Mineralized tissue-formation periodontai wound heaiing
Sven Lindskog^ and Leif Department of ^Oral Histology and Cell Biology, School of Dentistry, Karolinska Institutet; ^Department of Periodontology, Public Dental Service of Skantsull, Stockholm County Council, Stockholm, Sweden
Lindskog S & Blomlof L: Mineralized tissue-formation in periodontal wound healing. J Clin Periodontol 1992; 19: 741-748. © Munksgaard 1992. ., v , Abstract. The purpose of the present study was to examine and compare the different mineralized tissues that are found on and around the dental root following treatment of different periodontal pathosis. The material has been compiled from previously published experimental studies on periodontal therapies and trauma treatments. 4 distinctly different appearances of the minerahzed tissue layers on the marginal dentin surfaces were described; new cementum, non-attached bone-like tissue, partly attached bone-like tissue and ankylosis preceded by root resorption. It was concluded that, healing in the periodontal/root interface following periodontal therapy may yield different mineralized tissues, depending on a number of host-specific and external factors. The temporal pattern of such healing processes is schematically represented.
Invasive periodontal therapies, such as subgingival scaling and periodontal surgery produces healing results ranging from (1) a recurrent pathological pocket, (2) a long epithelial junction, (3) capsule formation (connective tissue attachment), (4) new attachment to (5) ankylosis. Recurrent extensive pathological pocket formation is found after surgery in plaque-infected dentitions (Nyman et al. 1977). A long epithehal junction or capsule formation are commonly found after subgingival scaling and fiap surgery (Yukna 1976, Caton & Nyman 1980, Caton et al. 1980, Bloml5f et al. 1987, 1989, Lindskog et al. 1991). New attachment with reparative cementum, new collagen fibers and new alveolar bone is only occasionally found after fiap surgery under certain favorable circumstances, such as in conjunction with guided tissue regeneration (Nyman et al. 1982, Gottlow et al. 1984), implantation of freeze-dried decalcified bone (Bowers et al. 1989a, b) and experimental chemical conditioning ofthe root surface (Blomldf et al. 1987, 1989). Reparative cementum formation "will occur with equal frequency over cementum and dentin when the oral environment is excluded" (Middleton & Bowers 1990). However, mineralized tissue formation on denuded root surfaces is not only limited to periodontal therapy, but is rather a universal sequela to injuries to the dento-alveolar com-
plex. In this context, a unified nomenclature is lacking and any mineralized tissue on the root surface not attached to alveolar bone is regarded as reparative cementum or even regeneration of original cementum. The purpose of the present study was to examine and compare the different mineralized tissues that are found on and around the dental root following treatment of different periodontal pathosis. The material has been compiled from previously published experimental studies on periodontal therapies and trauma treatments. Material and Methods Experimental material
Lateral incisors and first and second premolars in young and old monkeys (Macaca fascicularis) from two previous experimental studies (Blomlof et al. 1991, Lindskog et al. 1991) on periodontal therapies and trauma treatments of denuded dentin surfaces were reexamined. The treatments involved mechanical denudation of dentin surfaces in experimentally avulsed and replanted teeth in young and old monkeys as well as denudation of dentin surfaces in marginal periodontal wounds. Histological preparation and evaluation
After sacrifice, the parts of the jaws containing the experimental teeth were dis-
Key words: bone; dental cementum; monkey; periodontal therapy. Accepted for publication 10 October 1991
sected out and fixed in cold 5% neutralbuffered formalin for 48 hours, demineralized in 10% formic acid, infiltrated and embedded in paraffin and sectioned step-serially at levels 70 /zm apart, perpendicularly or parallel to the long axes of the teeth. Each section was 5 fxm thick. The sections were stained with hematoxylin and eosin and examined in a light microscope with both ordinary transmitted and polarized light. Every 3rd section was used for morphologic evaluation and the tissue reaction at the periodontal/root interface was described morphologically with special emphasis on differences and similarities to original cementum and alveolar bone. Results
4 distinctly different appearances of the mineralized tissue layers formed on the marginal dentin surfaces could be distinguished, based on a comparison to adjacent alveolar bone and original cementum. New cementum (Fig. 1), closely resembling original cementum, was attached to the root surface with fibrebundles arranged in a pallisade-like fashion. The formation of it had been preceded by a superficial resorption of the dentin surface. The new cementum was uniformly thin and predominantly acellular. However, occasionally embed-
742
Lindskog & Blomlof
Fig. L Longitudinal section from a lower second incisor (A) in a young monkey with a marginal defect on the proximal side. (B) to (E) show details from (A). A long junctional epithelium (arrowhead) covers the most cervical dentin surface in the marginal defect (B). Apical to this area, a thin layer with new cementum (arrowheads) attached to the resorbed root surface can be seen (C, D). Note the resorption lacunoe on the dentin surface filled with new cementum (E, E). The new cementum is in turn covered by a mono-layer of cementoblast-like cells (arrowheads). The new cementum displays functionally oriented birefringent embedded fibre-bundles under polarized light (ari-ows) (E).
