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Periodontology 2000, Vol.

62, 2013, 218–231  2013 John Wiley & Sons A/S


Printed in Singapore. All rights reserved PERIODONTOLOGY 2000

Surgical and nonsurgical


periodontal therapy. Learned
and unlearned concepts
L I S A J. A. H E I T Z -M A Y F I E L D & N I K L A U S P. L A N G

Nonsurgical and surgical periodontal therapies have, tissue shrinkage, leading to pocket-depth reduction.
for several decades, been and remain the basis of In the early 1980s, the value of gingival curettage was
periodontal treatment concepts. However, one must challenged in a split-mouth clinical study where
be aware that the way we treat patients in 2013 is scaling and root planing was performed in all quad-
indeed different from how we treated them 30 years rants and was followed, 4 weeks later, by gingival
ago. We now have a greater understanding of the curettage in two quadrants. Five weeks following
etiologic factors associated with periodontitis, the treatment, similar improvements in periodontal tis-
mechanisms involved in periodontal wound healing sue health were observed, regardless of treatment,
and the inter-relationship between patient factors with a reduction in probing depth and gingival
(such as smoking and diabetes) and treatment out- inflammation, and an increase in clinical attachment
comes. Technological advances have provided clini- level (26). It was concluded that gingival curettage did
cians with a range of options for instrumentation. not result in any additional improvement in peri-
Furthermore, greater emphasis has been placed on odontal tissue health and, as a result, intentional soft-
the importance of patient-centered outcomes in tissue curettage was phased out.
clinical research.
We have learned a lot during these past years,
having been fortunate enough to learn from the Removal of contaminated root
experience of some very famous periodontists from cementum
all over the world. Research in periodontology has,
for much of the last 50 years, exceeded that of any In the 1970s and 1980s nonsurgical periodontal ther-
other dental specialty. In addition to the sheer vol- apy was performed using predominately hand instru-
ume of investigative work, education and teaching in mentation, with the aim being to remove supragingival
periodontology have been underpinned by the criti- and subgingival calculus and plaque, and contami-
cal evaluation of both old and new concepts. So what nated root cementum. Historically it was thought that
have we learned in relation to nonsurgical and sur- aggressive scaling and root planing was required
gical periodontal therapy, and what has changed over to remove bacterial products (lipopolysaccharide ⁄
the past few decades? endotoxin) bound to the contaminated root surface
(22). We have since learned from in-vitro studies that
bacterial endotoxins are weakly adherent to root sur-
Gingival curettage faces and therefore excessive removal of cementum is
not required to remove bacterial products (14, 45, 75,
In the 1970s, scaling and root planing combined with 79). The concept of removal of contaminated cemen-
gingival curettage was a common procedure for tum and hard-tissue deposits as the key to successful
periodontal therapy. Gingival curettage, defined as periodontal treatment was challenged in a clinical
the removal, by means of a curette, of the inner study published in 1995 (73). In this study mucope-
surface of the soft-tissue wall of the pocket, was riosteal flaps were raised following supragingival
performed in order to promote new attachment and debridement and oral-hygiene instruction, and

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bone was recontoured to eliminate angular bony ing adjunctive antimicrobials via a systemic, local or
defects. While the control teeth were thoroughly root topical route.
planed, the test teeth were not instrumented other
than to chip off large calculus deposits using the tip of a
scaler, followed by irrigation with sterile saline. Flaps Evidence-based periodontology
were apically repositioned at the level of the bone crest.
One year after therapy, clinical and microbiological Evidence-based periodontology has been described
parameters showed similar improvements at test and as a tool to support decision-making and integrate
control teeth with reductions in probing depths and in the best available evidence into clinical practice (80).
the proportions of periodontal pathogens (Porphyro- The systematic review, as opposed to the traditional
monas gingivalis, Fusobacterium sp. and Campylo- narrative review, provides a comprehensive appraisal
bacter rectus). It was concluded that the reduction of of research using transparent methods whilst aiming
selected gram-negative anaerobic organisms in the to minimize bias (81). In 2002, the 4th European
subgingival plaque is a more important element for the Workshop on Periodontology was held in Ittingen,
success of periodontal therapy than is the removal Switzerland, and for the first time for a major work-
of contaminated root cementum and mineralized shop, all reviews were carried out as systematic re-
deposits by root planing (73). Furthermore, in an views. These were discussed by a select group of 60
experimental study it was observed, using electron periodontists, most of whom were unfamiliar with
microscopy, that the epithelial attachment on calculus the new system, so the learning curves were steep.
that had been treated with chlorhexidine gluconate After much discussion and debate, the systematic
had the same ultrastructure as normal epithelial reviews were accepted and published in the Journal
attachment on various tooth surfaces (60). Periodontal of Clinical Periodontology; from this, some old con-
healing occurred, even in the presence of calculus, cepts were unlearned, some were confirmed and
provided that the subgingival bacterial plaque some new ones were introduced.
had been removed. From this we learned that while The introduction of the systematic review process
the removal of calculus is important because it is a to periodontology has also influenced the way in
major plaque-retentive factor, the intentional removal which research has been designed and reported over
of root substance and contaminated cementum is the past decade. The randomized controlled trial,
not required for successful treatment. Thus, the term considered to be the highest level of evidence, has
Ôroot planingÕ is now frequently referred to as been strongly promoted to be used when appropri-
ÔdebridementÕ. ate. The Consolidated Standards of Reporting Trials
guidelines have also been more widely promoted.
Furthermore patient-based analyses, as opposed to
Periodontal biofilms periodontal site-based analyses, are now considered
as the standard. Systematic reviews published in the
The end of the 20th century saw some great advances last decade have addressed a number of focused
in techniques for microbial analysis. With the use of questions related to nonsurgical and surgical peri-
molecular identification techniques, checkerboard odontal therapy. This has led to a greater under-
DNA–DNA hybridization, biofilm models, fluores- standing of the combined results of research pub-
cence in-situ hybridization and confocal scanning lished over previous decades, and to identification of
laser microscopy, our understanding of the complex areas where further research is required.
nature, composition and role of periodontal biofilms
in health and disease expanded significantly (65, 66,
115, 118, 119). Recent elucidation of the human oral Nonsurgical periodontal therapy
microbiome and the identification of new species
associated with periodontitis have established that Manual debridement vs. machine-driven
the periodontal microflora is extremely diverse (24, debridement
128). These advances have had a significant impact
on microbial diagnostics and on our understanding Most studies in the 1970s and 1980s were conducted
of bacterial cell interactions and antimicrobial-resis- using hand instruments, including curettes, scalers
tance mechanisms. In particular, they underpinned and hoes, and this was considered the Ôgold standardÕ.
the necessity for the thorough mechanical removal or Since the 1990s, the use of powered instruments,
disruption of the periodontal biofilm when prescrib- including the magnetostrictive and piezoelectric

