Root Surface Demineralization in Periodontal Therapy Subject Review

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Root Surface Demineralization in Periodontal Therapy:

Subject Review*
Scott H. Nightingale and Phillip J. Sheridan

Accepted for publication 2 June 1982

The literature of root surface demineralization in periodontal therapy is reviewed. Root


surface alterations in periodontal disease and root surface preparation are also discussed.

ROOT SURFACE ALTERATIONS IN PERIODONTAL granules may represent bacteria,4'7 or they may result
DISEASE from penetration of exogenous bacterial or salivary sub-
stances.6
Selvig,1 in an ultrastructural study, observed changes In 1971, Hatfield and Baumhammers8 exposed mono-
in the mineralization patterns and surface appearance of
cementum that corresponded to the degree of breakdown
layers of gingival epithelial cells in tissue culture to
of periodontal connective tissue attachment associated
healthy and periodontally diseased roots of extracted
teeth. The monolayers exposed to the involved roots
with periodontal disease. Cementum, in areas where showed irreversible morphologic changes, while those
disease activity had resulted in complete breakdown of
the connective tissue attachment and in areas where it exposed to healthy roots did not. They hypothesized that
toxic factors or endotoxins released by oral microorga-
was lined by epithelium, was characterized ultrastruc-
nisms in the periodontal pocket had penetrated the root
turally by a reduction in the number and size of mineral surfaces to later leach out and produce cytotoxic effects.
crystals, by loss of typical collagen structure, and by a The plaque flora in Periodontitis is predominantly
very irregular surface outline. These alterations extended Gram-negative, and most Gram-negative bacteria con-
40 to 100 µ from the cementum border but did not
tain a complex lipopolysaccharide (endotoxin) in their
reach the cemento-dentinal junction. walls.9
Selvig and Zander2 found higher contents of calcium, Aleo et al.9 found endotoxin present in cementum of
magnesium and phosphorus in the cervical cementum of untreated periodontally involved teeth. They too used
periodontally diseased roots than in corresponding areas human gingival fibroblasts to study the in vitro attach-
of healthy teeth. They also demonstrated the presence of
ment of cells to the root surfaces of such teeth. They
a highly mineralized zone in the superficial layer of the
found that root portions exposed to the disease process
root surface in periodontally diseased teeth. They related
had minimal cell attachment, while uninvolved root
these changes to penetration of minerals from the surface areas had cell attachment that was normal.10
while the tooth root was exposed to either the environ- Everhart and Stahl11 found antigen in the cementum
ment of the periodontal pocket or the oral cavity. Later
of periodontally involved teeth which was not present in
studies confirmed these findings and also identified high
the cementum of impacted teeth. They later extracted
levels of fluoride in the hypermineralized zone.3 this antigenic component from cementum. Using coun-
Organic changes also take place in root surfaces ex- tercurrent immunoelectrophoresis to show the antibody-
posed to the periodontal pocket. In 1951, Bass4 described antigen reaction, they demonstrated that a component
refractile "pathologic granules" in exposed cementum from pocket-exposed cementum will react with homol-
and underlying dentin. These granules were studied
further by Armitage and Christie,5 who observed them ogous serum and with heterologous sera from persons
with periodontal disease.12'13
in areas of incompletely mineralized collagen fibrils. Whether endotoxin is adsorbed to or trapped within
Bigarre and Yardin6 later determined that the granules the irregularities in the exposed root surface has not been
contained cholesterol or steroid. Although their signifi- established. However, by acting as a reservoir, the dis-
cance is not well understood, the granules may represent
eased root surface may perpetuate the destructive effects
foci of degradation of collagen. On the other hand, the of endotoxin on the periodontium.
ROOT SURFACE PREPARATION
*
From the Department of Dentistry, Section of Periodontics, Mayo
Clinic and Mayo Foundation, Rochester, MN 55905. Preparation of the root surface in periodontal therapy
611
J. Periodontol.
612 Nightingale, Sheridan October, 1982

