international dental journal 7 1 ( 2 0 2 1 ) 4 6 2 − 4 7 6

Concise Clinical Review

Current Concepts in the Management of Periodontitis

TaeHyun Kwon a*, Ira B. Lamster b, Liran Levin c

a
Private Practice, Keene, NH, USA
b
Stony Brook University School of Dental Medicine, Stony Brook, NY, USA
c
Faculty of Medicine and Dentistry, University of Alberta, Edmonton, AB, Canada

A R T I C L E I N F O A B S T R A C T

Article history: Periodontitis is a common disorder affecting >40% of adults in the United States. Globally, the
Available online 19 February 2021 severe form of the disease has a prevalence of 11%. In advanced cases, periodontitis leads to
tooth loss and reduced quality of life. The aetiology of periodontitis is multifactorial. Subgingival
Key words: dental biofilm elicits a host inflammatory and immune response, ultimately leading to irrevers-
Biofilm ible destruction of the periodontium (i.e. alveolar bone and periodontal ligament) in a susceptible
dental plaque host. In order to successfully manage periodontitis, dental professionals must understand the
oral hygiene pathogenesis, primary aetiology, risk factors, contributing factors and treatment protocols. Care-
periodontal disease ful diagnosis, elimination of the causes and reduction of modifiable risk factors are paramount
non-surgical periodontal therapy for successful prevention and treatment of periodontitis. Initial non-surgical periodontal therapy
primarily consists of home care review and scaling and root planing. For residual sites with
active periodontitis at periodontal re-evaluation, a contemporary regenerative or traditional
resective surgical therapy can be utilised. Thereafter, periodontal maintenance therapy at a reg-
ular interval and long-term follow-ups are also crucial to the success of the treatment and long-
term retention of teeth. The aim of this review is to provide current concepts of diagnosis, pre-
vention and treatment of periodontitis. Both clinical and biological rationales will be discussed.
Ó 2021 Published by Elsevier Inc. on behalf of FDI World Dental Federation. This is an open
access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)

Periodontitis States had periodontitis, with 7.8% having severe periodonti-

tis.6 This survey confirmed a high prevalence of periodontitis
Periodontitis is a chronic multifactorial inflammatory disease in the United States affecting almost 50% of the adult popula-
associated with the accumulation of dental plaque (which will tion (30 years old or older).6 Globally, approximately 11% of
be referred to as dental biofilm/biofilm), and characterised by the world population may have severe periodontitis, affecting
progressive destruction of the teeth-supporting apparatus, 743 million individuals (Figure 2).7−13 Furthermore, a robust
including the periodontal ligament and alveolar bone.1,2 The literature has identified potential associations between peri-
disease involves complex dynamic interactions among specific odontitis and certain non-communicable chronic diseases.14
bacterial pathogens, destructive host immune responses, and In addition, the loss of periodontal support was associated
environmental factors such as smoking (Figure 1).1,3 The com- with a significant reduction in masticatory performance.15
mon features of periodontitis include gingival inflammation, Thus, periodontitis and its clinical ramifications, including
clinical attachment loss, radiographic evidence of alveolar tooth loss, may have a substantially negative effect on oral
bone loss, sites with deep probing depths, mobility, bleeding health related quality of life (OHRQoL), while successful man-
upon probing and pathologic migration.2,4,5 agement may improve patients’ OHRQoL.15,16

Prevalence and significance Aetiology

According to data from the National Health and Nutrition Dental biofilm
Examination Survey 2009−2014, 42% of adults in the United
For a susceptible host, microbial infection in subgingival dental
* Correspondence author. Dr TaeHyun Kwon, Monadnock Perio & biofilm by periodontal pathogens, in particular a group of spe-
Implant Center, 819 Court street, Unit A, Keene, NH 03431, USA. cific gram-negative anaerobic species referred to as the red
E-mail address: [email protected] (T. Kwon). complex, results in chronic inflammation.17,18 These red-
https://doi.org/10.1111/idj.12630
0020-6539/Ó 2021 Published by Elsevier Inc. on behalf of FDI World Dental Federation. This is an open access article under the CC BY-NC-
ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
 management of periodontitis 463

production of matrix metalloproteinases (MMPs) by macro-

phages, fibroblasts, junctional epithelial cells, and neutro-
phils.3,25 The resulting MMPs then mediate the destruction of
collagen fibres in periodontal tissues, especially periodontal
ligaments.3 In addition, the pro-inflammatory cytokines
induce the expression of receptor activator of nuclear factor kB
ligand (RANK-L) on the osteoblasts and T helper cells. The
resulting RANK-L on the osteoblasts and the T helper cells
then interacts with receptor activator of nuclear factor kB
(RANK) on osteoclast precursors, which results in the genesis
of osteoclasts and their maturation. The mature osteoclasts
mediate alveolar bone destruction.26,27

Natural history/progression

Periodontitis was previously believed to progress at a con-

stant rate until treatment or tooth loss.28 For instance, indi-
viduals with so-called rapidly progressing periodontitis
Fig. 1 – Periodontitis is multifactorial in nature and results exhibited an annual rate of interproximal attachment loss of
from the presence of pathogenic bacteria, the host inflam- between 0.1 and 1.0 mm, while individuals with moderately
matory and immune responses and other identified envi- progressing periodontitis exhibited a loss of between 0.05 and
ronmental and systemic risk factors. 0.5 mm.29 Individuals with minimal to no progression exhib-
ited an annual loss rate of between 0.05 and 0.09 mm.29 Cur-
rently, based on longitudinal observations from human and
animal studies, periodontitis is now believed to progress by
complex bacteria include Porphyromonas gingivalis, Tannerella recurrent acute episodes instead.28,30 During their lifetime,
forsythia, and Treponema denticola, which are predominantly patients with periodontitis exhibit a cycle of bursts of
found in deep periodontal pockets of patients with periodonti- destruction at individual sites over short periods of time, fol-
tis (Table 1).17−24 Lipopolysaccharide along with other viru- lowed by longer periods of remission.28,31
lence factors from these periodontal pathogens stimulate the
host macrophages, and other inflammatory and constituent
cells, leading to the production of a range of pro-inflammatory Diagnosis
cytokines such as tumour necrosis factor (TNF)-a, interleukin
(IL)-1b and prostaglandin E2 (PGE2). The presence of these pro- A patient’s medical history should be obtained prior to peri-
inflammatory cytokines and virulence factors stimulates the odontal assessment. This will provide identification of any

Fig. 2 – Global prevalence of severe periodontitis7−9 in comparison to diabetes10, hypertension11, depression12 and asthma.13
464 kwon et al.