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ultrasonics, the linear oscillating device (Vector- included studies and concluded that further well-
system) and sonic instruments, have become designed studies are required to determine the
increasingly popular, with claims of increased efficacy effectiveness of the Er:YAG laser for nonsurgical
and efficiency (123, 130). Some studies have reported a treatment of chronic periodontitis (107).
reduced time for scaling and root planing, improved
access, less damage to the root surface and less dis-
Photodynamic therapy
comfort for the patient using slimline tip designs (12).
However, overall, similar positive clinical and micro- Antimicrobial photodynamic therapy, used alone or
biological outcomes were achieved with the use of as an adjunct to scaling and root planing, was
machine-driven and hand instrumentation, and even introduced in the late 1990s and involves the use of
newer designs of powered instruments have so far not low-power lasers with appropriate wavelength to
shown any further benefit when compared with other target microorganisms treated with a photosensitizer.
ultrasonic devices in nonsurgical periodontal therapy A systematic review published in 2011, which in-
(48, 123, 130). cluded seven randomized controlled trials with a
Studies by Badersten and co-workers in the 1980s, parallel design, concluded that the use of photody-
using hand instruments, found that the effectiveness namic therapy adjunctive to scaling and root planing
of calculus removal is influenced by initial pocket provides short-term benefits, but microbiological
depth, tooth type and surface, as well as operator outcomes are contradictory (110). Six of seven studies
experience (5–7). As probing depths increase, elimi- included in the review evaluated photodynamic
nation of calculus and associated biofilm becomes therapy plus scaling and root planing vs. scaling and
more challenging, with studies reporting a higher root planing alone, whilst two studies compared
percentage of residual calculus on root surfaces in photodynamic therapy with scaling and root planing.
pockets with probing depths of >6 mm (up to 44%) No evidence of the effectiveness for the use of anti-
compared with pockets with probing depths of 4– microbial photodynamic therapy as an alternative to
5 mm (up to 29%; 30, 92). These findings have been scaling and root planing was found. The authors
confirmed in studies evaluating machine-driven concluded that long-term randomized controlled
instrumentation (130). trials reporting data on microbiological changes and
Adverse outcomes following nonsurgical debride- costs are needed to support the long-term efficacy
ment may include patient discomfort, root-surface of adjunctive antimicrobial photodynamic therapy
damage and root-surface sensitivity (48). Overzealous (110).
debridement should be avoided in sites with shallow
probing depths (<3 mm) to avoid trauma and sub-
Pocket irrigation with antiseptics
sequent attachment loss and root-surface sensitivity
(57). The use of antiseptics in nonsurgical periodontal
therapy may include pocket irrigation. Antiseptics,
including povidone-iodine, dilute sodium hypochlo-
Lasers
rite and chlorhexidine gluconate, have been used for
In the 1990s the erbium-doped:yttrium-aluminium- periodontal pocket irrigation following debridement
garnet (Er:YAG) laser was introduced for periodontal with the aim of suppressing the biofilm. Some studies
therapy; however, the clinical effectiveness of the have shown further reduction in periodontal patho-
Er:YAG laser remains controversial. A systematic re- gens and probing depths compared with scaling and
view, including five randomized controlled trials of root planing alone (95, 97, 102, 103). As gingival
split-mouth design, evaluated the effectiveness of the crevicular fluid within a periodontal pocket is re-
Er:YAG laser in the treatment of chronic periodontitis placed every 90 s, the effects of antiseptic pocket
as an alternative therapeutic strategy to scaling and irrigation are only transient and the risks of antisep-
root planing (112). Meta-analyses showed no statis- tics penetrating the gingival tissue and causing sys-
tically significant difference in clinical attachment temic effects are minimized. Nevertheless, care
gain, probing-depth reduction or change in gingival should be taken to check the patientÕs medical history
recession, indicating no evidence of a superior as povidone-iodine can cause allergic reactions and
effectiveness of the Er:YAG laser compared with should not be used in patients with thyroid dys-
scaling and root planing (112). The results were in function or during pregnancy or breastfeeding (116).
agreement with an earlier systematic review, pub- While a recent systematic review shows that
lished in 2008, which observed heterogeneity of adjunctive use of povidone-iodine irrigation of

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pockets during nonsurgical periodontal therapy may time. Although some of these locally applied anti-
offer a small increase in probing-depth reduction microbial systems have been shown to offer some
(104), overall the use of antiseptic irrigants delivered benefit over scaling and root planing alone, the ef-
in conjunction with powered instruments has not fects were modest and mostly short term. In a sys-
shown any advantage (106). tematic review published in 2003, a meta-analysis of
19 studies that included scaling and root planing and
Full-mouth disinfection local sustained-release agents compared with scaling
and root planing alone, indicated significant
In the 1990s the convention of staged debridement adjunctive probing-depth reduction or clinical
with quadrant or sextant instrumentation at 1- to 2- attachment gain for minocycline gel, microencapsu-
week intervals was challenged with the introduction lated minocycline, chlorhexidine chip and doxycy-
of the full-mouth disinfection approach aimed at cline gel (39). In a subsequent systematic review,
preventing re-infection from untreated pockets (90). published in 2005, the most positive results occurred
The full-mouth disinfection protocol includes full- for adjunctive tetracycline, minocycline, metronida-
mouth scaling and root planing within 24 h, in zole and chlorhexidine, with modest improvements
addition to twice-daily chlorhexidine mouthrinsing, in probing-depth reductions compared with scaling
tongue scraping, chlorhexidine tonsil spraying and and root planing alone (11). The authors questioned
subgingival irrigation with chlorhexidine three times the clinical significance of these small improvements.
within 10 min and repeated after 8 days. The full- Furthermore, some of the subgingival antimicrobial-
mouth scaling and root planing protocol includes delivery systems developed for clinical use are no
full-mouth scaling and root planing without anti- longer available.
septics. Two systematic reviews, combining the re-
sults of a number of randomized controlled trials,
concluded that all three treatment approaches may Nonsurgical therapy and
be recommended for nonsurgical periodontal ther- adjunctive systemic antimicrobials
apy (25, 53).
Thus, while technological advances have intro- The adjunctive use of systemic antimicrobials for
duced a range of different instruments and novel periodontal therapy has been discussed for many
techniques over the past decades, the critical factor decades. Owing to the heterogeneity of the study
for successful nonsurgical periodontal therapy re- designs employed to assess the efficacy of systemi-
mains the thoroughness of root debridement and the cally administered antimicrobial agents, it is difficult
patientÕs standard of oral hygiene, rather than the to reach a conclusion regarding whether or not there
treatment modality. Therefore, operator and patient are clinical benefits, the type of drug that should be
preference may play a large part in determining the prescribed and the dose, and the most effective
choice of instrumentation for nonsurgical therapy, timing of drug administration in relation to
including the choice between staged debridement, mechanical therapy. Most studies have evaluated
full-mouth disinfection and full-mouth scaling and systemic antimicrobials in conjunction with nonsur-
root planing. gical debridement, the rationale for their use being
the suppression of periodontal pathogens persisting
in biofilms in deep pockets, root furcations and
Nonsurgical therapy and concavities or residing within the periodontal tissues.
adjunctive local antimicrobial In particular the periodontal pathogen Actinobacillus
delivery actinomycetemcomitans has been reported to be dif-
ficult to eradicate with nonsurgical therapy alone (72,
Local delivery of antibacterial agents into periodontal 74, 87). The persistence of A. actinomycetemcomitans
pockets has been investigated since the late 1970s, and other periodontal pathogens has been associated
and various antimicrobials and delivery systems have with continued progression of disease compared with
been developed with the aim of maintaining high improved clinical outcomes when these organisms
levels of antimicrobial agents in the crevicular fluid are not detected following therapy (21). Despite the
with minimal systemic uptake. All are intended for obvious possible benefits of targeting periodontal
use as adjunctive therapies, with scaling and root biofilms with antimicrobials there has been a con-
planing providing substantivity of an antimicrobial sensus that, owing to the risk of adverse effects,
system at an effective concentration of drug over including the development of bacterial antimicrobial

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resistance, interactions with other drugs and possible 0.45 mm in deep pockets (probing depth ‡6 mm) in
allergic reactions (91, 108, 125), systemic antimicro- 19 (83%) of 23 comparisons (38).
bials should be used in select cases where microbial In the past decade there has been further evidence
diagnostics indicate the presence of high levels of to support the use of systemic antimicrobials, in
periodontal pathogens (A. actinomycetemcomitans combination with nonsurgical debridement, for
and P. gingivalis) or in patients diagnosed with treatment of patients with advanced disease and
aggressive periodontitis. deep pockets (probing depth >6 mm) with the aim
The use of adjunctive systemic antimicrobials for of reducing the need for additional therapy.
nonsurgical treatment of chronic or aggressive peri- While a range of systemic antimicrobials, including
odontitis was evaluated in two systematic reviews: azithromycin (23, 36, 67, 105, 117), spiramycin (3, 8),
one in 2002 (43) and the other in 2003 (38). From tetracycline (3, 37, 41, 55, 87, 93), clindamycin (64,
the limited meta-analyses that could be performed, 113), doxycycline (28, 82, 113), metronidazole (17, 54,
a statistically significant additional benefit for 61, 62, 83, 85, 86, 100, 113, 120, 131, 137), amoxicillin
spiramycin (probing-depth change = 0.41 mm) and and clavulanic acid (37, 64, 89, 132) and amoxicillin
amoxicillin plus metronidazole (clinical attachment (100), has been included in clinical studies, the
change = 0.45 mm) in deep pockets (probing depth combination of metronidazole and amoxicillin has
>6 mm) was observed (43; Table 1). We learned that recently been the most widely documented (9, 10, 15,
systemic antimicrobials, in conjunction with scaling 27, 35, 68, 69, 100, 114, 121, 127, 133, 135, 136) for
and root planing, can offer an additional benefit over adjunctive treatment of chronic and aggressive peri-
scaling and root planing alone in terms of probing- odontitis. Cionca et al. (15) found that systemic
depth reduction, clinical attachment gain and re- metronidazole, combined with amoxicillin, signifi-
duced risk of additional clinical attachment loss. cantly improved the 6-month clinical outcomes of
Herrera et al. (43) concluded, in their systematic re- full-mouth nonsurgical periodontal debridement,
view, that patients with deep pockets, ÔactiveÕ or thus significantly reducing the need for additional
progressive periodontitis or a specific microbiological therapy.
profile might benefit from adjunctive systemic anti- Ten years after the first systematic reviews were
microbials. The authors, however, cautioned that the published, a large multicenter randomized controlled
evidence was limited and that the decision to pre- trial confirmed the adjunctive benefit of the combi-
scribe systemic antibiotics should be made on an nation of amoxicillin and metronidazole with scaling
individual patient basis, taking into account the and root planing on clinical attachment gain and
possibility of adverse events. Haffajee et al. (38) probing-depth reduction for the treatment of mod-
concluded that systemically administered antimi- erate chronic periodontitis (32). At 3 months, scaling
crobials were uniformly beneficial in providing an and root planing alone resulted in pronounced
improvement in clinical attachment gain when used probing-depth reduction at sites with initially deep
as adjuncts to scaling and root planing. Overall, pockets (probing depth ‡5 mm) and some clinical
adjunctive systemic antimicrobials provided a mean attachment gain. While adjunctive antimicrobials did
benefit, at 6 months, of clinical attachment change of not improve the clinical outcomes at 3 months, at
0.29 mm in shallow pockets (probing depth <4 mm) 24 months there was significantly more clinical
in seven (87%) of eight comparisons, of 0.29 mm in attachment gain (0.5 mm) and probing-depth
moderate pockets (probing depth 4–5 mm or 4– reduction (0.5 mm) in the group who received
6 mm) in eight (80%) of 10 comparisons and of adjunctive systemic amoxicillin and metronidazole.