usually includes scaling to remove plaque and calcified eralized in situ by contact with acid before flap closure
deposits and root-planing to remove surface layers which showed better histologie attachment of the healing flaps
have been altered by disease. Jones and O'Leary14 found and more new cementum and bone formation 6 weeks
that in vitro root-planing removes nearly all detectable to 3 months after the procedure than did contralateral
bacterial endotoxin from periodontally involved root controls. Ten per cent of the demineralized teeth showed
surfaces. This type of root preparation is a prerequisite prolonged résorption of dentin during healing, with no
for new attachment and periodontal health. pulpal reactions noted. In a subsequent histologie study
of more than 1,000 teeth in 50 dogs and 5 cats, Register
DEMORALIZATION OF DENTIN and Burdick25 duplicated these results. Additionally, they
Recent evidence suggests that regeneration of the con- determined the optimal demineralization that produced
nective tissue attachment to the root can be significantly histologie attachment of flaps with new cementum, using
enhanced by demineralization of the exposed dentin. HCl at various pH and application times. They then
This information has important implications regarding duplicated the degree of demineralization, using lactic,
new attachment procedures, since an early and durable citric, phosphoric, trichloroacetic and formic acids and
attachment of gingival connective tissue to tooth during RDO (a proprietary demineralizer) in various combina-
tions of pH and application times. In all, 250 different
healing could significantly reduce apical epithelial mi- combinations were studied. At comparable deminerali-
gration along the root surface and under the healing flap; zation rates, all acids produced identical results. Roots
such migration can impede regeneration of bone, cemen-
tum and periodontal ligament.15 Furthermore, the loss of
that were "underdemineralized" exhibited a detachment
such tissues would deprive the periodontium of a pre- artifact on processing. "Overdemineralized" roots dem-
onstrated attachment with no detachment artifact on
dominantly connective tissue attachment which might
be better able to resist further pathologic change than processing but without cementogenesis. Optimal demin-
would a long junctional epithelium. eralization produced new attachment with cemento-
genesis and no detachment on processing. Undeminer-
USE OF ACIDS alized controls showed only partial attachment, with
The use of acids in the treatment of Periodontitis dates epithelium frequently migrating under the flap through
the entire length of the wound. The attachment that
to the last century. In 1899, Stewart16 described an
occurred consistently separated on processing. This re-
operation that included elevation of the gingiva from the search utilized experimentally induced defects in dogs
teeth, scraping of tooth root surfaces to remove cemen- and cats, and the results are not necessarily applicable to
tum, and application of "pure sulfuric or hydrochloric chronic, naturally occurring defects in humans. Never-
acid to decalcify the surface." He reported consider-
theless, it was concluded that citric acid, pH 1, applied
...