ded cementocyte-like cells were seen. These were, in comparison to osteocytes, smaller. The new cementum was invariably attached to the connective tissue in the periodontal space with fibre-bundles resembling functionally
oriented periodontal fibres which were, in turn, attached to the alveolar bone. Isolated islands of epithelial cells resembling epithelial rests of Malassez were seen in the periodontal space. Non-attached bone-like tissue (Fig. 2)
had a distinct multi-layered arrangement identical to the adjacent alveolar bone as seen in polarized hght (Fig. 3). It was exclusively cellular with embedded osteocyte-like cells and appeared tc be loosely apposed to a smooth dentir
Mineralized tissue-formation in periodontal wound healing
Fig. 2. Transversal section from a lower second incisor (A) in an old monkey with a marginal proximal defect. (B) to (B) show details from (A). A non-attached bone-like tissue-layer loosely apposed to a smooth dentin surface covers the defect. Note the abundance of tissue debris (arrowheads) between the bone-like tissue and the dentin surface (B, C). The bone-like tissue varies in thickness with a multi-layered arrangement and embedded cells, giving an appearance identical to bone (D, E).
D surface which had not been subjected to any prior resorption. An intervening connective tissue layer between the alveolar bone and the non-attached bonelike tissue appeared invariably to be organized in a capsule-like fashion with fibre-bundles running parallel to the root surface as seen in polarized light (Fig. 3). Occasionally, tissue debris was found between the mineralized tissue
743
and the dentin surface (Fig. 2). The mineralized tissue layer varied in thickness and frequently, isolated islands of bonelike tissue (Fig. 4) and of epithelial cells resembling epithehal rests of Malassez were seen in the periodontal space, close to the root surfaces. Partly attached bone-like tissue (Fig. 5) had an essentially identical morphology to non-attached bone-like tissue
with the exception of occasional shallow resorption lacunoe on the dentin surface. These were filled with a bone-like tissue which was continuous with the non-attached parts of the tissue layer. Ankylosis preceded by root resorption (Fig. 6) was seen as alveolar bone attached to a resorbed dentin surface. The bone tissue had a multi-layered arrangement as seen in polarized light.
Lindskog & Blomlof
744
f Fig. 3. Transversal section from an upper second incisor in an old monkey (A) with a marginal proximal defect. Note the bone-like tissue in the defect (arrowheads) and the adjacent original cementum (arrow). (B) and (C) show details from (A) under polarized light. The bone-like tissue displays a distinct multi-layered arrangement under polarized light with no apparent functional arrangement (B). The adjacent original cementum has an abundance of functionally oriented fibres (B).
Discussion
Periodontal disease, periodontal therapy and traumatic injuries to the periodontium each, in their own way, damage the periodontium and provoke formation of areas of necrotic tissue and granulation tissue. It is a well-established fact that these areas, in turn evoke an array of both destructive and reparative cellular processes in the periodontium, the end result depending on a number of different, both host-specific and external factors. Much time has been devoted to identifying these factors and, in this context, reinfection (Nyman et al. 1977, Blomlof et al. 1991), degree of infiammation (Berg et al. 1990), root surface conditioning (for review see Egelberg 1987), size of the damaged area (Andreasen 1981), functional stimuli (Andersson 1985) and, different surgical techniques (Nyman et al. 1982, Gottlow et al. 1984, Bowers et al. 1989a, b) have been discussed. Irrespective of these modifying factors, a limited resorptive activity, either of necrotic soft tissue or of mineralized dental tissues, appear inFig. 4, Transversal section from a lower second incisor (A) in an old monkey with a marginal variably to precede the subsequent healing process. proximal defect. The dentine surface is covered by a non-attached bone-like tissue-layer (B) From the present results it was evi(arrows) and a pathological pocket epithelium. Note the isolated island of bone-like tissue in dent that three out ofthe four identified the periodontal space, close to the root surface (arrowhead). •• • : ; ; , ..