Table 1. Adjunctive systemic antimicrobials for nonsurgical treatment of chronic or aggressive periodontitis in deep
pockets. Initial probing depth >6 mm.

Drug Variable Pooled 95% confidence P-value References


estimate interval for estimate

Spiramycin Probing-depth reduction 0.41 mm 0.08–0.73 0.014 (3, 8)


Amoxicillin ⁄ Clinical attachment gain 0.45 mm 0.19–0.71 0.001 (10, 29)
metronidazole
Meta-analyses of the differences in treatment effect between scaling and root planing and scaling and root planing plus systemic antimicrobials. From Herrera et al.
(43). Studies include patients diagnosed with either chronic or aggressive periodontitis.
Pooled estimate represents the difference (in mm) in favor of scaling and root planing plus the systemic antimicrobial therapy.

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Smoking reduced clinical attachment gain and A systematic review including four randomized
probing pocket-depth reduction in both treatment controlled trials (27, 68, 114, 125, 133), which evalu-
groups (32). ated the effect of systemic amoxicillin and metroni-
A recent systematic review included studies (ran- dazole in combination with scaling and root planing
domized controlled trials and case series) in patients in patients with chronic periodontitis, also reported a
diagnosed with aggressive (1, 2, 9, 13, 34, 35, 42, 49, clinical benefit of this antibiotic combination com-
51, 63, 69, 76, 99, 124, 127, 135, 136) or chronic (10, pared with scaling and root planing alone (109). The
15, 16, 27, 31, 32, 70, 71, 78, 114, 126, 133, 134) results of the meta-analyses showed significantly
periodontitis, and aimed to estimate the size of the more clinical attachment gain (0.2 mm) and probing-
effect when systemic amoxicillin and metronidazole depth reduction (0.4 mm) in favor of scaling and root
were combined with scaling and root planing (138; planing in conjunction with amoxicillin ⁄ metronida-
Table 2). An indirect comparison was made with data zole. No significant differences were found for
from another review that analyzed the overall effect bleeding on probing or suppuration [Sgolastra et al.
of nonsurgical therapy alone (18). The authors con- (109); Table 3].
cluded that the adjunctive use of amoxicillin and Thus, in 2012 we have a greater body of research to
metronidazole resulted in additional clinical benefits support the adjunctive use of some systemic antimi-
compared with scaling and root planing alone (18, crobials in nonsurgical periodontal therapy. The main
138). effect of this adjunctive benefit is observed in patients
Another systematic review, published in 2012, in- with deep pockets (initial probing depth >6 mm) or in
cluded six randomized controlled trials (9, 35, 69, 127, patients diagnosed with aggressive periodontitis. The
135, 136) in patients with aggressive periodontitis most well-documented systemic antimicrobial drug
who had been treated with scaling and root planing, regimen is the combination of amoxicillin and met-
alone, or in combination with amoxicillin and met- ronidazole, which is most commonly administered for
ronidazole (111). The results of the meta-analysis 7–14 days at the completion of scaling and root plan-
analyzing full-mouth data showed significantly more ing. The prescribed dosage varies from to 250–500 mg
clinical attachment gain (0.4 mm) and probing-depth of amoxicillin three times a day and 250–400 mg of
reduction (0.6 mm) in favour of full-mouth scaling metronidazole three times a day.
and root planing and systemic amoxicillin and met- This, however, does not mean that indiscriminate
ronidazole with no significant risk of adverse events use of systemic antimicrobials should be advocated.
(Table 3). The decision to use adjunctive systemic antimicro-

Table 2. Probing-depth reduction (A) and clinical attachment gain (B) (pre- and post-treatment) following scaling
and root planing in conjunction with the combination of amoxicillin and metronidazole

Baseline Weighted mean 95% References For comparison


probing difference ± standard confidence (scaling and root
depth deviation (mm) interval planing alone) Cobb (18)

(A) Probing-depth reduction


4–6 mm 1.47 ± 0.22 1.52–1.42 (34, 35, 76, 133) 1.29

>4 mm 2.17 ± 0.62 2.3–2.04 (15, 16, 32, 70, 98)


‡6 mm 2.59 ± 033 2.65–2.53 (1, 124, 126, 134)

‡7 mm 3.72 ± 0.66 3.83–3.61 (13, 34, 35, 51, 76, 98, 133) 2.16
Baseline Weighted mean 95% References For
probing difference ± standard confidence comparison,
depth deviation (mm) interval Cobb (18)
(B) Clinical attachment gain
4–6 mm 1.31 ± 0.33 1.24–2.73 (51, 70, 71, 124) 0.55
>4 mm 1.49 ± 0.42 1.40–1.58 (15, 16, 32, 70)
‡6 mm 1.66 ± 0.66 1.54–1.78 (1, 126, 134)
‡7 mm 2.66 ± 0.88 2.51–2.81 (13, 34, 35, 51, 76, 98, 133) 1.19
From Zandbergen et al. (138).
Results presented according to initial probing-depth categories.
For comparison, data from Cobb (18), describing the pre- and post-treatment effect of scaling and root planing alone, are presented. Studies include patients
diagnosed with either chronic or aggressive periodontitis.

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Table 3. Clinical therapeutic efficiency of scaling and root planing vs. scaling and root planing plus systemic
amoxicillin + metronidazole in patients with chronic periodontitis* (A) (109) and aggressive periodontitis  (B) (111)

Mean difference 95% confidence P-value for estimate in favor of scaling


Full-mouth analysis (mm) interval and root planing + amoxicillin ⁄ metronidazole

(A) Chronic periodontitis


Clinical attachment gain 0.21 0.02–0.4 <0.05

Probing-depth reduction 0.43 0.24–0.63 <0.05


Full-mouth analysis Mean 95% P-value for estimate in favor of scaling and
difference confidence root planing + amoxicillin ⁄ metronidazole
(mm) interval
(B) Aggressive periodontitis
Clinical attachment gain 0.42 0.23–0.61 <0.00001
Probing-depth reduction 0.58 0.39–0.77 <0.0004
*From Sgolastra et al. (109): randomized controlled trials included refs (27, 68, 114 and 133). Follow-up varied from 3 to 24 months.
 From Sgolastra et al. (111): randomized controlled trials included refs (9, 35, 69, 127, 135 and 136).