able success. for 2 to 3 minutes was the most desirable combination to


Research in bone induction has suggested a new ra-
tionale for the demineralization of dentin as an adjunct produce optimal demineralization for new attachment in
human trials.
to regenerative periodontal technique.17"23 A number of
investigators have demonstrated reproducible Osteogen- USE OF CITRIC ACID
esis within and about dentin fragments demineralized by
acid in vitro and implanted into the muscle, oral or Advantages of the use of citric acid, pH 1, for 2 to 3
subcutaneous tissue of both animal18'20,22 and human.17 minutes include: less résorption of dentin before cemen-
These authors observed differentiation into osteoblasts togenesis, less coagulation of tissue and blood than with
of the mesenchymal cells adjacent to the implants and other agents, and ease of clinical use. No pronounced
observed evidence of Osteogenesis as early as 10 days root résorption or pulpal response was noted with any of
after implantation. Lamellar bone and bone marrow the agents tested. Slight contact of the acid with the
formation were subsequently observed. The bone-induc- surrounding periodontal tissues slowed bone repair
tive effect of demineralized dentin was lost if the dentin somewhat, but had no effect on new attachment. Other
was exposed to chemical solvents that denature or de- advantages of citric acid for use in humans include the
range the fibrous protein matrix.18 In addition, the in- facts that citrates are used as anticoagulants in transfused
duction of bone appeared to be more active on the blood and that citric acid is essential to human metabo-
surface areas of the substrates that had been in direct lism and is found in many foods. These facts make it an
contact with the acid.17'19 These findings suggested to unlikely allergen.26 Endogenous citric acid from the met-
investigators that demineralizing the dentinal wall of a abolic citric acid cycle has been associated with solubil-
periodontal pocket may induce the formation of new ization of bone mineral during bone résorption.27'28
bone and cementum, resulting in repair of the osseous Citric acid may act on dentinal hydroxyapatite in three
defect. ways. First, it releases hydrogen ions, which demineralize
Register,24 in a pilot study of 21 teeth in monkeys, the crystalline structure. Second, it contains two or more
dogs and a cat, determined that dentin wounds demin- groups in its molecule which can combine with calcium
Volume 53
Number 10 Root Surface Demineralization 613
and act as a chelating agent. Third, it can participate in dibular premolars of six Beagle dogs. The defects were
surface exchange, with citrate ions replacing phosphate treated using citric acid and flap surgery. Six weeks after
ions in the hydroxyapatite structure.28,29 the initial surgical procedure, one side of each dog was
re-treated in exactly the same manner. Histologie eval-
SIMULATED PERIODONTAL DEFECTS IN uation showed closure of the furcations and new connec-
ANIMALS tive tissue attachment, including deposition of new ce-
mentum in 77% of the treated teeth. The authors con-
In a later study of simulated periodontal defects in
cluded that the repeated surgical curettage and acid
dogs, Register and Burdick30 reviewed histologie sections application did not improve the overall results. Nilvéus
of controls and of defects treated with citric acid at 1,2,
and Egelberg38 created through-and-through furcation
3, 4, 5, and 6 weeks, 6 months, and 1 year after surgical
treatment of the defects. The results were substantially pockets in the mandibular premolars of Beagle dogs.
similar to those reported previously.24'25 The authors They applied citric acid to instrumented root surfaces
described seeing under the light microscope "cementum during flap surgery and assessed three adjunctive thera-
pins" that extended into dentinal tubules widened by peutic measures: (1) the effect of systemic antibiotics, (2)
the use of Gelfoam® within the defects, and (3) coronal
demineralization. They hypothesized that this enhanced
mechanical fixation, together with the bone-inductive repositioning of the mucoperiosteal flaps. They observed
effect of demineralized dentin on adjacent mesenchymal regeneration and new attachment histologically, regard-
less of the use of antibiotics or Gelfoam or flap position.
cells, represented the mechanism for the accelerated
reattachment observed in experimental animals. They
proposed that this response be categorized as "a cellular EXAMINATION OF EXTRACTED TEETH
phenomenon with mechanical assistance."30 Others have
suggested that irregularities in the dentin surface may Garrett et al.39 studied the effect of topically applied
aid in the attachment of new connective tissue.31'32 Scan- citric acid on periodontally diseased human tooth roots,
ning electron microscopic studies have demonstrated that using scanning and transmission electron microscopy.
dentin treated with 50% citric acid becomes considerably Sixteen extracted teeth were studied. Teeth were treated
roughened owing to preferential demineralization of the with saturated citric acid (pH 1) for 3 minutes. Results
peritubular dentin.33 indicated that the acid had no effect on surfaces that had
Crigger et al.34 studied the effect of saturated citric not been root-planed. After application of the acid to
acid (pH 1) applied topically for 3 minutes in the treat- root-planed surfaces, however, a 4 µ wide zone of
ment of experimental furcation defects in dogs. Thirteen demineralization, not seen in control teeth, was observed.
of 23 acid-treated furcations showed complete formation This zone was characterized by exposed collagen fibrils,
of new attachment, while all of the contralateral control identified by their banding pattern, that were continuous
teeth showed epithelium-lined defects on histologie eval- between the mineralized and the demineralized zones of
uation 6 weeks post-treatment. The authors suggested the root. The authors speculated that the ineffectiveness
cautious interpretation of their results because of the of the acid on the unplaned root surfaces was due to the
artificial nature and lack of chronicity in the experimen- hypermineralization of the root surface previously re-
tal defects and because the anatomy of the canine pre- ported in Periodontitis.2
molar teeth studied provided unusually favorable con- These authors39 proposed some new theories regarding
ditions for tight flap adaptation and protection of the the mechanism of enhanced new attachment using citric
surgical site. Simulated periodontal pockets and the ca- acid. They cited evidence that cementogenesis is en-
nine healing response do not adequately represent the hanced by prior surface résorption or demineraliza-
chronic destructive periodontal lesions seen in humans. tion31' 32,40-44 and suggested that acid demineralization of
Dogs have more dentinal tubules than adult humans, the root surface during therapy might aid new attach-
especially in the cervical area of the root.35 If the mech- ment by reducing or eliminating the need for cell-medi-
anism of enhanced new attachment, due to deminerali- ated root résorption, which normally precedes cemento-
zation, involves mechanical fixation of "cementum pins" genesis. They also believed that the exposed dentinal
into dentinal tubules, then a better response would be collagen fibers observed on root-planed demineralized
expected in dogs. In spite of these drawbacks, however, roots could provide a nidus for direct splicing with new
dogs and other experimental animals have provided a collagen fibrils of the healing flap. This direct collage-
convenient model for histologie studies of new attach- nous type of attachment could occur much sooner after
ment. Nyman et al.36 created periodontal defects in surgery than new attachment mediated by new cemen-
monkeys. They applied saturated citric acid to planed tum. Seven days after surgery, new connective tissue
root surfaces for 3 minutes during flap surgery. They formation is well under way, while cementum formation
observed no new connective tissue attachment in either requires several weeks and is not predictable.45 This
the demineralized teeth or the undemineralized controls. initial attachment of connective tissue could prevent the
Nilvéus et al.37 created furcation defects in the man- establishment of a long junctional epithelium, thereby
J. Periodontol.
614 Nightingale, Sheridan October, 1982