Table 1 – Red-complex bacteria and their characteristics

Pathogens Characteristics19 Virulence factors Major functions
Porphyromonas Gram negative Capsule Antiphagocytic20
gingivalis Non-motile Fimbriae Cellular adhesion20
Anaerobic Outer membrane proteins Contain LPS, eliciting the host pro-inflammatory response and the
Pleomorphic production of pro-inflammatory cytokines21
rod Gingipains Possibly linked to Alzheimer’s disease22
(coccal to short)  Degrade host proteins, providing essential amino acids, peptides and
Tannerella Gram negative Various proteinases heme for the growth of Tannerella forsythia23
forsythia Non-motile  Degrade periodontal tissues23
Anaerobic  Activate host degradative enzymes23
Pleomorphic rod  Modify host cell proteins to expose cryptotopes for bacterial
(spindle shaped) colonisation23
 Cleave components in host innate (cytokines, complement
factors) and adaptive immune system (immunoglobulins), thus
paralysing host immunity23
 Active components involved in clotting and fibrinolysis23
Surface lipoproteins Induces host cellular apoptosis23
Treponema Gram negative Motility and chemotaxis Enable the bacterium to rapidly colonise new sites, penetrate deep
denticola Motile periodontal pockets, and penetrate epithelial layers24
Anaerobic  Impair neutrophil chemotaxis and phagocytosis
Cork-screw shaped Outer sheath proteins  Interact synergistically with other periodontal pathogens including
or spiralled (dentilisin, major sheath Porphyromonas gingivalis and Tannerella forsythia at several levels24
proteins, lipoproteins)  Bind to and coat their surface with soluble host proteins, thus
Metabolic end products avoiding and delaying host recognition24
Cytotoxic to various host cells24
 Contribute to biofilm formation and persistence24
Toxin-antitoxin system,  Resist to various environmental assaults such as antibiotics24
and transposases  Allows transfer of virulence genes through horizontal gene
transferwithin biofilm24

systemic or environmental risk factors for periodontitis, such on host immune cells, especially neutrophils, was reported,
as diabetes and smoking. A comprehensive periodontal evalu- making their host more susceptible to periodontitis.35−37 Con-
ation includes several clinical parameters: biofilm index, peri- sistent with these findings, light and heavy smokers are at a
odontal probing depth, presence of bleeding on probing, greater risk for developing alveolar bone loss with an odds
gingival recession, mucogingival deformity, furcation involve- ratio of 3.25 and 7.28, respectively, compared to non-smokers.
ment, tooth mobility, and occlusal trauma. A comprehensive Similarly, light and heavy smokers are at a greater risk for
radiographic evaluation is a part of the initial periodontal eval- developing periodontal attachment loss with an odds ratio
uation to determine the extent of horizontal and vertical alveo- 2.05 and 4.07, respectively, compared to non-smokers.38 Fur-
lar bone loss. According to the 2017 World Workshop on the thermore, smoking has a negative impact on the outcome of
Classification of Periodontal and Peri-Implant Diseases and active periodontal therapy as well as long-term maintenance
Conditions2, a new periodontitis classification categorises the periodontal therapy.39,40 Thus, patients should be continu-
disease based on a multi-dimensional staging and grading sys- ously reminded of the importance of smoking cessation for
tem. Staging is determined by the severity of the disease at ini- successful management of periodontitis.41
tial presentation and the complexity of disease management
(Table 2).2 Furthermore, grading is used as an indicator of the Diabetes
rate of periodontitis progression, which is determined by the
history as well as the presence of risk factors for periodontitis Patients with uncontrolled diabetes are at a greater risk for
(Table 3).2 developing periodontitis as compared to systemically healthy
patients or patients with well-controlled diabetes.42,43 Plausi-
ble biological mechanisms underlying this association have
Risk factors been scientifically validated.43 The association is partly due
to alterations in the immune system of patients with uncon-
Smoking trolled diabetes, which result in impaired neutrophil function
or hyper-responsive macrophages producing pro-inflamma-
Smoking is the most important environmental risk factor for tory cytokines.43 Furthermore, patients with uncontrolled
periodontitis. Compared to non-smokers or past smokers, diabetes exhibit alterations in connective tissue metabolism,
smokers exhibited a significantly higher prevalence of which modulates the resorptive and formative process in the
red-complex periodontal pathogens in their subgingival bio- periodontium.43 The alterations in connective tissue metabo-
film.32−34 Furthermore, a potential negative effect of smoking lism are due to higher levels of advanced glycation end
 management of periodontitis 465

The stage of periodontitis is initially determined based on clinical attachment loss (CAL). If CAL is not available, then radiographic bone loss can be used. A history of tooth loss due to periodontitis may modify
the stage. In the presence of any complexity factor, the stage may shift to a higher tier. For example, the presence of class II or III furcation involvement would shift to either stage III or IV regardless of CAL,
Tooth loss due to periodontitis of ≥5
products (AGEs) and interaction with their receptors, recep-