Mineralized tissue-formation in periodontal wound healing
D
, -It
Fig. 5. Transversal section from an upper second incisor (A) in a young monkey with a marginal proximal defect. (B) to (D) show details from (A). A partly attached bone-like tissuelayer outlines the dentin defect (B, C). Note the embedded osteocyte-like lacunoe (D) and the morphological resemblance to alveolar bone.
mineralized tissue healing patterns on the denuded dentin surfaces started with either a limited (partly attached bonelike tissue) or a complete (new cementum and ankylosis) resorption of the root surfaces. It rnay be argued that the remaining healing pattern (non-at-
tached bone-like tissue) also involved resorptive activity, however, not of the dentin surface but rather in the adjacent granulation/necrotic tissue in the periodontal space. This leads to interesting theoretical possibilities of interpretation regarding the subsequent healing pro-
745
cesses, since the mineralized tissues which formed subsequently had distinctly different morphological appearances (Fig. 7). The fact that the bone-like tissue appeared to be separated from the dentin surface in some areas, was probably due to an artifactual split between the dentin surface and the bone-like tissue during the histo-technical procedure (Listgarten 1972). However, this only emphasizes the fact that this tissue was not properly attached to the dentin surface in contrast to new cementum as well as partly attached bone-like tissue where fibrebundles inserted into the dentin surface in resorption lacunoe. The non-attached bone-like tissue was most hkely only loosely apposed to the dentin surface (Jansen et al. 1955). It is clear from previous studies that a resorptive process may be followed and possibly also initiates formation of mineralized tissue (for review, see Arnett (1990)), provided it occurs in an osteogenic environment such as the periodontal membrane. However, in the periodontium, the end result appears also to be highly dependent on modifying factors as discussed above. These may, as in the case of reinfection even jeopardize the periodontal healing process entirely by promoting epithelial down-growth (Berg et al. 1990, Blomlof et al. 1991). It is tempting to suggest that the different mineralized tissues are the result of repopulation of the resorbed areas by mesenchymal cells expressing different phenotypes (Fig. 8) (Melcher et al. 1987, McCulloch & Bordin 1991), either a cementoblast phenotype (new cementum) or an osteoblast phenotype (non-attached bone-hke tissue; partly attached bone-like tissue and ankylosis preceded by root resorption). Expression of a cementoblast phenotype appeared only possible after a superficial resorption of the entire denuded dentin area (Fig. 1). However, this can not be entirely sufficient to promote formation of new cementum since resorption also preceded ankylosis and bone-Hke tissue formation. Additional factors such as the potency of the source of undifferentiated mesenchymal cells, as in young teeth with incomplete root closure probably also determine which type of mineralized tissue-healing that can be expected (Blomlof et al. 1991). Bone-like tissue was found in two different situations, either partially preceded by root resorption (Fig. 5) or on
746
Lindskog & Blomlof the pool of undifferentiated mesenchymal cells in the periodontal membrane apical to the damaged areas (Iglhaut et al. 1988) have probably been attracted to isolated areas of resorption in the granulation/necrotic tissue and, stimulated by the resdrptive activity, started to form islands of bone-like tissue (Fig. 4). This reasoning could also apply to formation of bone-like tissue preceded by resorption on the dentine surface, although the factors that initiate dentin resorption can not in retrospect be identified. The fact that the bone-like tissue, irrespective of attachment to the dentin surface had not formed an ankylotic fusion with the alveolar bone may have been due to ingrowth of intervening periodontal connective tissue with an epithelial net-work (L0e & Waerhaug 1961, Lindskog et al. 1988). However, when the regenerative potential