,32-34 whereas they differed from tially paralleled DEPTH gain. The presence of a graft others where less favorable outcomes had been ob- supporting supracrestal tissues during the healing served.35-39 The reason for these discrepancies may phase could explain this observation. However, be found in a wide range of predictors, including pa- whether and to what extent the additional use of ACBP tient selection, defect characteristics, maintenance to EMD may affect the wound healing dynamics phase, and surgical variables.39,40 In our material of deep periodontal defects compared to mere EMD the same surgical approach based on supracrestal application needs be clinically and histologically con- soft tissue preservation was used for both treatment firmed. In this respect, several histologic studies41-44 groups; the only investigated variable was the appli- in humans demonstrated the periodontal regenerative cation of ACBP to fill the intraosseous component of potential of the autogenous bone, leading to cemen- the defect. In all cases flap design and suture tech- tum and bone formation. In contrast, inconsistent his- nique were adequately selected with respect to the tologic results have been reported on the regenerative morphologic characteristics of the defect to preserve potential (i.e., presence and extent of newly formed an adequate amount of supracrestal soft tissue and bone and cementum) of EMD in the treatment of intra- achieve primary closure in the interdental area.
Primary closure eliminates or, to a greater extent, Two considerations about data analysis must be reduces the chances of post-surgical infection and made. First, among the 28 treated defects, four de- contamination of the blood clot and, possibly, the bi- fects were present in smoker patients. Due to the lim- ologic agent or the graft. Incomplete primary closure ited number of smokers in the study population, may be of particular concern when a non-supportive statistical analysis of treatment outcome between material, such as EMD, is used to reconstruct in smokers and non-smokers was not performed. Sec- toto the attachment apparatus, including alveolar ond, clinical examiners were not masked as to the bone.7,15 In this respect, proper soft tissue manage- surgical procedures, so that a potential bias in out- ment, leading to optimal EMD-induced wound healing come assessment cannot be completely excluded.
process, may partly account for the limited clinical However, it must be considered that the examiners Guida, Annunziata, Belardo, Farina, Scabbia, Trombelli were expert and rigorous clinicians, trained and cali- 12. Venezia E, Goldstein M, Boyan BD, Schwartz Z. The brated to ensure accuracy and reproducibility of clin- use of enamel matrix derivative in the treatment of periodontal defects: A literature review and meta-analysis. Crit Rev Oral Biol Med 2004;15:382-402.
13. Sanz M, Tonetti MS, Zabalegui I, et al. Treatment of intrabony defects with enamel matrix proteins or bar- With the limits of the present study, our data support rier membranes: Results from a multicenter practice- the clinical effectiveness of a regenerative procedure based clinical trial. J Periodontol 2004;75:726-733.
based on EMD application, either alone or in combi- 14. Froum S, Lemler J, Horowitz R, Davidson B. The use of enamel matrix derivative in the treatment of peri- nation with an ACBP, in the treatment of deep intraos- odontal osseous defects: A clinical decision tree based seous defects. The combined EMD + ACBP procedure on biologic principles of regeneration. Int J Periodon- led to a reduced post-surgery recession and increased tics Restorative Dent 2001;21:437-449.
proportion of defects with substantial CAL gain (‡6 15. Lekovic V, Camargo PM, Weinlaender M, Nedic M, Aleksic Z, Kenney EB. A comparison between enamelmatrix proteins used alone or in combination with bo-vine porous bone mineral in the treatment of intrabony periodontal defects in humans. J Periodontol 2000;71:1110-1116.
This study was partly supported by a Research Grant 16. Zucchelli G, Amore C, Montebugnoli L, De Sanctis M.
of the Second University of Naples, Naples, Italy, and Enamel matrix proteins and bovine porous bone min- the Italian Ministry of Education, University and Re- eral in the treatment of intrabony defects: A compar- search Grant ex 60%, Research Center for the Study ative controlled clinical trial. J Periodontol 2003;74: of Periodontal Diseases, University of Ferrara, Fer- 17. Velasquez-Plata D, Scheyer ET, Mellonig JT. Clinical comparison of an enamel matrix derivative used aloneor in combination with a bovine-derived xenograft for the treatment of periodontal osseous defects in 1. Hoffman RL. Formation of periodontal tissues around humans. J Periodontol 2002;73:433-440.
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48. Majzoub Z, Bobbo M, Atiyeh F, Cordioli G. Two 37. Parodi R, Liuzzo G, Patrucco P, et al. Use of Emdogain patterns of histologic healing in an intrabony defect in the treatment of deep intrabony defects: 12-months following treatment with enamel matrix derivative: A clinical results. Histologic and radiographic evalua- human case report. Int J Periodontics Restorative Dent tion. Int J Periodontics Restorative Dent 2000;20:584- 38. Minabe M, Kodama T, Kogou T, et al. A comparative Correspondence: Dr. Luigi Guida, Department of Odon- study of combined treatment with a collagen mem- tostomatological, Orthodontic and Surgical Disciplines, brane and enamel matrix proteins for the regeneration Second University of Naples, Via L. De Crecchio 6, 80138 of intraosseous defects. Int J Periodontics Restorative Naples, Italy. Fax: 39-81-5665524; e-mail: luigi.guida@ 39. Tonetti MS, Lang NP, Cortellini P, et al. Enamel matrix proteins in the regenerative therapy of deep intrabony Accepted for publication September 8, 2006.


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