bials should be made on an individual basis, and odontal tissues, the pathogenesis of periodontal
adequate debridement, good oral hygiene and disease and the mechanisms of periodontal wound
maintenance care are still the most important criteria healing, the necessity for pocket elimination was also
for successful treatment outcomes. The reliance on challenged. We learned that the main goal of peri-
patient compliance must be taken into account when odontal surgery was to gain access to the root surface
considering the use of adjunctive systemic antimi- for adequate debridement and to establish gingival
crobials. contours that are optimal for the patientÕs self-per-
formed plaque control. The access flap (including
the numerous techniques described over nearly
Surgical periodontal therapy 100 years: the original Widman flap described in
1918, the Neumann flap described in 1920, the
In the 1970s and 1980s we learned, from some modified flap operation described by Kirkland in
important clinical trials, that nonsurgical periodontal 1931, the apically repositioned flap described by
therapy is effective in eliminating inflammation in Friedman in 1962 and the modified Widman flap
deep pockets and in improving clinical attachment described by Ramfjord & Nissle in 1974) enabled
levels (4, 44, 77). However, we also learned that, de- access to the root surfaces, root concavities and fur-
spite our best efforts at meticulous nonsurgical cations for adequate debridement. The type of sur-
instrumentation, residual plaque and calculus may gery performed in the 1970s and 1980s was largely
still be found (129). It was accepted that in situations dependent on the philosophy of each dental school.
where signs of inflammation persist, surgical therapy A number of clinical trials in the 1970s and early
may be indicated. 1980s, evaluating the potential of periodontal sur-
Periodontal surgery was historically advocated for gery, revealed that in patients meeting high standards
the removal of diseased tissue, with the predominant of oral hygiene the surgical technique used to gain
technique being excision of the diseased gingival access for thorough debridement of the root surfaces
tissue by gingivectomy and removal of what was was of minor importance for the overall long-term
thought to be necrotic bone. Upon the discovery that result (52, 94, 101). We also learned the importance of
periodontal disease did not result in necrosis of bone, postoperative plaque control in determining the
and that gingival inflammation and bone loss repre- outcome of periodontal surgery. In a study evaluating
sented a defense reaction, this concept was aban- periodontal surgery, patients who did not have ade-
doned. Pocket elimination then became the main quate plaque control continued to lose attachment,
objective of periodontal therapy, and the gingivec- irrespective of the type of surgery they received (84).
tomy or apically positioned flap procedures were Patients who had adequate plaque control had long-
commonly performed to eliminate the periodontal term maintenance of clinical attachment levels,
pocket and allow access to the root surface for scaling demonstrating that the success of surgical peri-
and oral-hygiene procedures. In the 1980s, with a odontal therapy is aligned to the quality of the
greater understanding of the biology of the peri- maintenance care and plaque control (84). Provided

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that proper postoperative plaque-control levels are gical treatment of chronic periodontal disease, were
established and maintained, most surgical-treatment included. Meta-analyses indicated that 12 months
techniques will result in conditions that favor the following treatment, surgical therapy resulted in
long-term maintenance of the periodontium. 0.6 mm more probing-depth reduction and in
We also learned the importance of subject-related 0.2 mm more clinical attachment gain than did
factors, including compliance and smoking, as they nonsurgical therapy in deep pockets (>6 mm). In
relate to periodontal wound healing and treatment pockets of 4–6 mm, scaling and root planing resulted
outcomes following surgical therapy (47). in 0.4 mm more clinical attachment gain and 0.4 mm
In recent years, refinement of periodontal surgical less probing-depth reduction than did surgical ther-
techniques has been possible with development of apy. Therefore, when considering surgery in pockets
new instrumentation and the use of illumination and of 4–6 mm, the advantage in probing-depth reduc-
magnification. Minimally invasive periodontal surgi- tion should be balanced against the disadvantage in
cal approaches and microsurgical techniques are clinical attachment gain. In shallow pockets (1–
currently being evaluated and may show advantages 3 mm), nonsurgical therapy resulted in 0.5 mm less
in wound-healing outcomes and less recession and clinical attachment loss compared with surgical
patient morbidity (19, 20, 33, 96, 122). A recent sys- therapy (Table 4). From this systematic review it was
tematic review showed that periodontal surgery for concluded that both scaling and root planing alone
the treatment of intrabony defects was associated with and scaling and root planing combined with a flap
high tooth retention and improvement of periodontal procedure are effective methods for the treatment of
clinical parameters, and that clinical attachment gain chronic periodontitis, in terms of attachment gain and
may be greater when a papilla preservation flap is reduction in gingival inflammation. Furthermore, in the
used in comparison with an access flap (33). The pa- treatment of deep pockets (probing depth >6 mm),
pilla preservation technique is one of a number of open-flap debridement results in greater probing-depth
techniques developed as part of the surgical approach reduction and clinical attachment gain (40). Long-
to regenerative therapy, which is discussed in another term treatment outcomes available from studies
article in this volume of Periodontology 2000. comparing nonsurgical with surgical treatment sug-
gest that both treatment modalities are equally
effective in establishing gingival health and prevent-
Surgical debridement vs. nonsurgical ing further loss of attachment (40).
debridement
In 2002, Heitz-Mayfield et al. (40) evaluated the
effectiveness of surgical vs. nonsurgical therapy for Critical probing depth for decision
the treatment of chronic periodontitis in a systematic making
review. Six randomized controlled studies of split-
mouth design, published from 1982 to 1996 (46, 50, On the basis of clinical outcome data from a longitu-
56, 59, 88, 94) and comparing surgical with nonsur- dinal randomized controlled clinical trial in 15 patients

Table 4. Clinical therapeutic efficiency of nonsurgical therapy vs. surgical therapy 12 months after treatment

Initial Outcome variable Weighted 95% P-value for Conclusion


probing mean confidence weighted
depth difference interval mean
(mm)a difference

1–3 mm Clinical attachment gain )0.51 )0.73 to )0.29 0.000 Favors scaling
and root planing
4–6 mm Probing-depth reduction 0.35 0.23 to 0.45 0.000 Favors surgery

4–6 mm Clinical attachment gain )0.37 )0.49 to )0.26 0.000 Favors scaling
and root planing
>6 mm Probing-depth reduction 0.58 0.38 to 0.79 0.000 Favors surgery

>6 mm Clinical attachment gain 0.19 0.04 to 0.35 0.017 Favors surgery
The results are presented according to initial probing-depth categories.
*(Weighted mean difference between surgical therapy and nonsurgical therapy (scaling and root planing).
From Heitz-Mayfield et al. (40).

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Fig. 1. Regression analysis leading


to critical probing depth as a basis
for the decision-making process in
periodontal therapy (from Lindhe
et al. (58)). MWF, modified Widman
flap; RPL, scaling and root planing.

with advanced periodontitis (58), a concept of ‘‘critical may be used as a guideline in the clinical decision-
probing depth’’ was developed for decision making making process on periodontal therapy.
following the completion of a hygienic phase [initial
periodontal therapy (non-surgical therapy + oral hy-
giene instruction)]. The critical probing depth repre- Conclusions
sents a baseline probing-depth value above which the
outcome of a therapy will result in attachment gain and While we have learned a great deal over the past
below which the outcome of therapy will result in decades and have been introduced to new techniques
clinical attachment loss (Fig. 1). In the present illus- and technologies, this new information has not
tration the critical probing depth for nonsurgical ther- diminished our recognition of the importance of
apy (scaling and root planing) is 2.9 mm. This, in turn, thorough mechanical debridement and optimal pla-
means that below this probing depth the site would lose que control for successful nonsurgical and surgical
clinical attachment as a result of therapy. However, periodontal therapy.
above this value clinical attachment gain will result. On • We have learned that while a thorough disruption
the other hand, for the access flap therapy, the critical and removal of the periodontal biofilm is required
probing depth is 4.2 mm. Again, this means that open for successful treatment outcomes, removal of the
flap debridement is only beneficial above this value, root surface is not necessary.
while below this value, attachment loss may result. • We have learned that the use of specific systemic
Looking at the data from both scaling and root antimicrobials, in patients with advanced or
planing and access flap surgery, another critical aggressive periodontitis and deep probing depths,
probing depth is 5.4 mm. This, in turn, means that may be beneficial as an adjunct to nonsurgical
flap surgery is indicated predominantly with a prob- periodontal therapy, thereby reducing the need for
ing depth of ‡5.4 mm, while between 2.9 mm and additional therapy.
5.4 mm nonsurgical therapy is to be preferred. • We have learned that full-mouth disinfection and
It has to be borne in mind, however, that these full-mouth scaling and root planing protocols can
critical probing-depth values represent mean scores be an equivalent treatment option to conventional
with a modest variation. Nevertheless, the principle quadrant debridement.

