Background: Although many authors have reported the use of root surface biomodification (RSB), the clinical outcomes in terms of root coverage are still unclear, as a number of biomodifier agents have been used in combination with various periodontal plastic surgical techniques. In this review we aim to evaluate the efficacy of RSB in root coverage and its impact on the outcomes.
Methods: A search of MEDLINE and Cochrane databases was carried out along with 2 manual searches. A combination of specific terms was used to identify relevant studies that met well-defined inclusion and exclusion criteria. Clinical attachment level, probing depth and percentage root coverage after treatment were among the results expected to be reported in the included articles.
Results: A total of 10 articles were identified and data were extracted. Only 6 met the inclusion criteria. Among these 6 studies, citric acid, ethylenediaminetetraacetic acid and laser therapy were used as RSB agents and free gingival graft, subepithelial connective tissue graft plus coronally advanced flap and semilunar coronally respositioned flap were the surgical approaches to root coverage treatment. Baseline and outcome data were analyzed and compared.
Conclusion: RSB provided no additional benefit in terms of the evaluated clinical parameters. Within the limitations of this review, we found no evidence to support the use of RSB prior to root coverage treatment.
Gingival recession is characterized by displacement of the gingival margin apically from the cemento-enamel junction resulting in root surface exposure.1 A significant proportion of the adult population is affected by this alteration,2-4 which may lead to esthetic concerns and complaints of hypersensitivity.5 Local trauma, anatomic factors and inflammatory conditions are the main causes of gingival recession.6,7
Several surgical approaches can be used to achieve root coverage. Laterally8,9 and coronally advanced flaps,10 free11,12 and subepithelial connective tissue grafts,13 guided tissue regeneration14 and combined techniques with variants15 have resulted in various rates of success. Regardless of technique, the ultimate goal is complete root coverage, and attempts have been made to increase the success rate and predictability of various techniques.16,17
Some authors suggest that root surface biomodification (RSB) with chemical agents, in conjunction with scaling and root planing, improves gingival attachment.18 These agents remove the smear layer, exposing collagen fibres on the dentin matrix and eliminating cytopathic substances that inhibit human gingival fibroblast growth.19 Citric acid,8,9,11,12,20 tetracycline,13 sodium hypochlorite9 and ethylenediaminetetraacetic acid (EDTA)21,22 are the main substances used; more recently, lasers23,24 have also been employed.
Despite the variety of agents, reviews have not shown a significant improvement in root coverage with the use of RSB.17,25,26 However, such studies have compared specific biomodifier agents and a limited number of techniques; none has compared surgical approaches with various RSB protocols. In addition, although these reviews have suggested that RSB is irrelevant, none had RSB assessment as a primary objective.
This study aimed to review the literature systematically to answer the question: does RSB have any positive or negative effect when used before root coverage procedures? We followed the approach outlined in the Cochrane Collaboration's Handbook27: specification of the problem (see above); formulation of a plan to conduct a literature search using specific index terms and retrieve publications; and interpretation of the evidence found in the literature retrieved.
Material and Methods
The search for relevant studies to be included in this review was carried out in 3 steps.
On 30 March 2011, MEDLINE was searched for entries since 1 January 1966. The search was limited to randomized controlled trials, published in English, in humans over 19 years of age, with an available abstract (Table 1). On the same day, the Cochrane Central Register of Controlled Trials was consulted using the following strategy: "Gingival recession" [search all text] AND "Root coverage" [search all text]. Articles appearing in both database searches were considered only once. To ensure the widest possible search, the indexing terms were used as both MeSH terms and free text in the MEDLINE search, and the truncation symbol * was used in the Cochrane Library search.
To identify studies not found in the databases search, issues of the following journals, published between January 2000 and December 2010, were searched manually: Journal of Periodontology, Journal of Clinical Periodontology, International Journal of Periodontics and Restorative Dentistry, and Journal of Periodontal Research.
In addition, the reference lists of the studies identified in the online and manual searches described above were also checked. During this search, an effort was made to identify titles containing words suggesting root coverage approaches, such as coronally or laterally repositioned flaps, semilunar coronally repositioned flap, subepithelial connective tissue graft and other surgical techniques; and words suggesting an RSB technique, such as EDTA, citric acid and tetracycline.