Extending to middle or apical third of

 Secondary occlusal trauma (tooth

 Less than 20 remaining teeth (10

Need for complete rehabilitation
In addition to stage III complexity:
tors for AGE (RAGEs), in patients with uncontrolled diabetes

radiographic bone loss, or tooth loss due to periodontitis. The extent and distribution is primarily determined by the percentage of teeth involved2. The table was modified from Papapanou et al. (2018).2
 Bite collapse, drifting, flaring
compared to systemically healthy patients or patients with

 Masticatory dysfunction
well-controlled diabetes.43−47 The interaction between AGEs
and RAGEs results in the marked elevation of gingival crevic-

mobility degree ≥2)

 Severe ridge defect
ular fluid levels of IL-1b, TNF-a and PGE2 in patients with

opposing pairs)
uncontrolled diabetes.43,45,47 These pro-inflammatory cyto-
kines then contribute to the inflammatory response that
characterises periodontitis.43,45,47 Lastly, macrovascular (i.e.
the root

due to:
Stage IV

≥5 mm

teeth

atherosclerosis) and microvascular changes (i.e. thickening of

the basement membrane) in patients with uncontrolled dia-
betes may result in the abnormal growth of vessels, impaired
regeneration of vessels, and abnormal homeostatic transport
Tooth loss due to periodontitis of
Extending to middle or apical third

 Furcation involvement Class II

In addition to stage II complexity:

across the basement membrane in the periodontium.43

For each stage, describe extent as localised (<30% of teeth involved), generalised, or molar/incisor pattern

Clinically, patients with type 2 diabetes exhibited an

 Vertical bone loss ≥3 mm

increased risk of periodontitis with an odds ratio of 2.81 for

 Probing depth ≥6 mm

 Moderate ridge defect

clinical attachment loss and an odds ratio of 3.43 for alveolar

bone loss.33 Patients with diabetes exhibit a greater percent-
age of teeth having at least one site with a probing depth of
of the root

5 mm or more, a greater percentage of sites with bleeding on

<4 teeth

probing, and a greater number of missing teeth compared to

or III
Stage III

≥5 mm

non-diabetic patients.48 Moreover, patients with uncontrolled

diabetes may not respond as favourably to periodontal ther-
apy as do patients with periodontitis but milder diabetes.43
Maximum probing depth ≤5 mm.

Thus, patients’ glycaemic status should be continuously

Mostly horizontal bone loss

monitored, and haemoglobin A1c (HbA1c) levels should be

Coronal third (15% to 33%)

documented. Ideally, the HbA1c level should be <7.0%.2 For

patients with poorly managed diabetes, inter-professional
practice is essential.
3 to 4 mm

Contributing factors
Stage II

Overhanging/over-contoured restorations
No tooth loss due to periodontitis

Overhanging or over-contoured restorations may promote

Maximum probing depth ≤4 mm.

dental biofilm retention, initiating a local periodontal

Mostly horizontal bone loss

lesion.49,50 Thus, a restoration with overhang or excessive

contour should be eliminated during the course of periodon-
tal therapy to create an environment that allows biofilm
Coronal third (<15%)

removal (Figure 3).

Open interproximal contacts

1 to 2 mm
Stage I

Open interproximal contacts may promote biofilm retention

due to chronic food impaction.51 Thus, during the course of
treatment, open interproximal contacts should be corrected.
Radiographic bone loss
Interdental CAL at site
Table 2 – The stages of periodontitis

Occlusal trauma
of greatest loss

Add to stage as
Tooth loss

descriptor

Though occlusal trauma is not considered a risk factor for

alveolar bone loss or development of periodontal disease,
Local

when occlusal trauma is present, periodontitis may exhibit a

greater rate of progression.52,53 Thus, resolution of occlusal
trauma should be considered during periodontal therapy
Periodontal stage

(Figure 4). For example, fremitus on centric occlusion or

distribution

excursive movement should be eliminated in periodontally

Complexity

Extent and

compromised teeth. Teeth presenting with excessive or

Severity

increasing mobility as a result of occlusal trauma may be

splinted.54
466 kwon et al.

Table 3 – The grades of periodontitis

Periodontitis grade Grade A: Slow rate of Grade B: Moderate rate Grade C: Rapid rate of
progression of progression progression
Primary Direct evidence Longitudinal (radiographic bone loss or Evidence of no loss over <2 mm over 5 years
criteria of progression date CAL) 5 years
≥2 mm over
5 years
Indirect evidence % bone loss/ <0.25 0.25 to 1.0 ≥ 1.0
Case of progression age Heavy biofilm deposits with Destruction commensurate Destruction exceeds expectation
phenotype low levels of destruction with biofilm deposits given biofilm deposits; specific
clinical patterns suggestive of
periods of rapid progression and/
or early onset disease (e.g. molar/
incisor pattern; lack of expected
response to standard bacterial
control therapies)
Grade modifiers Risk factors Smoking Non-smoker Smoker <10 cigarettes/day
Smoker ≥10
cigarettes/day
Diabetes Normoglycaemic/ no HbA1c <7.0% in patients HbA1c ≥7.0% in patients with
diagnosis of diabetes with diabetes diabetes

Grade is primarily determined by the direct evidence of progression. If not available, then the indirect evidence of progression can be used. In the
presence of risk factors for periodontitis, the grade can shift to a higher tier.2 The table was modified from Papapanou et al. (2018).2
CAL, clinical attachment loss; HbA1c, haemoglobin A1c.