of the remaining periodontal connective tissue is impaired or absent, a complete ankylotic fusion will be the consequence. Ankylosis (Fig. 6), as described as the last group of mineralized tissue-formation on exposed dentin surfaces may thus, be regarded as the only possible healing reaction when the balance between the expression of cementoblastlike and osteoblast-like phenotypes only favours the latter. This type of healing then, by definition falls within the group of scar tissue-formation, analogous with escessive epithelial down-growth along the root surfaces (long epithelial junction and pathological pocket formation). In conclusion, healing in the periodontal/root interface following periodontal therapy may yield several different mineralized tissues, depending on a number of host-specific and external factors. Apart from scar tissue formation (ankylosis and epithelial downgrowth), most of the mineralized tissues found on the root surfaces present only evidence of a limited repair process. The Fig. 6. Transversal section from an upper second incisor (A) in an old monkey with a marginal only exception appears to be new ceproximal defect. (B) and (D) show details from figure 6A. The central part of the defect is mentum, found commonly after reoccupied by ankylosis (AN) preceded by root resorption (B, D). The bone tissue has a multi- sorption on the root surface, for which layered arrangement and contains numerous embedded osteocytes. The surrounding dentin the term regeneration should be resurface in the defect is covered by a layer of non-attached bone-like tissue (arrows) (C, D). served. The temporal pattern of the healing processes has been summarized in Fig. 9. a non-resorbed dentin surface (Fig. 2). tissue had formed not directly on the It is interesting to note that the non- dentin surface but rather within the attached bone-like tissue sometimes was periodontal space, close to the root sur- Acknowledgements seen with an intervening layer of tissue face, only to appear associated with the debris towards the root surface (Fig. 2). root after an extended healing period. This study was supported by the Swed This would indicate that the mineralized Cells with an osteoblast phenotype from ish Medical Research Council (grant no
AN
AN
t
s
Mineralized tissueformation in periodontal wound healing
747
necrotic/granula tion Undillerenlialed
ecto-mesenchymal
PDM-cell
Environmental influence
PDM-fibroblasi
Cementoblast
Osteoblast
Fig. 8. Schematic representation of the suggested differentiation of cell phenotypes responsible for the formation of the different healing tissues in the marginal periodontal space. Three different phenotypes are possible; a periodontal fibroblast forming new periodontal membrane, a cementoblast phenotype producing new cementum and, an osteoblast phenotype producing non-attached bone-like tissue, partly attached bonelike tissue or ankylosis.
li
v^ S
P
Necrosis/granulation
'
Sven Lindskog^ and Leif Department of ^Oral Histology and Cell Biology, School of Dentistry, Karolinska Institutet; ^Department of Periodontology, Public Dental Service of Skantsull, Stockholm County Council, Stockholm, Sweden
Lindskog S & Blomlof L: Mineralized tissue-formation in periodontal wound healing. J Clin Periodontol 1992; 19: 741-748. © Munksgaard 1992. ., v , Abstract. The purpose of the present study was to examine and compare the different mineralized tissues that are found on and around the dental root following treatment of different periodontal pathosis. The material has been compiled from previously published experimental studies on periodontal therapies and trauma treatments. 4 distinctly different appearances of the minerahzed tissue layers on the marginal dentin surfaces were described; new cementum, non-attached bone-like tissue, partly attached bone-like tissue and ankylosis preceded by root resorption. It was concluded that, healing in the periodontal/root interface following periodontal therapy may yield different mineralized tissues, depending on a number of host-specific and external factors. The temporal pattern of such healing processes is schematically represented.
