Periodontology 2000, Vol. 68, 2015, 308–332 Printed in Singapore. All rights reserved
© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
PERIODONTOLOGY 2000
Clinical concepts for regenerative therapy in furcations MARIANO SANZ, KARIN JEPSEN, PETER EICKHOLZ & SØREN JEPSEN
Description of the furcation lesion The furcation area represents a unique periodontal site with specific anatomic and pathogenic characteristics and with important clinical and therapeutic implications. The progression of chronic inflammation during periodontitis may affect the bifurcation or trifurcation of multirooted teeth. The furcation area has a complex anatomic morphology, which makes it difficult, if not impossible in some instances, to debride this area properly during routine periodontal instrumentation, as well as to clean it during routine home-care practices, when the root surfaces have been colonized by the subgingival biofilm. Furcation involvement is therefore an important complication in the progression of periodontitis and is a risk factor for progression of further attachment loss and, at the same time, reduces the efficacy of periodontal therapy. In fact, long-term retrospective studies assessing the maintenance of periodontal health after periodontal therapy have found higher tooth mortality and a more compromised prognosis for teeth with furcation involvement (72, 110) and prospective clinical trials have provided evidence for the reduced efficacy of periodontal therapies in multirooted teeth with furcation involvement (85, 86, 145). The furcation lesion has been defined by the American Academy of Periodontology as ‘the pathologic resorption of bone in the anatomic area of a multirooted tooth where the roots diverge’. It is the anatomic location of the pathology that defines the lesion and hence it is essential to have a good knowledge of the anatomy to ensure the correct diagnosis and optimal treatment planning and to understand how these anatomic factors may influence the etiology and pathogenesis of this lesion. The furcation area can be divided into three parts: (i) the roof; (ii) the surface immediately coronal to the root separation (flute);
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and (iii) the area of root separation (1). Although there are many individual variations, there are specific anatomic features depending on the tooth affected. For example, maxillary molars usually have three roots (a mesiobuccal root, a distobuccal root and a palatal root), whereas mandibular molars normally have two roots (a mesial root and a distal root) and maxillary premolars usually have two roots (one buccal root and one lingual root). Further, the buccal furcation entrance in the first mandibular molar is located close to the cemento–enamel junction, whereas it is more apically situated in the second mandibular molars. Similarly, the mesial–palatal furcation entrance of the maxillary first molar is located close to the palatal third of the tooth, whereas the distal–palatal furcation is in the middle portion of the tooth (65). Other morphological factors may also contribute to the pathogenesis of the lesion. The root trunk, being part of the root complex that extends between the cemento–enamel junction and the furcation entrance, is usually shorter on the buccal aspect of first and second mandibular molars, compared with the lingual aspect (106). This length has important implications because a molar with a short root trunk will develop a furcation lesion earlier, whereas, in contrast from a therapeutic point of view, it will be easier to instrument a furcation lesion if it is located more coronally (16, 74, 76). The presence of root concavities in the furcation area is also a frequent finding. They are present in all two-rooted maxillary premolars, in most mandibular roots and in many maxillary roots (15). These concavities add to the difficulty of adequately debriding the root surfaces during the treatment of these lesions. Another important factor, which enables access for mechanical debridement in the treatment of this lesion, is the diameter of the furcation entrance. About half of the furcation entrances
Regenerative therapy in furcation defects
has a diameter of 0.05). The number of Class II furcations that were closed or converted to Class I was greater for enamel matrix derivative plus demineralized freeze-dried bone allograft plus guided tissue regeneration. Another recent randomized clinical trial on proximal Class II furcation defects on maxillary molars compared the combination of enamel matrix derivative plus hydroxyapatite/beta-tricalcium phosphate with hydroxyapatite/beta-tricalcium phosphate alone in 30 patients with 30 defects (133). Horizontal bone level gains after 6 months were 1.7 1.3 mm for both treatment modalities. The enamel matrix derivative plus hydroxyapatite/beta-tricalcium phosphate group showed seven closed furcations and seven conversions to Class I versus four closed furcations and 10 conversions to Class I in the hydroxyapatite/beta-tricalcium phosphate group (P > 0.05).