Mucogingival deformity Scaling and root planing

After adequate home care or biofilm control is achieved, scal-
The presence of 2 mm or more of attached gingiva is consid- ing and root planing should be performed at the sites with
ered necessary to maintain gingival health.55 A significantly periodontal probing depths of 5 mm or greater. This phase of
higher gingival index was noted for teeth with <2 mm of treatment should be delivered in conjunction with correction
attached gingiva compared to those with at least 2 mm of of local contributing factors, extraction of hopeless teeth and
attached gingiva.55 Thus, all mucogingival deformities should treatment of active carious lesions. During scaling and root
be recorded during a comprehensive periodontal evaluation planing, adequate local anaesthesia should be administered
and, if indicated, treated during the phase of surgical peri- prior to initiating the procedure to ensure patient comfort.
odontal therapy. Automated instruments, such as piezoelectric or ultrasonic
scalers, may be used in combination with manual instru-
Anatomical factors ments.67 For areas where access is difficult, automated
instruments may be superior to curettes for removal of sub-
The presence of certain anatomical factors such as a cemen- gingival biofilm and calculus.68 Occlusal adjustment should
tal tear56, narrow furcation entrance,57 enamel pearl,58,59 root be considered to relieve fremitus, severe mobility, or exces-
concavity,57 cervical enamel projection,60 and positioning of sive central and lateral excursive contact.54 Clinically, a peri-
the tooth61,62 may increase the risk of local periodontal odontal explorer such as Old Dominion University explorer
attachment loss (Figure 5). Thus, these factors should be con- 11/12 should be used to check for removal of subgingival cal-
sidered during diagnosis and treatment. culus. Furthermore, post-operative intraoral radiographs
may be helpful to assess removal of subgingival calculus visi-
ble on pre-operative intraoral radiographs. For patients with
Treatment severe periodontitis, adjunctive use of systemic antibiotics
may be considered.69,70 Recent randomised clinical trials71,72
Initial cause-related therapy as well as systematic reviews and meta-analysis73−75
reported a significant improvement in the outcome of scaling
Home care review and root planing when antibiotics were used systemically as
Achieving adequate home care is an essential component of an adjunctive therapy. For example, in a recent systematic
prevention of periodontal disease, successful periodontal review of a total of 28 double-blinded randomised controlled
therapy and long-term retention of the dentition.63−65 Clini- trials investigating the benefit of systemic antibiotics as an
cians should educate patients about the importance of effec- adjunctive therapy to scaling and root planing in the treat-
tively removing dental biofilm at home, especially prior to ment of moderate to severe periodontitis,76 meta-analysis
proceeding with active periodontal therapy (Figure 6).66 The reported a statistically significant additional full-mouth prob-
importance of adequate home care should be reinforced fre- ing depth mean reduction of 0.448 mm and a clinical attach-
quently during the initial and subsequent phases of periodon- ment gain of 0.389 mm at 6-month follow-up in the antibiotic
tal treatment. versus the placebo control groups, which appeared to persist
 management of periodontitis 467

Fig. 3 – Management of a restoration with excessive contour.

(a) Pre-operative radiograph; over-contoured restoration
was present on the distal aspect of the mandibular right
second molar, causing biofilm and food accumulation in the
area. As a result, the distal aspect of the mandibular right
second molar exhibited 6−7 mm probing depths. (b) Post-
operative radiograph; the restoration was modified in order
Fig. 4 – A mandibular right central incisor with severe alveo-
to improve the distal contour of the mandibular right sec-
lar bone loss and secondary occlusal trauma. (a) Pre-opera-
ond molar.
tive radiograph; the mandibular right central incisor
exhibited a severe vertical bone loss. Clinically, the tooth
exhibited excessive mobility as a result of occlusal trauma.
(b) One year post-operative radiograph; after initial peri-
at 12-month follow-up (i.e. pocket probing reduction of odontal therapy with occlusal adjustment and splinting,
0.485 mm and clinical attachment level gain of 0.285 mm).76 radiographic evidence of increased height of alveolar bone
These improvements were further supported by reductions was noted for the mandibular incisors. No surgical treat-
in bleeding on probing and in frequency of residual periodon- ment was performed.
tal pockets, and increases in periodontal pocket closure.76
The most significant benefit was observed with amoxicillin
and metronidazole.76 Considering the limited evidence to
support the superiority of any specific dosage regimen, clini- modulation therapy was also reported in several studies.83,84
cians should consider using the highest dosage for the short- When administered at sub-antimicrobial dosages, doxycy-
est duration of time to reduce the risk of antibiotic cline inhibits MMPs in the gingival tissues without a microbial
resistance.73 For a localised site with a deep periodontal prob- effect.83,84 The significant adjunctive effect of sub-antimicro-
ing depth, administration of a locally delivered antibiotic (i.e. bial dosage doxycycline in addition to scaling and root plan-
minocycline microspheres77−80) or an antimicrobial (i.e. ing was found in treating patients with periodontitis.83
chlorhexidine chip81,82) may be considered. Benefit of host Furthermore, the adjunctive use of omega-3 fatty acids and
468 kwon et al.

Fig. 5 – A mandibular right second molar with a distal cemen-

tal tear. Right mandibular second molar exhibited cemental
tear on its distal surface. This was associated with an infrab-
ony defect as well as a deep periodontal pocket (9 mm).

Fig. 6 – Effect of home care on reducing periodontal inflam-

81 mg acetylsalicylic acid with scaling and root planing in mation. Improved home care/biofilm removal should be
patients with periodontitis resulted in a significant reduc- demonstrated prior to beginning active periodontal therapy.
tion of probing depths and a significant clinical attach- Patient presented with generalised gingival marginal ery-
ment gain compared to scaling and root planing alone.85,86 thema as well as oedema in the maxillary arch. Moderate
This significant adjunctive benefit is possibly due to the deposits of dental biofilm were noted at the gingival margin.
combined effect of producing host endogenous protective As a result of home care, after 9 weeks, significant resolu-
mediators such as resolvins, in addition to the anti- tion of gingival erythema and oedema were noted. Mini-
inflammatory effect, on resolving inflammation.85,86 Avail- mally visible dental biofilm was present, indicating effective
able adjunctive therapeutic modalities are summarised in home care. Scaling and root planing was then initiated, spe-
Table 4.69−75,77−102 It must be emphasised that limited lit- cifically aimed at the removal of supragingival and subgin-
erature and evidence are available for most adjunctive gival calculus. After completing initial cause-related
therapeutic modalities except systemic antibiotics and therapy and achieving a stable periodontium, the maxillary
that clinicians should carefully plan using these modali- left lateral incisor was extracted due to its linguoversion
ties based on the most current evidence.103 and endodontic pathology. (a) Initial. (b) After 9 weeks of
home care. (c) Periodontal re-evaluation: 6 weeks after com-
Table 4 – Available adjunctive therapies to scaling and root pleting initial cause-related therapy (i.e. home care, scaling
planing and root planing; no periodontal surgery was performed).