Invasive periodontal therapies, such as subgingival scaling and periodontal surgery produces healing results ranging from (1) a recurrent pathological pocket, (2) a long epithelial junction, (3) capsule formation (connective tissue attachment), (4) new attachment to (5) ankylosis. Recurrent extensive pathological pocket formation is found after surgery in plaque-infected dentitions (Nyman et al. 1977). A long epithehal junction or capsule formation are commonly found after subgingival scaling and fiap surgery (Yukna 1976, Caton & Nyman 1980, Caton et al. 1980, Bloml5f et al. 1987, 1989, Lindskog et al. 1991). New attachment with reparative cementum, new collagen fibers and new alveolar bone is only occasionally found after fiap surgery under certain favorable circumstances, such as in conjunction with guided tissue regeneration (Nyman et al. 1982, Gottlow et al. 1984), implantation of freeze-dried decalcified bone (Bowers et al. 1989a, b) and experimental chemical conditioning ofthe root surface (Blomldf et al. 1987, 1989). Reparative cementum formation "will occur with equal frequency over cementum and dentin when the oral environment is excluded" (Middleton & Bowers 1990). However, mineralized tissue formation on denuded root surfaces is not only limited to periodontal therapy, but is rather a universal sequela to injuries to the dento-alveolar com-
plex. In this context, a unified nomenclature is lacking and any mineralized tissue on the root surface not attached to alveolar bone is regarded as reparative cementum or even regeneration of original cementum. The purpose of the present study was to examine and compare the different mineralized tissues that are found on and around the dental root following treatment of different periodontal pathosis. The material has been compiled from previously published experimental studies on periodontal therapies and trauma treatments. Material and Methods Experimental material
Lateral incisors and first and second premolars in young and old monkeys (Macaca fascicularis) from two previous experimental studies (Blomlof et al. 1991, Lindskog et al. 1991) on periodontal therapies and trauma treatments of denuded dentin surfaces were reexamined. The treatments involved mechanical denudation of dentin surfaces in experimentally avulsed and replanted teeth in young and old monkeys as well as denudation of dentin surfaces in marginal periodontal wounds. Histological preparation and evaluation
After sacrifice, the parts of the jaws containing the experimental teeth were dis-
Key words: bone; dental cementum; monkey; periodontal therapy. Accepted for publication 10 October 1991
sected out and fixed in cold 5% neutralbuffered formalin for 48 hours, demineralized in 10% formic acid, infiltrated and embedded in paraffin and sectioned step-serially at levels 70 /zm apart, perpendicularly or parallel to the long axes of the teeth. Each section was 5 fxm thick. The sections were stained with hematoxylin and eosin and examined in a light microscope with both ordinary transmitted and polarized light. Every 3rd section was used for morphologic evaluation and the tissue reaction at the periodontal/root interface was described morphologically with special emphasis on differences and similarities to original cementum and alveolar bone. Results
4 distinctly different appearances of the mineralized tissue layers formed on the marginal dentin surfaces could be distinguished, based on a comparison to adjacent alveolar bone and original cementum. New cementum (Fig. 1), closely resembling original cementum, was attached to the root surface with fibrebundles arranged in a pallisade-like fashion. The formation of it had been preceded by a superficial resorption of the dentin surface. The new cementum was uniformly thin and predominantly acellular. However, occasionally embed-
742
Lindskog & Blomlof
Fig. L Longitudinal section from a lower second incisor (A) in a young monkey with a marginal defect on the proximal side. (B) to (E) show details from (A). A long junctional epithelium (arrowhead) covers the most cervical dentin surface in the marginal defect (B). Apical to this area, a thin layer with new cementum (arrowheads) attached to the resorbed root surface can be seen (C, D). Note the resorption lacunoe on the dentin surface filled with new cementum (E, E). The new cementum is in turn covered by a mono-layer of cementoblast-like cells (arrowheads). The new cementum displays functionally oriented birefringent embedded fibre-bundles under polarized light (ari-ows) (E).
ded cementocyte-like cells were seen. These were, in comparison to osteocytes, smaller. The new cementum was invariably attached to the connective tissue in the periodontal space with fibre-bundles resembling functionally
oriented periodontal fibres which were, in turn, attached to the alveolar bone. Isolated islands of epithelial cells resembling epithelial rests of Malassez were seen in the periodontal space. Non-attached bone-like tissue (Fig. 2)
had a distinct multi-layered arrangement identical to the adjacent alveolar bone as seen in polarized hght (Fig. 3). It was exclusively cellular with embedded osteocyte-like cells and appeared tc be loosely apposed to a smooth dentir
Mineralized tissue-formation in periodontal wound healing
Fig. 2. Transversal section from a lower second incisor (A) in an old monkey with a marginal proximal defect. (B) to (B) show details from (A). A non-attached bone-like tissue-layer loosely apposed to a smooth dentin surface covers the defect. Note the abundance of tissue debris (arrowheads) between the bone-like tissue and the dentin surface (B, C). The bone-like tissue varies in thickness with a multi-layered arrangement and embedded cells, giving an appearance identical to bone (D, E).