Abstracts or unpublished studies were not included. (The literature search is summarized in Fig. 1).
To be included in this review, the study had to meet the following criteria, which were considered during all 3 steps of the search.
- Inclusion criteria: Randomized controlled trials in systemically healthy human nonsmokers; patients with Miller's class I or II gingival recession or deeper than 3 mm but without interdental bone loss; published in English; presenting any modality of RSB in the test group; and including baseline data and final measurements of recession.
- Exclusion criteria: Studies in animals; lacking baseline–outcome comparisons; with insufficient data; with more than one variable in addition to RSB; and case reports, book chapters and narrative reviews because of their weaker clinical evidence.
Study Analysis and Data Extraction
Abstracts of the selected articles were read by both authors independently. The full text was ordered for all studies appearing to meet the inclusion criteria, for studies for which an abstract was considered relevant by at least 1 author and when the title, keywords and abstract contained insufficient information to make a decision.
Reading of relevant studies and quality evaluation28 were carried out independently by both authors to assess their suitability for this review. A study was considered good when it met all the criteria and fair when it did not meet all criteria but was judged to have no fatal flaw that would invalidate its results.28 Disagreements between the authors were resolved through discussion of the study's design and characteristics to reach a consensus on inclusion or exclusion. Articles were excluded if agreement could not be reached.
Data from the included articles were extracted with the aid of a protocol sheet designed especially for this study. They included assessment of variables, such as the extent of recession before and after surgery, probe depth, root sensitivity, percentage of coverage and increase in keratinized mucosa.
Literature Search and Study Characteristics
The MEDLINE search yielded 8 titles and abstracts; the Cochrane search did not produce any different studies. From these, 5 articles were deemed to meet the inclusion criteria and were read in full; 4 were considered relevant after data extraction and interpretation.
The manual searches resulted in 8 additional abstracts: 5 were selected, read in full and their data extracted; of these 2 were considered relevant.
Thus, 6 studies met the inclusion–exclusion criteria after a full reading (Table 2). The other 4 studies9,12,20,29 were excluded because they provided no information about recession characteristics, did not refer to Miller30 classifications and lacked sample data.
*Good = meets all criteria; fair = does not meet all criteria but has no fatal flaw that would invalidate its results.
Note: EDTA = ethylenediaminetetraacetic acid; Er:YAG = erbium-doped yttrium aluminium garnet; Nd:YAG = neodymium yttrium aluminium garnet; SE + CAF = subepithelial connective tissue graft associated with coronally advanced flap.
Of the 6 included studies, semilunar coronally repositioned flap was used in 1,21 subepithelial connective tissue graft associated with coronally advanced flap (SE + CAF) was performed in 45,8,23,24 and free gingival graft was used in 1.11 Regarding RSB in the test group, citric acid was used in 2 studies8,11; EDTA 24% with different application methods in 221,22; and lasers with 2 different protocols in 2.23,24 All 6 studies included a 6-month follow-up.
None of the included studies reported any additional benefit from RSB. Furthermore, in 2 situations,21,23 the intervention in the test group had a negative impact on the treatment outcome.
Citric acid and free gingival graft11: The range of coverage for the control and test groups was 39–94% and 53–94%, respectively. Mean coverage was 66% and 74%, respectively. No significant difference was found between pre- and post-operative measures of recession, probing depth, amount of keratinized tissue and percentage root coverage.
Citric acid and SE + CAF8: Treatment produced a reduction in recession height (2.79 ± 0.79 mm for the control group and 2.56 ± 0.73 mm for the test group) and width (3.74 ± 1.19 for control group and 3.50 ± 0.73 mm for test group), an increase in keratinized tissue (2.47 ± 1.6 mm for control group and 2.3 ± 1.2 mm for test group) and no significant change in probing depth (−0.16 ± 0.06 mm for control group and −0.13 ± 0.81 mm for test group).
Thus, there were no statistically significant differences between groups.
EDTA and SE + CAF22: There were no statistically significant differences between the control and test groups for pocket depth, increase in level of clinical attachment (4.1 mm for control group and 4.0 mm for test group) or root coverage (97.5% and 97.1%, respectively).