Adjunctive therapies Specifics

Systemic antibiotics Amoxicillin and
Periodontal re-evaluation
metronidazole69−71,73−75
Azithromycin71,87−91
Doxycycline92−94 Four to six weeks after completing scaling and root planing, a
Locally delivered antibiotics/ Minocycline microspheres77−80 re-evaluation should be conducted (Figure 6). A comprehen-
antimicrobials* Chlorhexidine chip81,82 sive periodontal charting should be updated and the findings
Host modulation therapy* Subclinical dose compared to the initial charting to determine the degree of
doxycycline83,84 improvement. Furthermore, patient compliance, as deter-
Omega-3 and 81 mg ASA79,80
mined by adherence to the suggested home care regimen,
Other adjunctive therapies* Antimicrobial photodynamic
therapy95
should be carefully evaluated. Generally, for areas with rela-
Laser therapy96,97 tively shallow probing depths (i.e. 1−5 mm), non-surgical
Probiotics98,99 management, including repeated root planing if indicated,
Propolis100,101 frequent periodontal maintenance therapy and continuous
Chlorhexidine102 reinforcement of home care could be considered as a treat-
ment approach. The efficiency of subgingival calculus
ASA, acetylsalicylic acid.
* Limited literature is available and clinicians should carefully plan using removal decreases as the probing depth increases.104,105
these modalities based on the most current evidence. Thus, for areas with persistently deep periodontal probing
 management of periodontitis 469

depths (i.e. 6 mm or deeper), surgical periodontal therapy

may be indicated. It must be emphasised that excellent com-
pliance with suggested home care is an indispensable pre-
requisite for proceeding with surgical therapy in order to
achieve the optimal surgical outcome.64 Thus, if necessary,
surgical therapy should be delayed until adequate biofilm
removal is demonstrated by the patient.64

Periodontal surgical therapy

Resective periodontal surgery

Areas with persistently deep probing depths generally exhibit
underlying infrabony or vertical defects. Such teeth with
infrabony or vertical defects exhibit significantly reduced sur-
vival compared to teeth without those defects.106,107 Thus, for
these teeth, osseous resective surgery may be considered. Dur-
ing this surgery, infrabony or vertical osseous defects should
be reduced or eliminated by osteotomy and osteoplasty.108
Thereafter, the gingival tissue may be positioned apically at the
new height of alveolar crest. This would result in resolution or
reduction of the deep probing depths (Figure 7).108 For areas
with persistently deep probing depths without an apparent
underlying alveolar defect, soft tissue resection may be consid-
ered.109−114 Post-surgically, resective periodontal surgery may
result in attachment loss in immediately neighbouring but less
involved sites,115 dentinal hypersensitivity from the exposed
root surfaces,116,117 transient increase in tooth mobility,118 and
loss of interproximal papilla.119 The loss of interproximal
papilla may result in chronic food impaction, aesthetic con-
cerns and phonetic change.119

Regenerative periodontal surgery

Regenerative periodontal surgery is intended to re-estab-
lish periodontal tissues lost as a result of the disease pro-
cess. Specifically, the goal of this type of surgery is to
increase attachment of the teeth to the periodontium and
induce bone gain and increased support for the denti-
tion.120,121 For infrabonyr or vertical defects, periodontal
regenerative therapy should also be considered. Guided
tissue regeneration utilises a barrier membrane with vari-
ous particulate bone graft material.122−125 A number of dif-
ferent approaches have been introduced. Recently, in
order to further enhance the outcome of periodontal
regeneration, biologic modifiers have been utilised in com-
bination with bone replacement grafts and barrier mem-
branes.126 Purified recombinant human platelet derived
growth factor BB (rhPDGF-BB) is a potent wound healing
Fig. 7 – Resective periodontal surgery in the area of a man- growth factor and stimulator of the proliferation and
dibular right first molar. (a) Mandibular right first molar with recruitment of cells of the periodontal ligament as well as
a persistent probing depth of 7 mm on mid-buccal aspect, bone cells.127 A meta-analysis and human histologic stud-
with grade II furcation. An infrabony defect was associated ies reported a greater clinical attachment gain and a
with the presence of cervical enamel projection. (b) greater bone fill with rhPDGF-BB in the treatment of
Advanced furcation involvement was confirmed. Osseous infrabony defects and advanced furcation lesions as com-
recontouring in combination with removal of the cervical pared to the carrier or bone replacement graft alone.127−129
enamel projection was planned. The buccal convexity of the
roots was reduced in order to decrease the horizontal furca-
tion depth. (c) Completion of recontouring prior to closure of complete removal of cervical enamel projection and reduc-
the surgical wound. Resolution of infrabony defect, tion in horizontal furcation depth were achieved.
470 kwon et al.