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Periodontal therapy

• We have learned that in patients with deep pockets 11. Bonito AJ, Lux L, Lohr KN. Impact of local adjuncts to
(>6 mm), access flap surgery may be beneficial, scaling and root planing in periodontal disease therapy: a
systematic review. J Periodontol 2005: 76: 1227–1236.
provided the patient receives regular supportive
12. Braun A, Jepsen S, Krause F. Subjective intensity of pain
periodontal therapy and has adequate oral hygiene. during ultrasonic supragingival calculus removal. J Clin
• We have learned that the value of new technologies Periodontol 2007: 34: 668–672.
and concepts may not be known for some time 13. Casarin RC, Ribeiro ED, Sallum EA, Nociti- FH Jr, Gon-
after their introduction. Proper evaluation requires calves RB, Casati MZ. The combination of amoxicillin and
metronidazole improves clinic and microbiologic results
adequate follow-up in well-conducted studies of
of one-stage, full mouth, ultrasonic debridement in
sufficient sample size. aggressive periodontitis treatment. J Periodontol 2012: 8:
• We have learned that an unbiased and transparent 988–998.
appraisal of the literature, using the systematic 14. Cheetham WA, Wilson M, Kieser JB. Root surface
review process, may change our paradigms. debridement – an in vitro assessment. J Clin Periodontol
• Sometimes we need to be prepared to unlearn old 1988: 15: 288–292.
15. Cionca N, Giannopoulou C, Ugolotti G, Mombelli A.
concepts in order to learn new ones. Amoxicillin and metronidazole as an adjunct to full-
mouth scaling and root planing of chronic periodontitis.
J Periodontol 2009: 80: 364–371.
References 16. Cionca N, Giannopoulou C, Ugolotti G, Mombelli A. Mi-
crobiologic testing and outcomes of full-mouth scaling
1. Aimetti M, Romano F, Guzzi N, Carnevale G. Full-mouth and root planing with or without amoxicillin ⁄ metroni-
disinfection and systemic antimicrobial therapy in gen- dazole in chronic periodontitis. J Periodontol 2010: 81: 15–
eralized aggressive periodontitis: a randomized, placebo- 23.
controlled trial. J Clin Periodontol 2012: 39: 284–294. 17. Clark DC, Shenker S, Stulginski P, Schwartz S. Effective-
2. Akincibay H, Orsal SO, Sengun D, Tozum TF. Systemic ness of routine periodontal treatment with and without
administration of doxycycline versus metronidazole plus adjunctive metronidazole therapy in a sample of mentally
amoxicillin in the treatment of localized aggressive peri- retarded adolescents. J Periodontol 1983: 54: 658–665.
odontitis: a clinical and microbiologic study. Quintessence 18. Cobb CM. Clinical significance of non-surgical periodon-
Int 2008: 39: e33–e39. tal therapy: an evidence-based perspective of scaling and
3. Al-Joburi W, Quee TC, Lautar C, Iugovaz I, Bourgouin J, root planing. J Clin Periodontol 2002: 29(Suppl 2): 6–16.
Delorme F, Chan EC. Effects of adjunctive treatment of 19. Cortellini P, Tonetti MS. Improved wound stability with a
periodontitis with tetracycline and spiramycin. J Period- modified minimally invasive surgical technique in the
ontol 1989: 60: 533–539. regenerative treatment of isolated interdental intrabony
4. Axelsson P, Lindhe J. Effect of controlled oral hygiene defects. J Clin Periodontol 2009: 36: 157–163.
procedures on caries and periodontal disease in adults. 20. Cortellini P, Tonetti MS. Clinical and radiographic out-
J Clin Periodontol 1978: 5: 133–151. comes of the modified minimally invasive surgical tech-
5. Badersten A, Nilveus R, Egelberg J. Effect of nonsurgical nique with and without regenerative materials: a
periodontal therapy. III. Single versus repeated instru- randomized-controlled trial in intra-bony defects. J Clin
mentation. J Clin Periodontol 1984: 11: 114–124. Periodontol 2011: 38: 365–373.
6. Badersten A, Nilveus R, Egelberg J. Effect of non-surgical 21. Dahlén G, Wikström M, Renvert S. Treatment of peri-
periodontal therapy (IV). Operator variability. J Clin Peri- odontal disease based on microbiological diagnosis. A 5-
odontol 1985: 12: 190–200. year follow-up on individual patterns. J Periodontol 1996:
7. Badersten A, Nilveus R, Egelberg J. Effect of nonsurgical 67: 879–887.
periodontal therapy (VIII). Probing attachment changes 22. Daly CG, Kieser JB, Corbet EF, Seymourt GJ. Cementum
related to clinical characteristics. J Clin Periodontol 1987: involved in periodontal disease: a review of its features
14: 425–432. and clinical management. J Dent 1979: 7: 185–193.
8. Bain CA, Beagrie GS, Bourgoin J, Delorme F, Holthuis A, 23. Dastoor SF, Travan S, Neiva RF, Rayburn LA, Giannobile
Landry RG, Roy S, Schuller P, Singer D, Turnbull R. The WV, Wang HL. Effect of adjunctive systemic azithromycin
effects of spiramycin and ⁄ or scaling on advanced peri- with periodontal surgery in the treatment of chronic peri-
odontitis in humans. J Can Dent Assoc 1994: 60: 209, 212– odontitis in smokers: a pilot study. J Periodontol 2007: 78:
217. 1887–1896.
9. Baltacioglu E, Aslan M, Sarac O, Saybak A, Yuva P. Analysis 24. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu
of clinical results of systemic antimicrobials combined WH, Lakshmanan A, Wade WG. The human oral microb-
with nonsurgical periodontal treatment for generalized iome. J Bacteriol 2010: 192: 5002–5017.
aggressive periodontitis: a pilot study. J Can Dent Assoc 25. Eberhard J, Jervoe-Storm PM, Needleman I, Worthington
2011: 77: b97. H, Jepsen S. Full-mouth treatment concepts for chronic
10. Berglundh T, Krok L, Liljenberg B, Westfelt E, Serino G, periodontitis: a systematic review. J Clin Periodontol 2008:
Lindhe J. The use of metronidazole and amoxicillin in the 35: 591–604.
treatment of advanced periodontal disease. A prospective, 26. Echeverria JJ, Caffesse RG. Effects of gingival curettage
controlled clinical trial. J Clin Periodontol 1998: 25: 354– when performed 1 month after root instrumentation. A
362. biometric evaluation. J Clin Periodontol 1983: 10: 277–286.