EDTA and semilunar coronally positioned flap21: Control and test groups showed 90.1% and 70.2% average root coverage and 66.7% and 40.0% complete root coverage, respectively. The control group showed a significant increase in width of the keratinized mucosa and a greater reduction in recession width and height. Root sensitivity was experienced by 9 patients before surgery and remained in 3 test group patients after conclusion of treatment. Thus, the use of EDTA negatively affected root coverage.
Nd:YAG laser and SE+CAF23: Both groups showed improvement in recession dimensions and clinical attachment levels. However, the control group showed greater reduction in recession depth and width. Similarly, average root coverage was 77% in the control group and 33% in the test group, and complete coverage was 65% and 18%, respectively. Thus, laser therapy negatively affected the results of the treatment.
Er:YAG laser and SE+CAF24: There were no significant differences between groups. Root coverage and gain in clinical attachment levels were achieved. Average root coverage was 86% and 80% and complete coverage was 67% and 75%, for the control and test groups, respectively. Thus, RSB using the Er:YAG laser does not enhance the results achieved with SE + CAF alone.
The importance of systematic reviews is well established, as they provide data for rational decision-making. The use of explicit methods allows assessment of what was done, limits bias and increases the reliability and accuracy of conclusions.27,31,32
This review assessed the results of available randomized controlled trials where RSB was used before root coverage; strict inclusion criteria were imposed to enable an unbiased analysis and a conclusion regarding the impact of this practice on treatment results.
Only studies dealing with patients with Miller class I and II recession were chosen, as this is the gingival recession classification30 most accepted and widespread; these are also the classes that show the highest success rates for root coverage. Some articles9,11,12,20 that did not refer to Miller classes, as this scheme had just been published at the time of the studies, might have been included; however, the lack of any description of recession characteristics, such as mean depth and the presence of interdental bone, resulted in their exclusion.
Some articles13,33 seemed relevant, but during evaluation of data, it was observed that different surgical approaches had been used for the control and test groups. Therefore, despite the use of RSB in test group, these articles were excluded as the additional variable affecting treatment outcome was beyond the scope of this review.
Similarly, studies including smokers were excluded because evidence of the negative impact of smoking on the success rates of periodontal therapy, including root coverage, has been well reported in the literature.34 These studies were also excluded for not presenting a description of recession characteristics.
Despite the widespread use of tetracycline for RSB,13 no studies dealing with this agent matched the selection criteria for our review.
Root sensitivity is usually the main complaint of patients who present with gingival recession.5 This sensitivity seems to increase when EDTA or citric acid is used in RSB. Surprisingly, only 1 of the analyzed studies21 reported data concerning root sensitivity before and after root coverage. After treatment, only patients submitted to RSB complained about root sensitivity, which could possibly be related to the demineralization promoted. The lack of this information from other studies limits comparisons among RSB protocols.
The absence of further post-operative complications may be related to the follow-up period. One study35 reported cervical root resorption 20 months after RSB with tetracycline, and the authors suggest that this long-term complication occurred as a result of the use of tetracycline. Similar conclusions were also found in another study.36 It is important to note that all studies included in this review included 6-month followup. We presume that long-term evaluations are necessary to provide sufficient data to reach proper conclusions concerning this issue.
Even though laser therapy has been widely studied in periodontics for pocket debridement, wound healing and in surgical approaches,37 no benefits were found from its bioestimulation38 in either of the 2 RSB protocols.23,24
The variety of RSB protocols (EDTA gel, EDTA in sterile water, citric acid at various concentrations and laser application) associated with surgical procedures, such as SE + CAF and semilunar coronally positioned flap, makes inter-study comparison impossible. The lack of consensus on the best protocol is pervasive.
Currently, several biomaterials, such as bone morphogenetic protein (BMP) and platelet-derived growth factor (PDGF), have shown promising results when applied to the root surface. In dogs, root surfaces conditioned with BMP stimulated cementum-like tissue formation and inhibited epithelial downgrowth.39 Good results were also achieved with PDGF, as it provided good root surface biocompatibility and had a positive effect on adhesion and growth of cultured fibroblasts on periodontally diseased surfaces.40,41 However, randomized controlled trials are required to confirm the benefits of these materials in terms of root coverage.