ligament cells.130,131 A meta-analysis reported that infrabony

defect sites that were treated with EMD revealed a signifi-
cantly greater clinical attachment gain compared to sites that
were treated with open-flap debridement, ethylenediamine-
tetraacetic acid, or a placebo.132
Therapy using an Nd:YAG laser was reported to achieve
periodontal regeneration (Figure 8).133,134 During this therapy,
the laser is used to selectively remove the diseased inner
sulcular epithelium, potentially exposing more of the dis-
eased root surface. Following thorough root planing of the
involved root surface, the laser is used again to create a stable
blood clot.133,134 However, considering the limited published
data, the use of Nd:YAG laser therapy for periodontal regener-
ation requires further evaluation.135
When planning regenerative periodontal therapy, the
morphology of the periodontal alveolar defect such as the
number of remaining alveolar walls (i.e. 1,2,3-walled defect)
and the angulation of the defect, should be carefully consid-
ered (Figure 9).106,123 Significantly better regenerative out-
comes were found with more remaining alveolar walls and a
defect angulation of <45 degrees.106,123

Mucogingival surgery
After completing initial periodontal therapy, and when there
is a specific indication, mucogingival deformity should be
carefully evaluated and treated if necessary. During this eval-
uation, among the clinical parameters considered are the
severity of gingival recession, progression of recession, width
of remaining keratinised gingiva, frenal involvement, vestib-
ular depth, presence of marginal gingival inflammation, den-
tinal hypersensitivity and aesthetic concerns.117

Periodontal maintenance therapy

For patients with a history of periodontal disease, periodontal

maintenance should be provided on a regular and recurrent
basis, generally at intervals of 2−6 months;136,137 however,
the appropriate interval should be determined following
completion of active periodontal therapy, and modified by
continuously assessing an individual’s risk for periodonti-
tis.137 Among the factors to be considered are medical history
(i.e. diagnosis of diabetes), smoking habit, presence of resid-
Fig. 8 – Regenerative periodontal therapy on a mandibular
ual sites with deep probing depths, presence of other afore-
right second molar. (a) Pre-operative radiograph; the mandib-
mentioned contributing factors, and the level of home
ular right second molar exhibited a vertical bone loss on its
care.137 A regular recall interval allows timely detection and
distal surface. (b) Post-operative radiograph; after 5 months
intervention upon the recurrence or re-activation of disease
of healing following laser-assisted periodontal regenerative
in patients who have been previously treated for periodonti-
therapy, an increase in the height of alveolar bone was noted
tis.136 For example, compared to erratic and non-compliant
on the distal surface of the mandibular right second molar.
patients, compliant patients who regularly attended peri-
(c) Post-operative radiograph; after 10 months of healing
odontal maintenance therapy exhibited a significantly
following laser-assisted periodontal regenerative therapy.
reduced tooth loss due to periodontitis.138 During mainte-
Further increase in the height of alveolar bone as well as an
nance therapy, periodontal charting should be updated
increase in alveolar bone density were noted on the distal
and radiographs obtained as needed. Furthermore, home
surface of the mandibular right second molar.
care should be thoroughly reviewed. For areas with persis-
tently deep or progressing periodontal probing depths, re-
Similarly, enamel matrix derivatives (EMD) have been initiating active periodontal therapy (i.e. scaling and root
used in periodontal regenerative therapy with the intent of planing, and surgical periodontal therapy) should be
inducing cell proliferation of both osteoblasts and periodontal considered.136
 management of periodontitis 471

arrest of periodontitis but when feasible the regeneration

of periodontium lost as a result of disease.139 Traditional
resective periodontal surgery offers reliable methods to
access root surfaces, reduce periodontal probing depths
and attain improved periodontal architecture.139 However,
these procedures offer only limited potential towards
recovering tissues destroyed during earlier active dis-
ease.139 The introduction of new biological modifiers and
new approaches to successful periodontal regeneration
indicates a trend favouring conservative surgical ther-
apy.139 This represents a fundamental shift in the intent of
periodontal surgery, away from tissue removal to an
approach that maintains existing periodontium and seeks
to re-establish support that was lost.
With the introduction of dental implants, a natural
tooth with a compromised periodontal prognosis may be
extracted and replaced with a dental implant instead of
receiving periodontal therapy. However, while implant
retention is high (at least 90% after 5 years), a meta-analy-
sis of a total of 6,283 implants estimated the frequency of
peri-implant mucositis and peri-implantitis as 30.7% and
9.6%, respectively, indicating that implant therapy is not
without complications.140 Furthermore, peri-implantitis
and periodontitis appeared to share common risk factors
such as poor oral hygiene, smoking and diabetes.141,142 The
previous history of periodontitis as well as having a resid-
ual site with a periodontal depth of 6 mm or more were
also associated with greater odds for developing peri-
implantitis.141,143−145 Thus, the premature and strategic
removal of a tooth with periodontitis for the sake of deliv-
ering implant therapy should be avoided.146 In addition,
when considering extraction of a tooth due to periodontitis
and subsequent replacement with a dental implant, clini-
cians should inform patients regarding the potential risk of
developing peri-implantitis, which may ultimately result in
implant failure.147
Lastly, there is now a robust literature indicating an
association between periodontitis and certain systemic
conditions.14,148,149 Although a detailed discussion of this
topic is beyond the scope of this review, this research has
Fig. 9 – Different types of periodontal alveolar defects. (a) resulted in a shift in how periodontitis and treatment of
Two-walled alveolar defect (mesial and palatal walls). (b) periodontal disease are considered in the larger context of
Three-walled alveolar defect (distal, lingual and buccal general health.150−152
walls; photograph courtesy of Dr Howard Yen, periodontist).
(c) Combined alveolar defect (coronally 1-walled defect and
apically 3-walled defect). Conclusions

Careful diagnosis, elimination of the causes and reduction

of modifiable risk factors are paramount for successful
prevention and treatment of periodontitis. Following the
Decision tree and current trends completion of initial non-surgical periodontal therapy pre-
dominantly consisting of home care review and scaling
A decision tree representing the management of a patient and root planing, contemporary regenerative or traditional
with periodontitis can be helpful (Figure 10), recognising resective surgical therapies can be utilized to eradicate
that the goals of periodontal therapy include not only the any residual site with active periodontitis. Thereafter,
472 kwon et al.