227
Heitz-Mayfield & Lang

27. Ehmke B, Moter A, Beikler T, Milian E, Flemmig TF. ment of chronic periodontitis. J Clin Periodontol 2002:
Adjunctive antimicrobial therapy of periodontitis: long- 29(Suppl 3): 92–102, discussion 160-102.
term effects on disease progression and oral colonization. 41. Hellden LB, Listgarten MA, Lindhe J. The effect of tetra-
J Periodontol 2005: 76: 749–759. cycline and ⁄ or scaling on human periodontal disease.
28. Feres M, Haffajee AD, Goncalves C, Allard KA, Som S, J Clin Periodontol 1979: 6: 222–230.
Smith C, Goodson JM, Socransky SS. Systemic doxycycline 42. Heller D, Varela VM, Silva-Senem MX, Torres MC, Feres-
administration in the treatment of periodontal infections Filho EJ, Colombo AP. Impact of systemic antimicrobials
(I). Effect on the subgingival microbiota. J Clin Periodontol combined with anti-infective mechanical debridement on
1999: 26: 775–783. the microbiota of generalized aggressive periodontitis: a 6-
29. Flemmig TF, Milian E, Karch H, Klaiber B. Differential month RCT. J Clin Periodontol 2011: 38: 355–364.
clinical treatment outcome after systemic metronidazole 43. Herrera D, Sanz M, Jepsen S, Needleman I, Roldan S. A
and amoxicillin in patients harboring Actinobacillus ac- systematic review on the effect of systemic antimicrobials
tinomycetemcomitans and ⁄ or Porphyromonas gingivalis. as an adjunct to scaling and root planing in periodontitis
J Clin Periodontol 1998: 25: 380–387. patients. J Clin Periodontol 2002: 29(Suppl 3): 136–159,
30. Gellin RG, Miller MC, Javed T, Engler WO, Mishkin DJ. The discussion 160–132.
effectiveness of the Titan-S sonic scaler versus curettes in 44. Hirschfeld L, Wasserman B. A long-term survey of tooth
the removal of subgingival calculus. A human surgical loss in 600 treated periodontal patients. J Periodontol
evaluation. J Periodontol 1986: 57: 672–680. 1978: 49: 225–237.
31. Giannopoulou C, Andersen E, Brochut P, Plagnat D, 45. Hughes FJ, Smales FC. Immunohistochemical investiga-
Mombelli A. Enamel matrix derivative and systemic anti- tion of the presence and distribution of cementum-asso-
biotics as adjuncts to non-surgical periodontal treatment: ciated lipopolysaccharides in periodontal disease. J
biologic response. J Periodontol 2006: 77: 707–713. Periodontal Res 1986: 21: 660–667.
32. Goodson JM, Haffajee AD, Socransky SS, Kent R, Teles R, 46. Isidor F, Karring T, Attstrom R. The effect of root planing
Hasturk H, Bogren A, Van Dyke T, Wennstrom J, Lindhe J. as compared to that of surgical treatment. J Clin Period-
Control of periodontal infections: a randomized controlled ontol 1984: 11: 669–681.
trial I. The primary outcome attachment gain and pocket 47. Javed F, Al-Rasheed A, Almas K, Romanos GE, Al-Hezaimi K.
depth reduction at treated sites. J Clin Periodontol 2012: Effect of cigarette smoking on the clinical outcomes of peri-
39: 526–536. odontal surgical procedures. Am J Med Sci 2012: 343: 78–84.
33. Graziani F, Gennai S, Cei S, Cairo F, Baggiani A, Miccoli M, 48. Jepsen S, Deschner J, Braun A, Schwarz F, Eberhard J.
Gabriele M, Tonetti M. Clinical performance of access flap Calculus removal and the prevention of its formation.
surgery in the treatment of the intrabony defect. A sys- Periodontol 2000 2011: 55: 167–188.
tematic review and meta-analysis of randomized clinical 49. Johnson JD, Chen R, Lenton PA, Zhang G, Hinrichs JE,
trials. J Clin Periodontol 2012: 39: 145–156. Rudney JD. Persistence of extracrevicular bacterial reser-
34. Guerrero A, Echeverria JJ, Tonetti MS. Incomplete adher- voirs after treatment of aggressive periodontitis. J Period-
ence to an adjunctive systemic antibiotic regimen de- ontol 2008: 79: 2305–2312.
creases clinical outcomes in generalized aggressive 50. Kaldahl WB, Kalkwarf KL, Patil KD, Molvar MP, Dyer JK.
periodontitis patients: a pilot retrospective study. J Clin Long-term evaluation of periodontal therapy: I. Response
Periodontol 2007: 34: 897–902. to 4 therapeutic modalities. J Periodontol 1996: 67: 93–
35. Guerrero A, Griffiths GS, Nibali L, Suvan J, Moles DR, 102.
Laurell L, Tonetti MS. Adjunctive benefits of systemic 51. Kaner D, Christan C, Dietrich T, Bernimoulin JP, Kleber BM,
amoxicillin and metronidazole in non-surgical treatment Friedmann A. Timing affects the clinical outcome of
of generalized aggressive periodontitis: a randomized adjunctive systemic antibiotic therapy for generalized
placebo-controlled clinical trial. J Clin Periodontol 2005: aggressive periodontitis. J Periodontol 2007: 78: 1201–1208.
32: 1096–1107. 52. Knowles J, Burgett F, Morrison E, Nissle R, Ramfjord S.
36. Haas AN, Silva-Boghossian CM, Colombo AP, Susin C, Comparison of results following three modalities of peri-
Albandar JM, Oppermann RV, Rosing CK. Adjunctive azi- odontal therapy related to tooth type and initial pocket
thromycin in the treatment of aggressive periodontitis: depth. J Clin Periodontol 1980: 7: 32–47.
microbiological findings of a 12-month randomized clin- 53. Lang NP, Tan WC, Krahenmann MA, Zwahlen M. A sys-
ical trial. J Dent 2012: 40: 556–563. tematic review of the effects of full-mouth debridement
37. Haffajee AD, Dibart S, Kent RL Jr, Socransky SS. Clinical and with and without antiseptics in patients with chronic
microbiological changes associated with the use of 4 periodontitis. J Clin Periodontol 2008: 35: 8–21.
adjunctive systemically administered agents in the treatment 54. Lindhe J, Liljenberg B, Adielson B, Borjesson I. Use of
of periodontal infections. J Clin Periodontol 1995: 22: 618–627. metronidazole as a probe in the study of human peri-
38. Haffajee AD, Socransky SS, Gunsolley JC. Systemic anti- odontal disease. J Clin Periodontol 1983: 10: 100–112.
infective periodontal therapy. A systematic review. Ann 55. Lindhe J, Liljenberg B, Adielsson B. Effect of long-term
Periodontol 2003: 8: 115–181. tetracycline therapy on human periodontal disease. J Clin
39. Hanes PJ, Purvis JP. Local anti-infective therapy: phar- Periodontol 1983: 10: 590–601.
macological agents. A systematic review. Ann Periodontol 56. Lindhe J, Nyman S. Scaling and granulation tissue removal
2003: 8: 79–98. in periodontal therapy. J Clin Periodontol 1985: 12: 374–388.
40. Heitz-Mayfield LJ, Trombelli L, Heitz F, Needleman I, 57. Lindhe J, Nyman S, Westfelt E, Socransky SS, Haffajee A.
Moles D. A systematic review of the effect of surgical Critical probing depths in periodontal therapy. Compend
debridement vs non-surgical debridement for the treat- Contin Educ Dent 1982: 3: 421–430.