D surface which had not been subjected to any prior resorption. An intervening connective tissue layer between the alveolar bone and the non-attached bonelike tissue appeared invariably to be organized in a capsule-like fashion with fibre-bundles running parallel to the root surface as seen in polarized light (Fig. 3). Occasionally, tissue debris was found between the mineralized tissue
743
and the dentin surface (Fig. 2). The mineralized tissue layer varied in thickness and frequently, isolated islands of bonelike tissue (Fig. 4) and of epithelial cells resembling epithehal rests of Malassez were seen in the periodontal space, close to the root surfaces. Partly attached bone-like tissue (Fig. 5) had an essentially identical morphology to non-attached bone-like tissue
with the exception of occasional shallow resorption lacunoe on the dentin surface. These were filled with a bone-like tissue which was continuous with the non-attached parts of the tissue layer. Ankylosis preceded by root resorption (Fig. 6) was seen as alveolar bone attached to a resorbed dentin surface. The bone tissue had a multi-layered arrangement as seen in polarized light.
Lindskog & Blomlof
744
f Fig. 3. Transversal section from an upper second incisor in an old monkey (A) with a marginal proximal defect. Note the bone-like tissue in the defect (arrowheads) and the adjacent original cementum (arrow). (B) and (C) show details from (A) under polarized light. The bone-like tissue displays a distinct multi-layered arrangement under polarized light with no apparent functional arrangement (B). The adjacent original cementum has an abundance of functionally oriented fibres (B).
Discussion
Periodontal disease, periodontal therapy and traumatic injuries to the periodontium each, in their own way, damage the periodontium and provoke formation of areas of necrotic tissue and granulation tissue. It is a well-established fact that these areas, in turn evoke an array of both destructive and reparative cellular processes in the periodontium, the end result depending on a number of different, both host-specific and external factors. Much time has been devoted to identifying these factors and, in this context, reinfection (Nyman et al. 1977, Blomlof et al. 1991), degree of infiammation (Berg et al. 1990), root surface conditioning (for review see Egelberg 1987), size of the damaged area (Andreasen 1981), functional stimuli (Andersson 1985) and, different surgical techniques (Nyman et al. 1982, Gottlow et al. 1984, Bowers et al. 1989a, b) have been discussed. Irrespective of these modifying factors, a limited resorptive activity, either of necrotic soft tissue or of mineralized dental tissues, appear inFig. 4, Transversal section from a lower second incisor (A) in an old monkey with a marginal variably to precede the subsequent healing process. proximal defect. The dentine surface is covered by a non-attached bone-like tissue-layer (B) From the present results it was evi(arrows) and a pathological pocket epithelium. Note the isolated island of bone-like tissue in dent that three out ofthe four identified the periodontal space, close to the root surface (arrowhead). •• • : ; ; , ..
Mineralized tissue-formation in periodontal wound healing
D
, -It
Fig. 5. Transversal section from an upper second incisor (A) in a young monkey with a marginal proximal defect. (B) to (D) show details from (A). A partly attached bone-like tissuelayer outlines the dentin defect (B, C). Note the embedded osteocyte-like lacunoe (D) and the morphological resemblance to alveolar bone.
mineralized tissue healing patterns on the denuded dentin surfaces started with either a limited (partly attached bonelike tissue) or a complete (new cementum and ankylosis) resorption of the root surfaces. It rnay be argued that the remaining healing pattern (non-at-
tached bone-like tissue) also involved resorptive activity, however, not of the dentin surface but rather in the adjacent granulation/necrotic tissue in the periodontal space. This leads to interesting theoretical possibilities of interpretation regarding the subsequent healing pro-
745
cesses, since the mineralized tissues which formed subsequently had distinctly different morphological appearances (Fig. 7). The fact that the bone-like tissue appeared to be separated from the dentin surface in some areas, was probably due to an artifactual split between the dentin surface and the bone-like tissue during the histo-technical procedure (Listgarten 1972). However, this only emphasizes the fact that this tissue was not properly attached to the dentin surface in contrast to new cementum as well as partly attached bone-like tissue where fibrebundles inserted into the dentin surface in resorption lacunoe. The non-attached bone-like tissue was most hkely only loosely apposed to the dentin surface (Jansen et al. 1955). It is clear from previous studies that a resorptive process may be followed and possibly also initiates formation of mineralized tissue (for review, see Arnett (1990)), provided it occurs in an osteogenic environment such as the periodontal membrane. However, in the periodontium, the