Preliminary results show that enamel matrix proteins, in combination with CAF — regardless of whether they are associated with connective tissue graft for the treatment of Miller class I or II gingival recession — produce good clinical results, with root coverage comparable or superior to other techniques. Further experimental studies on the dynamics of wound healing are needed to prove that enamel matrix proteins are really responsible for improving the percentage of regenerated versus repaired tissues in other techniques.42
Notwithstanding the probable benefits of biomaterials in promoting or inducing tissue regeneration, they are not usually considered RSB agents24 because they do not aim to remove a smear layer and expose the collagen matrix.19
Although other articles have discussed RSB, none has addressed it as the main variable. In fact, the variety of RSB agents used in clinical practice in combination with multiple mucogingival techniques makes the establishment of an accurate protocol difficult. In addition, recent studies23,24 have reported modalities, such as laser therapy, not studied for this purpose so far. As this subject is still being studied, subjected to clinical trials and used in periodontal practice, sometimes based on unverified beliefs, the doubt concerning the efficacy of RSB agents remains a subject of discussion.
Finally, based on this systematic review, it is evident that the use of RSB agents does not improve root coverage outcomes. Depending on the protocol adopted, RSB can even worsen the results of treatment. Thus, the use of any modality of RSB associated with root coverage should be reconsidered as no evidence of its efficacy is available in the literature unless new randomized controlled trials with well-designed methods present different conclusions.
Within the limitations of this systematic review, it is possible to conclude that all mucogingival surgery approaches used in the selected studies achieved a high rate of success in terms of root coverage; none of the RSB protocols reviewed produced any advantage to justify their use in root coverage procedures; and there is no evidence to support RSB prior to root coverage.
- American Academy of Periodontology. Glossary of Periodontal Terms. 4th ed. Chicago: American Academy of Periodontology; 2001. Available from: www.perio.org/resources-products/Perio-Terms-Glossary.pdf
- Kassab MM, Cohen RE. The etiology and prevalence of gingival recession. >J Am Dent Assoc. 2003;134(2):220-5.
- Rajapakse PS, McCracken GI, Gwynnett E, Steen ND, Guentsch A, Heasman PA. Does tooth brushing influence the development and progression of non-inflammatory gingival recession? A systematic review. J Clin Periodontol. 2007;34(12):1046-61. Epub 2007 Oct 22.
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- Kassab MM, Cohen RE. Treatment of gingival recession. J Am Dent Assoc. 2002;133(11):1499-506; quiz 1540.
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- Smith RG. Gingival recession. Reappraisal of an enigmatic condition and a new index for monitoring. J Clin Periodontol. 1997;24(3):201-5.
- Caffesse RG, De LaRosa M, Garza M, Munne-Travers A, Mondragon JC, Weltman R. Citric acid demineralization and subepithelial connective tissue grafts. J Periodontol. 2000;71(4):568-72.
- Oles RD, Ibbott CG, Laverty WH. Effect of root curettage and sodium hypochlorite treatment on pedicle flap coverage of localized recession. J Can Dent Assoc. 1988;54(7):515-7.
- Allen EP, Miller PD Jr. Coronal positioning of existing gingiva: short term results in the treatment of shallow marginal tissue recession. J Periodontol. 1989;60(6):316-9.
- Bertrand PM, Dunlap RM. Coverage of deep, wide gingival clefts with free gingival autografts: root planing with and without citric acid demineralization. Int J Periodontics Restorative Dent. 1988;8(1):64-77.
- Ibbott CG, Oles RD, Laverty WH. Effects of citric acid treatment on autogenous free graft coverage of localized recession. J Periodontol. 1985;56(11):662-5.
- Bouchard P, Nilveus R, Etienne D. Clinical evaluation of tetracycline HCl conditioning in the treatment of gingival recessions. A comparative study. J Periodontol. 1997;68(3):262-9.
- Al-Hamdan K, Eber R, Sarment D, Kowalski C, Wang HL. Guided tissue regeneration-based root coverage: meta-analysis. J Periodontol. 2003;74(10):1520-33.