improving the chance for regeneration of cementum, tal defects are rare or lacking. In 1975, Register54 pub-
periodontal ligament and alveolar bone. There is consid- lished an abstract of a project claiming an average of 7
erable evidence to support the concept of predictable mm of reattachment with bone repair 4 months after

new attachment between collagen fibers retained on the flap surgery with adjunctive citric acid treatment in
tooth and the detached fibers of a periodontal flap.46"49 human periodontal defects. A complete published report
Boyko et al.,50 in an electron microscopic study of of this work has not yet followed.
porcine molars demineralized by citric acid, confirmed There are several reports of human case histories.
the presence of formerly mineralized dentinal collagen Register26 reported three successfully treated cases of
fibers on the root surface. They also performed studies deep periodontal defects associated with nonvital, en-
of cell attachment using fibroblast-like cells of the peri- dodontically treated teeth using citric acid, pH 1, applied
odontal ligament of the monkey. They found that more for 2 to 3 minutes, both in conjunction with flap surgery
cells attached to demineralized roots than to undeminer- and introduced directly into the periodontal pocket in
alized roots, in vitro. These authors hypothesized that the conjunction with soft-tissue curettage. Passanezi et al.55
relatively greater attractiveness of demineralized roots to reported two cases of successful new attachment, in
cultured cells may have been due to the exposed collagen which dentin had been etched in situ using 37% phos-
on the root surface, since many cultured cell lines grow phoric acid with laterally sliding flap procedures in
well on collagen substrate.51 They suggested that the humans. Shiloah56 reported two cases of successful new
attractiveness of the collagen substrate covering the de- attachment after laterally sliding flap procedures and
mineralized root surfaces could represent the true mech- demineralization of root-planed dentin with citric acid,
anism of enhanced new attachment. pH 1, for 3 minutes. Otomo and Sims,57 in a controlled
study of coronally repositioned flaps to cover denuded
SURGERY AND CITRIC ACID roots, found that mean postoperative attachment levels
remained constant with preoperative levels in controls
Ririe et al.52'53 studied healing of periodontal connec- and in groups in which demineralization was achieved
tive tissue after surgical wounding and application of
citric acid in dogs. Root surfaces were exposed surgically, by citric acid. Liu and Solt,58 however, found a significant
gain in attachment when root-planed, denuded root sur-
root-planed and etched with citric acid, pH 1, for 3 faces were treated with citric acid, pH 1, for 2 minutes
minutes. Control teeth were not etched. Flaps were
before coronal repositioning of a flap subsequent to a
repositioned at their original level. Block sections were free gingival graft.
obtained at 7, 14, 21, and 42 days and examined with Two studies have considered block sections of human
light and electron microscopy. Compared with the con- teeth and periodontium after flap surgery and root-sur-
trols, the demineralized sites in the same animals showed face demineralization with citric acid. Stahl and Froum09
enhanced connective tissue healing with rapid and con- studied seven periodontally involved anterior and pos-
sistent establishment of connective tissue attachment terior teeth in two patients. After initial procedures that
devoid of initial embedding of collagen fibers in newly included root-planing and curettage, flap surgery was
formed cementum. These authors confirmed the findings
of Garrett et al.39 of a 3- to 5-µ wide zone of deminer- accomplished with further root-planing and application
of citric acid, pH 1, for 2 minutes. The control was
alization and observed interdigitation of new and previ- treated with saline. Sixteen weeks after surgery, block
ously mineralized collagen fibrils as early as 7 days after sections were removed and examined under the light
surgery. The authors likened this mode of connective microscope. Neither accelerated cementogenesis nor new
tissue attachment to dentin to the interdigitation of con- or accelerated attachment of collagen fibers to the for-
nective tissue fibers that occurs in the healing of a soft-
tissue incisional wound. They also observed microscopic
merly exposed areas of the root surfaces was observed.
The authors noted that the exposure to citric acid had
widening of the dentinal tubules in the demineralized no apparent effect on supra-alveolar collagen fibers,
specimens, with collagen fibrils projecting into the tu-
which were left intact on the root surfaces. They also
bules. No significant effects on the dental pulp or the noted that complete removal of cementum from the root
adjacent soft tissues were encountered. Noteworthy, the surfaces was difficult and was not always accomplished.
undemineralized controls also healed, but not as rapidly More extensive clinical trials were suggested to determine
or with the same sequence of events as did the acid-
the usefulness of root demineralization in periodontal
treated sites.
therapy.
Cole et al.60 conducted a similar study of ten surfaces
HUMAN STUDIES
of nine incisor teeth in six patients with chronic Peri-
of newly formed flap collagen with
Interdigitation odontitis. The experimental teeth were not scaled or
previously mineralized dentinal collagen has not been root-planed prior to the study. Full-thickness mucoper-
demonstrated in human material. In addition, reports of iosteal flaps were elevated. A notch was cut in the root
adequately controlled, statistically valid studies of in situ surface through the most apically positioned existing
demineralization used in treatment of human periodon- calculus deposit. The teeth were root-planed in an at-
Volume 53
Number 10 Root Surface Demineralization 615