end result appears also to be highly dependent on modifying factors as discussed above. These may, as in the case of reinfection even jeopardize the periodontal healing process entirely by promoting epithelial down-growth (Berg et al. 1990, Blomlof et al. 1991). It is tempting to suggest that the different mineralized tissues are the result of repopulation of the resorbed areas by mesenchymal cells expressing different phenotypes (Fig. 8) (Melcher et al. 1987, McCulloch & Bordin 1991), either a cementoblast phenotype (new cementum) or an osteoblast phenotype (non-attached bone-hke tissue; partly attached bone-like tissue and ankylosis preceded by root resorption). Expression of a cementoblast phenotype appeared only possible after a superficial resorption of the entire denuded dentin area (Fig. 1). However, this can not be entirely sufficient to promote formation of new cementum since resorption also preceded ankylosis and bone-Hke tissue formation. Additional factors such as the potency of the source of undifferentiated mesenchymal cells, as in young teeth with incomplete root closure probably also determine which type of mineralized tissue-healing that can be expected (Blomlof et al. 1991). Bone-like tissue was found in two different situations, either partially preceded by root resorption (Fig. 5) or on
746
Lindskog & Blomlof the pool of undifferentiated mesenchymal cells in the periodontal membrane apical to the damaged areas (Iglhaut et al. 1988) have probably been attracted to isolated areas of resorption in the granulation/necrotic tissue and, stimulated by the resdrptive activity, started to form islands of bone-like tissue (Fig. 4). This reasoning could also apply to formation of bone-like tissue preceded by resorption on the dentine surface, although the factors that initiate dentin resorption can not in retrospect be identified. The fact that the bone-like tissue, irrespective of attachment to the dentin surface had not formed an ankylotic fusion with the alveolar bone may have been due to ingrowth of intervening periodontal connective tissue with an epithelial net-work (L0e & Waerhaug 1961, Lindskog et al. 1988). However, when the regenerative potential of the remaining periodontal connective tissue is impaired or absent, a complete ankylotic fusion will be the consequence. Ankylosis (Fig. 6), as described as the last group of mineralized tissue-formation on exposed dentin surfaces may thus, be regarded as the only possible healing reaction when the balance between the expression of cementoblastlike and osteoblast-like phenotypes only favours the latter. This type of healing then, by definition falls within the group of scar tissue-formation, analogous with escessive epithelial down-growth along the root surfaces (long epithelial junction and pathological pocket formation). In conclusion, healing in the periodontal/root interface following periodontal therapy may yield several different mineralized tissues, depending on a number of host-specific and external factors. Apart from scar tissue formation (ankylosis and epithelial downgrowth), most of the mineralized tissues found on the root surfaces present only evidence of a limited repair process. The Fig. 6. Transversal section from an upper second incisor (A) in an old monkey with a marginal only exception appears to be new ceproximal defect. (B) and (D) show details from figure 6A. The central part of the defect is mentum, found commonly after reoccupied by ankylosis (AN) preceded by root resorption (B, D). The bone tissue has a multi- sorption on the root surface, for which layered arrangement and contains numerous embedded osteocytes. The surrounding dentin the term regeneration should be resurface in the defect is covered by a layer of non-attached bone-like tissue (arrows) (C, D). served. The temporal pattern of the healing processes has been summarized in Fig. 9. a non-resorbed dentin surface (Fig. 2). tissue had formed not directly on the It is interesting to note that the non- dentin surface but rather within the attached bone-like tissue sometimes was periodontal space, close to the root sur- Acknowledgements seen with an intervening layer of tissue face, only to appear associated with the debris towards the root surface (Fig. 2). root after an extended healing period. This study was supported by the Swed This would indicate that the mineralized Cells with an osteoblast phenotype from ish Medical Research Council (grant no
AN
AN
t
s
Mineralized tissueformation in periodontal wound healing
747
necrotic/granula tion Undillerenlialed
ecto-mesenchymal
PDM-cell
Environmental influence
PDM-fibroblasi
Cementoblast
Osteoblast
Fig. 8. Schematic representation of the suggested differentiation of cell phenotypes responsible for the formation of the different healing tissues in the marginal periodontal space. Three different phenotypes are possible; a periodontal fibroblast forming new periodontal membrane, a cementoblast phenotype producing new cementum and, an osteoblast phenotype producing non-attached bone-like tissue, partly attached bonelike tissue or ankylosis.
li
v^ S
P
Necrosis/granulation
'