Fig. 10 – A decision tree for treating a patient with periodontitis.

periodontal maintenance therapy and long-term follow-up 4. Page RC, Eke PI. Case definitions for use in population-based
are also crucial to the success of the treatment and long- surveillance of periodontitis. J Periodontol 2007;78(7
term retention of teeth. Suppl):1387–99.
5. Brunsvold MA. Pathologic tooth migration. J Periodontol
2005;76:859–66.
6. Eke PI, Thornton-Evans GO, Wei L, et al. Periodontitis in US
R EF E R E N CE S Adults: National Health and Nutrition Examination Survey
2009−2014. J Am Dent Assoc 2018;149 576−588.e6.
7. Richards D. Review finds that severe periodontitis affects
1. Slots J. Periodontitis: facts, fallacies and the future. Periodon- 11% of the world population. Evid Based Dent 2014;15:70–1.
tol 2000 2017;75:7–23. 8. Kassebaum NJ, Bernabe E, Dahiya M, et al. Global burden of
2. Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: con- severe periodontitis in 1990−2010: a systematic review and
sensus report of workgroup 2 of the 2017 World Workshop on meta-regression. J Dent Res 2014;93:1045–53.
the Classification of Periodontal and Peri-Implant Diseases 9. Frencken JE, Sharma P, Stenhouse L, et al. Global epidemiol-
and Conditions. J Periodontol 2018;89(Suppl 1):S173–82. ogy of dental caries and severe periodontitis - a comprehen-
3. Page RC, Offenbacher S, Schroeder HE, et al. Advances in the sive review. J Clin Periodontol 2017;44(Suppl 18):S94–S105.
pathogenesis of periodontitis: summary of developments, 10. International Diabetes Federation. Global diabetes data
clinical implications and future directions. Periodontol 2000 report 2010−2045. Available from: https://diabetesatlas.org/
1997;14:216–48. data/. Accessed May 9, 2020.
 management of periodontitis 473