Class III furcation involvement One case-series study evaluated the treatment of Class III mandibular furcation defects by the use of enamel matrix derivative alone or in combination with a bioresorbable membrane (41). Nine patients with a total of 14 Class III mandibular furcation defects were assigned to one of three groups: (i) enamel matrix derivative in four defects; (ii) guided tissue regeneration in three defects; and (iii) enamel matrix derivative and guided tissue regeneration in seven defects. None of the treatments resulted predictably in complete healing of the defects and there was no obvious difference between the various treatment modalities. At 6 and 12 months, partial closure of the Class III involvements had occurred in six of the 14 treated furcations. The remaining teeth still presented through-and-through
Regenerative therapy in furcation defects 6
B
70
2 LE-RM LM-RE 0
50 40 30 20 10
–2
2 0 4 6 Change of horizontal depth under membrane treatment (mm)
Emdogain® Membrane
n = 30
50 40
n = 16
30
n = 16
n = 12 n = 10
20 10 0
n=6
None
n=4 Moderate Little Postoperative pain
D
n = 11
n=4
n=3 0
I II Furcation class
50 40
Membrane n = 17
n = 16
n = 14
30
III
Emdogain®
n = 21 Number of patients (%)
70 60
Number of patients (%)
n=9
n=8
n=1 0
–2
C
Emdogain® Membrane
n = 27 n = 27
60
4 Number of detects (%)
Change of horizontal depth under Emdogain® treatment (mm)
A
n = 15
20 n=6 10
n=3
n=4
n=2 Strong
0
None
Moderate Little Postoperative swelling
Strong
Fig. 4. (A) Treatment according to treatment scatterplot for 45 individual pairs of mandibular buccal Class II furcation defects treated with enamel matrix derivative (Emdogain) or guided tissue regeneration (n = 45 patients available for re-entry). Change (mm) in horizontal furcation depth (surgery compared with re-entry) is shown. (B) Distribution of furcation class at 14 months following treatment of mandibular buccal class II furcations with enamel matrix derivative (Emdogain) or guided tissue
regeneration. (C) Postoperative pain (1 week postsurgery) following treatment with enamel matrix derivative (Emdogain) or guided tissue regeneration (n = 48 patients). (D) Postoperative swelling (1 week postsurgery) following treatment with enamel matrix derivative (Emdogain) or guided tissue regeneration (total n = 48 patients) (83). Reproduced with permission of American Academy of Periodontology. LE-RM: left EMD, right membrane; LMRE: left membrane, right EMD.
furcation defects. Within the limits of this case series, and taking into account the limited number of patients and furcation involvements in each treatment group, it was concluded that the use of enamel matrix derivative alone or in combination with guided tissue regeneration did not result in predictable regeneration of mandibular Class III furcation defects.
Conclusions and recommendations
Long-term results No long-term data (> 3 years) are available for the effects of enamel matrix derivative application in the regenerative therapy of furcation defects.
An evaluation of the scientific literature on the regenerative therapy of furcation lesions may warrant the following conclusions. An abundance of studies and several systematic reviews with meta-analyses have demonstrated efficacy of guided tissue regeneration therapy for the regenerative treatment of furcation defects. Guided tissue regeneration therapy generally results in significantly higher horizontal defect fill (i.e. horizontal probing attachment level and/or horizontal probing bone level gain) in Class II furcation involvement of mandibular and maxillary molars when compared with open flap debridement. This
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Sanz et al. A
D
B
E
C
F
G
therapy has demonstrated good clinical outcomes in buccal sites of mandibular and maxillary molars, but is unpredictable at interproximal sites. Complete furcation closure is not either a predictable outcome. There is only limited information for lingual sites. Class III furcation defects cannot be improved predictably by guided tissue regeneration procedures and therefore this therapy is not indicated in the treatment of these lesions. There are no significant differences in clinical outcomes when biodegradable membranes are compared with nonresorbable barrier membranes. Some bone grafts/bone substitutes may enhance the outcome of guided tissue regeneration therapy in furcations. Limited data are available on the effects of enamel matrix derivative application in the regenerative therapy of furcation involvement and thus no metaanalyses have been performed. Although enamel matrix derivative has demonstrated clinical improve-
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Fig. 5. (A) Periodontal measurements at baseline tooth no. 26. Recession: buccal to the cemento– enamel junction: 3 mm. Probing depth mesial = 2 mm, furcation class II; probing depth buccal = 6 mm; probing depth distal = 4 mm. Note minimal keratinized tissue at the furcation site. (B) Intra-operative view. Furcation class II (horizontal probing bone level = 6 mm), debrided root surface and cervical enamel projections removed. Placement of an orthodontic button to facilitate crown-attached sutures (61). Flap design: intrasulcular incision/no vertical release, mucoperiostal flap, papillae de-epithelialized, periosteal split in the vestibule. (C) Application of enamel matrix derivative after root surface conditioning with 24% EDTA for removal of the smear layer (83). (D) Application of xenogeneic bone mineral into the furcation defect (160). (E) Connective tissue graft from the palate placed onto the root surface and over the furcation area, secured by resorbable sling sutures (14). (F) Coronally advanced flap secured with crown-attached sutures (61). (G) Clinical and radiographic view at baseline, and 12 and 24 months after periodontal-regenerative surgery. Complete resolution of the furcation defect and recession coverage.