- da Silva RC, Joly JC, de Lima AF, Tatakis DN. Root coverage using the coronally positioned flap with or without a subepithelial connective tissue graft. J Periodontol. 2004;75(3):413-9.
- Cairo F, Pagliaro U, Nieri M. Treatment of gingival recession with coronally advanced flap procedures: a systematic review. J Clin Periodontol. 2008;35(8 Suppl):136-62.
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- Polson AM, Proye MP. Effect of root surface alterations on periodontal healing. II. Citric acid treatment of the denuded root. J Clin Periodontol. 1982;9(6):441-54.
- Pini-Prato G, Baldi C, Pagliaro U, Nieiri M, Saletta D, Rotundo R, et al. Coronally advanced flap procedure for root coverage. Treatment of root surface: root planning versus polishing. J Periodontol. 1999;70(9):1064-76.
- Oles RD, Ibbott CG, Laverty WH. Effects of citric acid treatment on pedicle flap coverage of localized recession. J Periodontol. 1985;56(5):259-61.
- Bittencourt S, Ribeiro Edel P, Sallum EA, Sallum AW, Nociti FH Jr, Casati MZ. Root surface biomodification with EDTA for the treatment of gingival recession with a semilunar coronally repositioned flap. J Periodontol. 2007;78(9):1695-701.
- Kassab MM, Cohen RE, Andreana S, Dentino AR. The effect of EDTA in attachment gain and root coverage. Compend Contin Educ Dent. 2006;27(6):353-60; quiz 361.
- Dilsiz A, Aydin T, Canakci V, Cicek Y. Root surface biomodification with Nd:YAG laser for the treatment of gingival recession with subepithelial connective tissue grafts. Photomed Laser Surg. 2010;28(3):337-43.
- Dilsiz A, Aydin T, Yavuz MS. Root surface biomodification with an Er:YAG laser for the treatment of gingival recession with subepithelial connective tissue grafts. Photomed Laser Surg. 2010;28(4):511-7.
- Chambrone L, Lima LA, Pustiglioni FE, Chambrone LA. Systematic review of periodontal plastic surgery in the treatment of multiple recession-type defects. J Can Dent Assoc. 2009;75(3):203a-f.
- Cheng YF, Chen JW, Lin SJ, Lu HK. Is coronally positioned flap procedure adjunct with enamel matrix derivative or root conditioning a relevant predictor for achieving root coverage? A systemic review. J Periodontal Res. 2007;42(5):474-85.
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- Caffesse RG, Alspach SR, Morrison EC, Burgett FG. Lateral sliding flaps with and without citric acid. Int J Periodontics Restorative Dent. 1987;7(6):42-57.
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- Cizza N, Migues D. Progressive root resorption associated with the treatment of deep gingival recession. A clinical case. Int J Periodontics Restorative Dent. 2010;30(6):619-25.
- Ben-Yehouda A. Progressive cervical root resorption related to tetracycline root conditioning. J Periodontol. 1997;68(5):432-5.
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- Miyaji H, Sugaya T, Ibe K, Ishizuka R, Tokunaga K, Kawanami M. Root surface conditioning with bone morphogenetic protein-2 facilitates cementum-like tissue deposition in beagle dogs. J Periodontal Res. 2010;45(5):658-63. Epub 2012 Jun 10.
- Belal MH, Watanabe H, Ichinose S, Ishikawa I. A time-dependent effect of PDGF-BB on adhesion and growth of cultured fibroblasts to root surfaces. Oral Dis. 2006; 12(6):543-52.
- Gamal AY, Mailhot JM. The effect of local delivery of PDGF-BB on attachment of human periodontal ligament fibroblasts to periodontitis-affected root surfaces — in vitro. J Clin Periodontol. 2000;27(5):347-53.
- Berlucchi I, Francetti L, Del Fabbro M, Testori T, Weinstein RL. Enamel matrix proteins (Emdogain) in combination with coronally advanced flap or subepithelial connective tissue graft in the treatment of shallow gingival recessions. Int J Periodontics Restorative Dent. 2002;22(6):583-93.