tempt to remove all cementum, and saturated citric acid eralized dentin may aid in the attachment of new con-
was applied for 5 minutes. The flaps were replaced, nective tissue.81,32 Complete formation of new attach-
sutured and allowed to heal. The patients received tet- ment has been described in acid-treated furcations in
racycline, 250 mg, four times a day for 7 days. They were dogs.34
seen at least once a week in professional hygiene main- Demineralization did not occur when saturated citric
tenance for 4 months after surgery, at which time block acid was applied to untreated diseased and hyperminer-
sections of tooth and periodontium were removed. Light alized extracted human tooth roots; however, application
microscopy revealed regeneration of soft tissue ranging of acid to root-planed surfaces resulted in a zone of
from 1.2 to 2.6 mm coronal to the apical border of the demineralization 4 µ wide.39 These studies indicated
notch. Cementogenesis was observed within the notch in that root-planing of hypermineralized root surfaces is
all ten specimens. Bone was noted coronal to the apical necessary before citric acid application if demineraliza-
border of the notch in four of the ten specimens. The tion is to be achieved. The use of citric acid deminerali-
authors also noted incomplete removal of cementum by zation in conjunction with surgical treatment of artifi-
root-planing. Ankylosis or root résorption was not ob- cially created periodontal defects in dogs has resulted
served. Because of no controls in the study, the authors in enhanced new attachment, including cementogene-
were unable to establish whether or not the acid condi- sis.52, 53
tioning is a prerequisite for new attachment. Encouraging results associated with demineralization
of root surfaces in periodontal therapy in humans have
SUMMARY AND CONCLUSIONS been reported. However, there are no well-controlled
In Periodontitis, root surface alterations have been human studies documenting the efficacy of root surface
noted extending 40 to 100 µ deep to the cementum deminerahzation in the treatment of Periodontitis. Ad-
surface.1 The diseased root surfaces have been demon- ditional clinical investigations are indicated to determine
strated to be hypermineralized,2 and "granules" have the place of root surface demineralization in periodontal
been described in exposed cementum.4"7 therapy.
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