ments in the treatment of buccal Class II furcation defects in mandibular molars, the complete closure of the furcation lesion is achieved only in a minority of the cases. Similarly, there is evidence indicating that the use of enamel matrix derivative in proximal furcations of maxillary molars might result in conversion of Class II furcation involvements to Class I, which may improve the individual tooth prognosis. The current evidence, however, does not support the use of enamel matrix derivative for the treatment of lingual Class II mandibular molar furcation defects. With regard to patient-centered outcomes, one multicenter trial in buccal mandibular Class II furcation defects found less patient morbidity following enamel matrix derivative treatment compared with guided tissue regeneration therapy. In selecting the regenerative therapy, careful case evaluation is important because the factors associated with the lesion, such as the defect size, the pres-
Regenerative therapy in furcation defects
ence of proximal bone to the level of the fornix, the thickness/biotype of the gingiva and the amount of keratinized tissue, have shown to clearly influence therapeutic outcome. Furthermore, similar to regenerative treatment of non-furcation periodontal lesions, patient-related factors, such as oral hygiene and smoking, must be taken into consideration. Promising pre-clinical data from furcation regeneration studies in experimental animals are available for growth factor- and differentiation factor-based technologies, but limited data are available from human clinical studies. Although cell-based therapies have received considerable attention in regenerative medicine, their experimental evaluation in the treatment of periodontal furcation lesions is at a very early stage of development. In summary, the indications and the limitations for currently available treatment modalities for the regeneration of furcation defects seem well established. In the future, new regenerative treatment modalities are clearly needed to improve the predictability of complete resolution of furcation defects.
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© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
PERIODONTOLOGY 2000
Clinical concepts for regenerative therapy in furcations MARIANO SANZ, KARIN JEPSEN, PETER EICKHOLZ & SØREN JEPSEN
Description of the furcation lesion The furcation area represents a unique periodontal site with specific anatomic and pathogenic characteristics and with important clinical and therapeutic implications. The progression of chronic inflammation during periodontitis may affect the bifurcation or trifurcation of multirooted teeth. The furcation area has a complex anatomic morphology, which makes it difficult, if not impossible in some instances, to debride this area properly during routine periodontal instrumentation, as well as to clean it during routine home-care practices, when the root surfaces have been colonized by the subgingival biofilm. Furcation involvement is therefore an important complication in the progression of periodontitis and is a risk factor for progression of further attachment loss and, at the same time, reduces the efficacy of periodontal therapy. In fact, long-term retrospective studies assessing the maintenance of periodontal health after periodontal therapy have found higher tooth mortality and a more compromised prognosis for teeth with furcation involvement (72, 110) and prospective clinical trials have provided evidence for the reduced efficacy of periodontal therapies in multirooted teeth with furcation involvement (85, 86, 145). The furcation lesion has been defined by the American Academy of Periodontology as ‘the pathologic resorption of bone in the anatomic area of a multirooted tooth where the roots diverge’. It is the anatomic location of the pathology that defines the lesion and hence it is essential to have a good knowledge of the anatomy to ensure the correct diagnosis and optimal treatment planning and to understand how these anatomic factors may influence the etiology and pathogenesis of this lesion. The furcation area can be divided into three parts: (i) the roof; (ii) the surface immediately coronal to the root separation (flute);