228
Periodontal therapy

58. Lindhe J, Socransky SS, Nyman S, Haffajee A, Westfelt E. altered subgingival environment induced by periodontal
‘‘Critical probing depths’’ in periodontal therapy. J Clin pocket reduction. J Clin Periodontol 1995: 22: 780–787.
Periodontol 1982: 9: 323–336. 74. Mombelli A, Schmid B, Rutar A, Lang NP. Persistence
59. Lindhe J, Westfelt E, Nyman S, Socransky SS, Heijl L, patterns of Porphyromonas gingivalis, Prevotella interme-
Bratthall G. Healing following surgical ⁄ non-surgical dia ⁄ nigrescens, and Actinobacillus actinomyetemcomitans
treatment of periodontal disease. A clinical study. J Clin after mechanical therapy of periodontal disease. J Peri-
Periodontol 1982: 9: 115–128. odontol 2000: 71: 14–21.
60. Listgarten MA, Ellegaard B. Electron microscopic evi- 75. Moore J, Wilson M, Kieser JB. The distribution of bacterial
dence of a cellular attachment between junctional epi- lipopolysaccharide (endotoxin) in relation to periodontally
thelium and dental calculus. J Periodontal Res 1973: 8: involved root surfaces. J Clin Periodontol 1986: 13: 748–751.
143–150. 76. Moreira RM, Feres-Filho EJ. Comparison between full-
61. Loesche WJ, Giordano JR, Hujoel P, Schwarcz J, Smith BA. mouth scaling and root planing and quadrant-wise basic
Metronidazole in periodontitis: reduced need for surgery. therapy of aggressive periodontitis: 6-month clinical re-
J Clin Periodontol 1992: 19: 103–112. sults. J Periodontol 2007: 78: 1683–1688.
62. Loesche WJ, Schmidt E, Smith BA, Morrison EC, Caffesse 77. Morrison EC, Ramfjord SP, Hill RW. Short-term effects of
R, Hujoel PP. Effects of metronidazole on periodontal initial, nonsurgical periodontal treatment (hygienic
treatment needs. J Periodontol 1991: 62: 247–257. phase). J Clin Periodontol 1980: 7: 199–211.
63. Machtei EE, Younis MN. The use of 2 antibiotic regimens 78. Muller HP, Heinecke A, Borneff M, Kiencke C, Knopf A,
in aggressive periodontitis: comparison of changes in Pohl S. Eradication of Actinobacillus actinomycetemcomi-
clinical parameters and gingival crevicular fluid biomar- tans from the oral cavity in adult periodontitis. J Peri-
kers. Quintessence Int 2008: 39: 811–819. odontal Res 1998: 33: 49–58.
64. Magnusson I, Low SB, McArthur WP, Marks RG, Walker 79. Nakib NM, Bissada NF, Simmelink JW, Goldstine SN.
CB, Maruniak J, Taylor M, Padgett P, Jung J, Clark WB. Endotoxin penetration into root cementum of periodon-
Treatment of subjects with refractory periodontal disease. tally healthy and diseased human teeth. J Periodontol
J Clin Periodontol 1994: 21: 628–637. 1982: 53: 368–378.
65. Marsh PD. Dental plaque: biological significance of a 80. Needleman I, Moles DR, Worthington H. Evidence-based
biofilm and community life-style. J Clin Periodontol 2005: periodontology, systematic reviews and research quality.
32(Suppl 6): 7–15. Periodontol 2000 2005: 37: 12–28.
66. Marsh PD, Moter A, Devine DA. Dental plaque biofilms: 81. Needleman IG. A guide to systematic reviews. J Clin Pe-
communities, conflict and control. Periodontol 2000 2011: riodontol 2002: 29(Suppl 3): 6–9, discussion 37–38.
55: 16–35. 82. Ng VW, Bissada NF. Clinical evaluation of systemic
67. Mascarenhas P, Gapski R, Al-Shammari K, Hill R, Soehren doxycycline and ibuprofen administration as an adjunc-
S, Fenno JC, Giannobile WV, Wang HL. Clinical response tive treatment for adult periodontitis. J Periodontol 1998:
of azithromycin as an adjunct to non-surgical periodontal 69: 772–776.
therapy in smokers. J Periodontol 2005: 76: 426–436. 83. Noyan U, Yilmaz S, Kuru B, Kadir T, Acar O, Buget E. A
68. Matarazzo F, Figueiredo LC, Cruz SE, Faveri M, Feres M. clinical and microbiological evaluation of systemic and
Clinical and microbiological benefits of systemic metro- local metronidazole delivery in adult periodontitis pa-
nidazole and amoxicillin in the treatment of smokers with tients. J Clin Periodontol 1997: 24: 158–165.
chronic periodontitis: a randomized placebo-controlled 84. Nyman S, Lindhe J, Rosling B. Periodontal surgery in pla-
study. J Clin Periodontol 2008: 35: 885–896. que-infected dentitions. J Clin Periodontol 1977: 4: 240–249.
69. Mestnik MJ, Feres M, Figueiredo LC, Duarte PM, Lira EA, 85. Palmer RM, Matthews JP, Wilson RF. Adjunctive systemic
Faveri M. Short-term benefits of the adjunctive use of and locally delivered metronidazole in the treatment of
metronidazole plus amoxicillin in the microbial profile periodontitis: a controlled clinical study. Br Dent J 1998:
and in the clinical parameters of subjects with generalized 184: 548–552.
aggressive periodontitis. J Clin Periodontol 2010: 37: 353– 86. Palmer RM, Matthews JP, Wilson RF. Non-surgical peri-
365. odontal treatment with and without adjunctive metroni-
70. Moeintaghavi A, Talebi-ardakani MR, Haerian-ardakani A, dazole in smokers and non-smokers. J Clin Periodontol
Zandi H, Taghipour S, Fallahzadeh H, Pakzad A, Fahami 1999: 26: 158–163.
N. Adjunctive effects of systemic amoxicillin and metro- 87. Palmer RM, Watts TL, Wilson RF. A double-blind trial of
nidazole with scaling and root planing: a randomized, tetracycline in the management of early onset periodon-
placebo controlled clinical trial. J Contemp Dent Pract titis. J Clin Periodontol 1996: 23: 670–674.
2007: 8: 51–59. 88. Pihlstrom BL, McHugh RB, Oliphant TH, Ortiz-Campos C.
71. Mombelli A, Brochut P, Plagnat D, Casagni F, Giannop- Comparison of surgical and nonsurgical treatment of
oulou C. Enamel matrix proteins and systemic antibiotics periodontal disease. A review of current studies and
as adjuncts to non-surgical periodontal treatment: clinical additional results after 61 ⁄ 2 years. J Clin Periodontol
effects. J Clin Periodontol 2005: 32: 225–230. 1983: 10: 524–541.
72. Mombelli A, Gmur R, Gobbi C, Lang NP. Actinobacillus 89. Purucker P, Mertes H, Goodson JM, Bernimoulin JP. Local
actinomycetemcomitans in adult periodontitis. I. Topo- versus systemic adjunctive antibiotic therapy in 28 pa-
graphic distribution before and after treatment. J Period- tients with generalized aggressive periodontitis. J Period-
ontol 1994: 65: 820–826. ontol 2001: 72: 1241–1245.
73. Mombelli A, Nyman S, Brägger U, Wennström J, Lang NP. 90. Quirynen M, Bollen CM, Vandekerckhove BN, Dekeyser C,
Clinical and microbiological changes associated with an Papaioannou W, Eyssen H. Full- vs. partial-mouth disin-

229
Heitz-Mayfield & Lang

fection in the treatment of periodontal infections: short- 105. Sampaio E, Rocha M, Figueiredo LC, Faveri M, Duarte
term clinical and microbiological observations. J Dent Res PM, Gomes Lira EA, Feres M. Clinical and microbio-
1995: 74: 1459–1467. logical effects of azithromycin in the treatment of
91. Quirynen M, Teughels W, van Steenberghe D. Microbial generalized chronic periodontitis: a randomized pla-
shifts after subgingival debridement and formation of cebo-controlled clinical trial. J Clin Periodontol 2011: 38:
bacterial resistance when combined with local or systemic 838–846.
antimicrobials. Oral Dis 2003: 9(Suppl 1): 30–37. 106. Sanz M, Teughels W. Innovations in non-surgical periodontal
92. Rabbani GM, Ash MM Jr, Caffesse RG. The effectiveness of therapy: Consensus Report of the Sixth European Workshop
subgingival scaling and root planing in calculus removal. on Periodontology. J Clin Periodontol 2008: 35: 3–7.
J Periodontol 1981: 52: 119–123. 107. Schwarz F, Aoki A, Becker J, Sculean A. Laser application
93. Ramberg P, Rosling B, Serino G, Hellstrom MK, Socransky in non-surgical periodontal therapy: a systematic review.
SS, Lindhe J. The long-term effect of systemic tetracycline J Clin Periodontol 2008: 35: 29–44.
used as an adjunct to non-surgical treatment of advanced 108. Serrano C, Torres N, Valdivieso C, Castano C, Barrera M,
periodontitis. J Clin Periodontol 2001: 28: 446–452. Cabrales A. Antibiotic resistance of periodontal pathogens
94. Ramfjord SP, Caffesse RG, Morrison EC, Hill RW, Kerry GJ, obtained from frequent antibiotic users. Acta Odontol
Appleberry EA, Nissle RR, Stults DL. Four modalities of Latinoam 2009: 22: 99–104.
periodontal treatment compared over five years. J Peri- 109. Sgolastra F, Gatto R, Petrucci A, Monaco A. Effectiveness of
odontal Res 1987: 22: 222–223. systemic amoxicillin ⁄ metronidazole as adjunctive therapy
95. Rams TE, Slots J. Local delivery of antimicrobial agents in to scaling and root planing in the treatment of chronic
the periodontal pocket. Periodontol 2000 1996: 10: 139–159. periodontitis: a systematic review and meta-analysis.
96. Retzepi M, Tonetti M, Donos N. Comparison of gingival J Periodontol 2012: 10: 1257–1269.
blood flow during healing of simplified papilla preservation 110. Sgolastra F, Petrucci A, Gatto R, Marzo G, Monaco A.
and modified Widman flap surgery: a clinical trial using Photodynamic therapy in the treatment of chronic peri-
laser Doppler flowmetry. J Clin Periodontol 2007: 34: 903– odontitis: a systematic review and meta-analysis. Lasers
911. Med Sci 2013: 28: 669–682.
97. Ribeiro Edel P, Bittencourt S, Sallum EA, Sallum AW, 111. Sgolastra F, Petrucci A, Gatto R, Monaco A. Effectiveness
Nociti FH Jr, Casati MZ. Non-surgical instrumentation of systemic amoxicillin ⁄ metronidazole as an adjunctive
associated with povidone-iodine in the treatment of therapy to full-mouth scaling and root planing in the
interproximal furcation involvements. J Appl Oral Sci treatment of aggressive periodontitis: a systematic review
2010: 18: 599–606. and meta-analysis. J Periodontol 2012: 83: 731–743.
98. Ribeiro Edel P, Bittencourt S, Zanin IC, Bovi Ambrosano 112. Sgolastra F, Petrucci A, Gatto R, Monaco A. Efficacy of
GM, Sallum EA, Nociti FH, Goncalves RB, Casati MZ. Full- Er:YAG laser in the treatment of chronic periodontitis:
mouth ultrasonic debridement associated with amoxicillin systematic review and meta-analysis. Lasers Med Sci 2012:
and metronidazole in the treatment of severe chronic 27: 661–673.
periodontitis. J Periodontol 2009: 80: 1254–1264. 113. Sigusch B, Beier M, Klinger G, Pfister W, Glockmann E. A
99. Rodrigues AS, Lourencao DS, Lima Neto LG, Pannuti CM, 2-step non-surgical procedure and systemic antibiotics in
Crespo Hirata RD, Hirata MH, Lotufo RF, De Micheli G. the treatment of rapidly progressive periodontitis. J Peri-
Clinical and microbiologic evaluation, by real-time poly- odontol 2001: 72: 275–283.
merase chain reaction, of non-surgical treatment of 114. Silva MP, Feres M, Sirotto TA, Soares GM, Mendes JA,
aggressive periodontitis associated with amoxicillin and Faveri M, Figueiredo LC. Clinical and microbiological
metronidazole. J Periodontol 2011: 83: 744–752. benefits of metronidazole alone or with amoxicillin as
100. Rooney J, Wade WG, Sprague SV, Newcombe RG, Addy M. adjuncts in the treatment of chronic periodontitis: a ran-
Adjunctive effects to non-surgical periodontal therapy of domized placebo-controlled clinical trial. J Clin Period-
systemic metronidazole and amoxycillin alone and com- ontol 2011: 38: 828–837.
bined. A placebo controlled study. J Clin Periodontol 2002: 115. Slots J. Human viruses in periodontitis. Periodontol 2000
29: 342–350. 2010: 53: 89–110.
101. Rosling B, Nyman S, Lindhe J, Jern B. The healing poten- 116. Slots J. Low-cost periodontal therapy. Periodontol 2000
tial of the periodontal tissues following different tech- 2012: 60: 110–137.
niques of periodontal surgery in plaque-free dentitions. A 117. Smith SR, Foyle DM, Daniels J, Joyston-Bechal S, Smales
2-year clinical study. J Clin Periodontol 1976: 3: 233–250. FC, Sefton A, Williams J. A double-blind placebo-con-
102. Rosling BG, Slots J, Christersson LA, Grondahl HG, Genco trolled trial of azithromycin as an adjunct to non-surgical
RJ. Topical antimicrobial therapy and diagnosis of sub- treatment of periodontitis in adults: clinical results. J Clin
gingival bacteria in the management of inflammatory Periodontol 2002: 29: 54–61.
periodontal disease. J Clin Periodontol 1986: 13: 975–981. 118. Socransky SS, Haffajee AD. The nature of periodontal
103. Rosling BG, Slots J, Webber RL, Christersson LA, Genco RJ. diseases. Ann Periodontol 1997: 2: 3–10.
Microbiological and clinical effects of topical subgingival 119. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL
antimicrobial treatment on human periodontal disease. J Jr. Microbial complexes in subgingival plaque. J Clin Pe-
Clin Periodontol 1983: 10: 487–514. riodontol 1998: 25: 134–144.
104. Sahrmann P, Puhan MA, Attin T, Schmidlin PR. Systematic 120. Soder B, Nedlich U, Jin LJ. Longitudinal effect of non-
review on the effect of rinsing with povidone-iodine dur- surgical treatment and systemic metronidazole for 1 week
ing nonsurgical periodontal therapy. J Periodontal Res in smokers and non-smokers with refractory periodontitis:
2010: 45: 153–164. a 5-year study. J Periodontol 1999: 70: 761–771.