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and (iii) the area of root separation (1). Although there are many individual variations, there are specific anatomic features depending on the tooth affected. For example, maxillary molars usually have three roots (a mesiobuccal root, a distobuccal root and a palatal root), whereas mandibular molars normally have two roots (a mesial root and a distal root) and maxillary premolars usually have two roots (one buccal root and one lingual root). Further, the buccal furcation entrance in the first mandibular molar is located close to the cemento–enamel junction, whereas it is more apically situated in the second mandibular molars. Similarly, the mesial–palatal furcation entrance of the maxillary first molar is located close to the palatal third of the tooth, whereas the distal–palatal furcation is in the middle portion of the tooth (65). Other morphological factors may also contribute to the pathogenesis of the lesion. The root trunk, being part of the root complex that extends between the cemento–enamel junction and the furcation entrance, is usually shorter on the buccal aspect of first and second mandibular molars, compared with the lingual aspect (106). This length has important implications because a molar with a short root trunk will develop a furcation lesion earlier, whereas, in contrast from a therapeutic point of view, it will be easier to instrument a furcation lesion if it is located more coronally (16, 74, 76). The presence of root concavities in the furcation area is also a frequent finding. They are present in all two-rooted maxillary premolars, in most mandibular roots and in many maxillary roots (15). These concavities add to the difficulty of adequately debriding the root surfaces during the treatment of these lesions. Another important factor, which enables access for mechanical debridement in the treatment of this lesion, is the diameter of the furcation entrance. About half of the furcation entrances
Regenerative therapy in furcation defects
has a diameter of 0.05). The number of Class II furcations that were closed or converted to Class I was greater for enamel matrix derivative plus demineralized freeze-dried bone allograft plus guided tissue regeneration. Another recent randomized clinical trial on proximal Class II furcation defects on maxillary molars compared the combination of enamel matrix derivative plus hydroxyapatite/beta-tricalcium phosphate with hydroxyapatite/beta-tricalcium phosphate alone in 30 patients with 30 defects (133). Horizontal bone level gains after 6 months were 1.7 1.3 mm for both treatment modalities. The enamel matrix derivative plus hydroxyapatite/beta-tricalcium phosphate group showed seven closed furcations and seven conversions to Class I versus four closed furcations and 10 conversions to Class I in the hydroxyapatite/beta-tricalcium phosphate group (P > 0.05).
Class III furcation involvement One case-series study evaluated the treatment of Class III mandibular furcation defects by the use of enamel matrix derivative alone or in combination with a bioresorbable membrane (41). Nine patients with a total of 14 Class III mandibular furcation defects were assigned to one of three groups: (i) enamel matrix derivative in four defects; (ii) guided tissue regeneration in three defects; and (iii) enamel matrix derivative and guided tissue regeneration in seven defects. None of the treatments resulted predictably in complete healing of the defects and there was no obvious difference between the various treatment modalities. At 6 and 12 months, partial closure of the Class III involvements had occurred in six of the 14 treated furcations. The remaining teeth still presented through-and-through
Regenerative therapy in furcation defects 6
B
70
2 LE-RM LM-RE 0
50 40 30 20 10
–2
2 0 4 6 Change of horizontal depth under membrane treatment (mm)
Emdogain® Membrane
n = 30
50 40
n = 16
30
n = 16
n = 12 n = 10
20 10 0
n=6
None
n=4 Moderate Little Postoperative pain
D
n = 11
n=4
n=3 0
I II Furcation class
50 40
Membrane n = 17
n = 16
n = 14
30
III
Emdogain®
n = 21 Number of patients (%)
70 60
Number of patients (%)
n=9
n=8
n=1 0
–2
C
Emdogain® Membrane
n = 27 n = 27
60
4 Number of detects (%)
Change of horizontal depth under Emdogain® treatment (mm)
A
n = 15
20 n=6 10
n=3
n=4
n=2 Strong
0
None
Moderate Little Postoperative swelling
Strong
Fig. 4. (A) Treatment according to treatment scatterplot for 45 individual pairs of mandibular buccal Class II furcation defects treated with enamel matrix derivative (Emdogain) or guided tissue regeneration (n = 45 patients available for re-entry). Change (mm) in horizontal furcation depth (surgery compared with re-entry) is shown. (B) Distribution of furcation class at 14 months following treatment of mandibular buccal class II furcations with enamel matrix derivative (Emdogain) or guided tissue
regeneration. (C) Postoperative pain (1 week postsurgery) following treatment with enamel matrix derivative (Emdogain) or guided tissue regeneration (n = 48 patients). (D) Postoperative swelling (1 week postsurgery) following treatment with enamel matrix derivative (Emdogain) or guided tissue regeneration (total n = 48 patients) (83). Reproduced with permission of American Academy of Periodontology. LE-RM: left EMD, right membrane; LMRE: left membrane, right EMD.
furcation defects. Within the limits of this case series, and taking into account the limited number of patients and furcation involvements in each treatment group, it was concluded that the use of enamel matrix derivative alone or in combination with guided tissue regeneration did not result in predictable regeneration of mandibular Class III furcation defects.
Conclusions and recommendations
Long-term results No long-term data (> 3 years) are available for the effects of enamel matrix derivative application in the regenerative therapy of furcation defects.
An evaluation of the scientific literature on the regenerative therapy of furcation lesions may warrant the following conclusions. An abundance of studies and several systematic reviews with meta-analyses have demonstrated efficacy of guided tissue regeneration therapy for the regenerative treatment of furcation defects. Guided tissue regeneration therapy generally results in significantly higher horizontal defect fill (i.e. horizontal probing attachment level and/or horizontal probing bone level gain) in Class II furcation involvement of mandibular and maxillary molars when compared with open flap debridement. This
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C
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therapy has demonstrated good clinical outcomes in buccal sites of mandibular and maxillary molars, but is unpredictable at interproximal sites. Complete furcation closure is not either a predictable outcome. There is only limited information for lingual sites. Class III furcation defects cannot be improved predictably by guided tissue regeneration procedures and therefore this therapy is not indicated in the treatment of these lesions. There are no significant differences in clinical outcomes when biodegradable membranes are compared with nonresorbable barrier membranes. Some bone grafts/bone substitutes may enhance the outcome of guided tissue regeneration therapy in furcations. Limited data are available on the effects of enamel matrix derivative application in the regenerative therapy of furcation involvement and thus no metaanalyses have been performed. Although enamel matrix derivative has demonstrated clinical improve-
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Fig. 5. (A) Periodontal measurements at baseline tooth no. 26. Recession: buccal to the cemento– enamel junction: 3 mm. Probing depth mesial = 2 mm, furcation class II; probing depth buccal = 6 mm; probing depth distal = 4 mm. Note minimal keratinized tissue at the furcation site. (B) Intra-operative view. Furcation class II (horizontal probing bone level = 6 mm), debrided root surface and cervical enamel projections removed. Placement of an orthodontic button to facilitate crown-attached sutures (61). Flap design: intrasulcular incision/no vertical release, mucoperiostal flap, papillae de-epithelialized, periosteal split in the vestibule. (C) Application of enamel matrix derivative after root surface conditioning with 24% EDTA for removal of the smear layer (83). (D) Application of xenogeneic bone mineral into the furcation defect (160). (E) Connective tissue graft from the palate placed onto the root surface and over the furcation area, secured by resorbable sling sutures (14). (F) Coronally advanced flap secured with crown-attached sutures (61). (G) Clinical and radiographic view at baseline, and 12 and 24 months after periodontal-regenerative surgery. Complete resolution of the furcation defect and recession coverage.
ments in the treatment of buccal Class II furcation defects in mandibular molars, the complete closure of the furcation lesion is achieved only in a minority of the cases. Similarly, there is evidence indicating that the use of enamel matrix derivative in proximal furcations of maxillary molars might result in conversion of Class II furcation involvements to Class I, which may improve the individual tooth prognosis. The current evidence, however, does not support the use of enamel matrix derivative for the treatment of lingual Class II mandibular molar furcation defects. With regard to patient-centered outcomes, one multicenter trial in buccal mandibular Class II furcation defects found less patient morbidity following enamel matrix derivative treatment compared with guided tissue regeneration therapy. In selecting the regenerative therapy, careful case evaluation is important because the factors associated with the lesion, such as the defect size, the pres-
Regenerative therapy in furcation defects
ence of proximal bone to the level of the fornix, the thickness/biotype of the gingiva and the amount of keratinized tissue, have shown to clearly influence therapeutic outcome. Furthermore, similar to regenerative treatment of non-furcation periodontal lesions, patient-related factors, such as oral hygiene and smoking, must be taken into consideration. Promising pre-clinical data from furcation regeneration studies in experimental animals are available for growth factor- and differentiation factor-based technologies, but limited data are available from human clinical studies. Although cell-based therapies have received considerable attention in regenerative medicine, their experimental evaluation in the treatment of periodontal furcation lesions is at a very early stage of development. In summary, the indications and the limitations for currently available treatment modalities for the regeneration of furcation defects seem well established. In the future, new regenerative treatment modalities are clearly needed to improve the predictability of complete resolution of furcation defects.
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