230
Periodontal therapy

121. Tinoco EM, Beldi MI, Campedelli F, Lana M, Loureiro 130. Walmsley AD, Lea SC, Landini G, Moses AJ. Advances in
CA, Bellini HT, Rams TE, Tinoco NM, Gjermo P, Preus power driven pocket ⁄ root instrumentation. J Clin Peri-
HR. Clinical and microbiological effects of adjunctive odontol 2008: 35: 22–28.
antibiotics in treatment of localized juvenile periodonti- 131. Walsh MM, Buchanan SA, Hoover CI, Newbrun E, Taggart
tis. A controlled clinical trial. J Periodontol 1998: 69: EJ, Armitage GC, Robertson PB. Clinical and microbiologic
1355–1363. effects of single-dose metronidazole or scaling and root
122. Trombelli L, Simonelli A, Schincaglia GP, Cucchi A, Farina planing in treatment of adult periodontitis. J Clin Period-
R. Single-flap approach for surgical debridement of deep ontol 1986: 13: 151–157.
intraosseous defects: a randomized controlled trial. J Pe- 132. Winkel EG, van Winkelhoff AJ, Barendregt DS, van der Weij-
riodontol 2012: 83: 27–35. den GA, Timmerman MF, van der Velden U. Clinical and
123. Tunkel J, Heinecke A, Flemmig TF. A systematic review of microbiological effects of initial periodontal therapy in con-
efficacy of machine-driven and manual subgingival junction with amoxicillin and clavulanic acid in patients with
debridement in the treatment of chronic periodontitis. adult periodontitis. A randomised double-blind, placebo-
J Clin Periodontol 2002: 29(Suppl 3): 72–81, discussion controlled study. J Clin Periodontol 1999: 26: 461–468.
90–71. 133. Winkel EG, van Winkelhoff AJ, Timmerman MF, van der
124. Valenza G, Veihelmann S, Peplies J, Tichy D, Roldan- Velden U, van der Weijden GA. Amoxicillin plus metro-
Pareja Mdel C, Schlagenhauf U, Vogel U. Microbial nidazole in the treatment of adult periodontitis patients. A
changes in periodontitis successfully treated by mechan- double-blind placebo-controlled study. J Clin Periodontol
ical plaque removal and systemic amoxicillin and metro- 2001: 28: 296–305.
nidazole. Int J Med Microbiol 2009: 299: 427–438. 134. Winkel EG, van Winkelhoff AJ, van der Velden U. Addi-
125. van Winkelhoff AJ, Herrera D, Oteo A, Sanz M. Antimi- tional clinical and microbiological effects of amoxicillin
crobial profiles of periodontal pathogens isolated from and metronidazole after initial periodontal therapy. J Clin
periodontitis patients in The Netherlands and Spain. J Clin Periodontol 1998: 25: 857–864.
Periodontol 2005: 32: 893–898. 135. Xajigeorgiou C, Sakellari D, Slini T, Baka A, Konstantinidis
126. van Winkelhoff AJ, Tijhof CJ, de Graaff J. Microbiological A. Clinical and microbiological effects of different anti-
and clinical results of metronidazole plus amoxicillin microbials on generalized aggressive periodontitis. J Clin
therapy in Actinobacillus actinomycetemcomitans-associ- Periodontol 2006: 33: 254–264.
ated periodontitis. J Periodontol 1992: 63: 52–57. 136. Yek EC, Cintan S, Topcuoglu N, Kulekci G, Issever H,
127. Varela VM, Heller D, Silva-Senem MX, Torres MC, Co- Kantarci A. Efficacy of amoxicillin and metronidazole
lombo AP, Feres-Filho EJ. Systemic antimicrobials combination for the management of generalized aggres-
adjunctive to a repeated mechanical and antiseptic ther- sive periodontitis. J Periodontol 2010: 81: 964–974.
apy for aggressive periodontitis: a 6-month randomized 137. Yilmaz S, Kuru B, Noyan U, Kadir T, Acar O, Buget E. A
controlled trial. J Periodontol 2011: 82: 1121–1130. clinical and microbiological evaluation of systemic
128. Wade WG. Has the use of molecular methods for the and local metronidazole delivery in early onset peri-
characterization of the human oral microbiome changed odontitis patients. J Marmara Univ Dent Fac 1996: 2:
our understanding of the role of bacteria in the patho- 500–509.
genesis of periodontal disease? J Clin Periodontol 2011: 138. Zandbergen D, Slot DE, Cobb CM, Van der Weijden FA.
38(Suppl 11): 7–16. The clinical effect of scaling and root planing and the
129. Waerhaug J. Healing of the dento-epithelial junction fol- concomitant administration of systemic amoxicillin and
lowing subgingival plaque control. II: as observed on ex- metronidazole: a systematic review. J Periodontol 2013: 84:
tracted teeth. J Periodontol 1978: 49: 119–134. 332–351.

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