11. World Health Organization. WHO fact sheet on hyperten- 34. Chigasaki O, Takeuchi Y, Aoki A, et al. A cross-sectional
sion. Available from: https://www.who.int/news-room/fact- study on the periodontal status and prevalence of red com-
sheets/detail/hypertension. Accessed May 9, 2020. plex periodontal pathogens in a Japanese population. J Oral
12. World Health Organization. WHO fact sheet on depression. Sci 2018;60:293–303.
Available from: https://www.who.int/news-room/fact- 35. Persson L, Bergstro € m J, Ito H, et al. Tobacco smoking and
sheets/detail/depression. Accessed May 9, 2020. neutrophil activity in patients with periodontal disease. J
13. World Health Organization. WHO factsheet on asthma. Periodontol 2001;72:90–5.
Available from: https://www.who.int/news-room/fact- 36. Shivanaikar SS, Faizuddin M, Bhat K. Effect of smoking on
sheets/detail/asthma. Accessed May 9, 2020. neutrophil apoptosis in chronic periodontitis: an immuno-
14. Beck JD, Papapanou PN, Philips KH, et al. Periodontal medi- histochemical study. Indian J Dent Res 2013;24:147.
cine: 100 years of progress. J Dent Res 2019;98:1053–62. 37. White PC, Hirschfeld J, Milward MR, et al. Cigarette smoke
15. Borges T de F, Regalo SC, Taba Jr M, et al. Changes in masti- modifies neutrophil chemotaxis, neutrophil extracellular
catory performance and quality of life in individuals with trap formation and inflammatory response-related gene
chronic periodontitis. J Periodontol 2013;84:325–31. expression. J Periodontal Res 2018;53:525–35.
16. Graziani F, Music L, Bozic D, et al. Is periodontitis and its 38. Grossi SG, Zambon JJ, Ho AW, et al. Assessment of risk for
treatment capable of changing the quality of life of a patient? periodontal disease. I. Risk indicators for attachment loss. J
Br Dent J 2019;227:621–5. Periodontol 1994;65:260–7.
17. Socransky SS, Haffajee AD, Cugini MA, et al. Microbial com- 39. Nociti FH, Casati MZ, Duarte PM. Current perspective of the
plexes in subgingival plaque. J Clin Periodontol 1998;25:134– impact of smoking on the progression and treatment of peri-
44. odontitis. Periodontol 2000 2015;67:187–210.
18. Socransky SS, Haffajee AD. Periodontal microbial ecology. 40. Mu € ller Campanile V, Megally A, Campanile G, et al. Risk fac-
Periodontol 2000 2005;38:135–87. tors for recurrence of periodontal disease in patients in
19. Haffajee AD, Socransky SS. Microbial etiological agents of maintenance care in a private practice. J Clin Periodontol
destructive periodontal diseases. Periodontol 2000 1994;5:78– 2019;46:918–26.
111. 41. Ryder MI, Couch ET, Chaffee BW. Personalized periodontal
20. Mohanty R, Asopa SJ, Joseph MD, et al. Red complex: polymi- treatment for the tobacco- and alcohol-using patient. Perio-
crobial conglomerate in oral flora: a review. J Family Med dontol 2000 2018;78:30–46.
Prim Care 2019;8:3480–6. 42. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in
21. Mysak J, Podzimek S, Sommerova P, et al. Porphyromonas non-insulin-dependent diabetes mellitus. J Periodontol 1991;
gingivalis: major periodontopathic pathogen overview. J 62:123–31.
Immunol Res 2014;2014:476068. 43. Mealey BL, Oates TW. Diabetes mellitus and periodontal dis-
22. Singhrao SK, Harding A, Poole S, et al. Porphyromonas gingi- eases. J Periodontol 2006;77:1289–303.
valis periodontal infection and its putative links with 44. Schmidt AM, Weidman E, Lalla E, et al. Advanced glycation
Alzheimer’s disease. Mediators Inflamm 2015;2015:137357. endproducts (AGEs) induce oxidant stress in the gingiva: a
23. Sharma A. Virulence mechanisms of Tannerella forsythia. potential mechanism underlying accelerated periodontal
Periodontol 2000 2010;54:106–16. disease associated with diabetes. J Periodontal Res 1996;31:
24. Dashper SG, Seers CA, Tan KH, et al. Virulence factors of the 508–15.
oral spirochete Treponema denticola. J Dent Res 2011;90: 45. Lalla E, Lamster IB, Schmidt AM. Enhanced interaction of
691–703. advanced glycation end products with their cellular receptor
25. Birkedal-Hansen H. Role of matrix metalloproteinases in RAGE: implications for the pathogenesis of accelerated peri-
human periodontal diseases. J Periodontol 1993;64(Suppl odontal disease in diabetes. Ann Periodontol 1998;3:13–9.
5S):474–84. 46. Lalla E, Lamster IB, Drury S, et al. Hyperglycemia, glycoxida-
26. Taubman MA, Kawai T. Involvement of T-lymphocytes in tion and receptor for advanced glycation endproducts:
periodontal disease and in direct and indirect induction of potential mechanisms underlying diabetic complications,
bone resorption. Crit Rev Oral Biol Med 2001;12:125–35. including diabetes-associated periodontitis. Periodontol
27. Taubman MA, Valverde P, Han X, et al. Immune response: 2000 2000;23:50–62.
the key to bone resorption in periodontal disease. J Periodon- 47. Lalla E, Lamster IB, Stern DM, et al. Receptor for advanced
tol 2005;76(11 Suppl):2033–41. glycation end products, inflammation, and accelerated peri-
28. Socransky SS, Haffajee AD, Goodson JM, et al. New concepts odontal disease in diabetes: mechanisms and insights into
of destructive periodontal disease. J Clin Periodontol 1984;11: therapeutic modalities. Ann Periodontol 2001;6:113–8.
21–32. 48. Lamster IB, Cheng B, Burkett S, et al. Periodontal findings in
29. Lo€ e H, Anerud A, Boysen H, et al. Natural history of periodon- individuals with newly identified pre-diabetes or diabetes
tal disease in man. Rapid, moderate and no loss of attach- mellitus. J Clin Periodontol 2014;41:1055–60.
ment in Sri Lankan laborers 14 to 46 years of age. J Clin 49. Jeffcoat MK, Howell TH. Alveolar bone destruction due to
Periodontol 1986;13:431–45. overhanging amalgam in periodontal disease. J Periodontol
30. Haffajee AD, Socransky SS. Attachment level changes in 1980;51:599–602.
destructive periodontal diseases. J Clin Periodontol 1986; 50. Jansson L, Ehnevid H, Lindskog S, et al. Proximal restorations
13:461–75. and periodontal status. J Clin Periodontol 1994;21:577–82.
31. Goodson JM, Tanner AC, Haffajee AD, et al. Patterns of pro- 51. Koral SM, Howell TH, Jeffcoat MK. Alveolar bone loss due to
gression and regression of advanced destructive periodontal open interproximal contacts in periodontal disease. J Perio-
disease. J Clin Periodontol 1982;9:472–81. dontol 1981;52:447–50.
32. Camelo-Castillo AJ, Mira A, Pico A, et al. Subgingival micro- 52. Glickman I, Smulow JB. Effect of excessive occlusal forces
biota in health compared to periodontitis and the influence upon the pathway of gingival inflammation in humans. J
of smoking. Front Microbiol 2015;6:119. Periodontol 1965;36:141–7.
33. Haffajee AD, Socransky SS. Relationship of cigarette smok- 53. Ericsson I, Lindhe J. Effect of longstanding jiggling on experi-
ing to the subgingival microbiota. J Clin Periodontol 2001; mental marginal periodontitis in the beagle dog. J Clin Perio-
28:377–88. dontol 1982;9:497–503.
474 kwon et al.

54. Anderegg CR, Metzler DG. Tooth mobility revisited. J Perio- periodontitis: =a systematic review=. BMC Oral Health 2016;
dontol 2001;72:963–7. 16:27.
55. Lang NP, Lo € e H. The relationship between the width of kera- 75. Nibali L, Koidou VP, Hamborg T, et al. Empirical or microbio-
tinized gingiva and gingival health. J Periodontol 1972;43: logically guided systemic antimicrobials as adjuncts to non-
623–7. surgical periodontal therapy? A systematic review. J Clin
56. Leknes KN, Lie T, Selvig KA. Cemental tear: a risk factor in Periodontol 2019;46:999–1012.
periodontal attachment loss. J Periodontol 1996;67:583–8. 76. Teughels W, Feres M, Oud V, et al. Adjunctive effect of sys-
57. Bower RC. Furcation morphology relative to periodontal temic antimicrobials in periodontitis therapy: a systematic
treatment: furcation root surface anatomy. J Periodontol review and meta-analysis. J Clin Periodontol 2020;47(Suppl
1979;50:366–74. 22):257–81.
58. Moskow BS, Canut PM, Studies on root enamel (2). Enamel 77. Bland PS, Goodson JM, Gunsolley JC, et al. Association of
pearls. A review of their morphology, localization, nomen- antimicrobial and clinical efficacy: periodontitis therapy
clature, occurrence, classification, histogenesis and inci- with minocycline microspheres. J Int Acad Periodontol
dence. J Clin Periodontol 1990;17:275–81. 2010;12:11–9.
59. Romeo U, Palaia G, Botti R, et al. Enamel pearls as a predis- 78. Williams RC, Paquette DW, Offenbacher S, et al. Treatment
posing factor to localized periodontitis. Quintessence Int of periodontitis by local administration of minocycline
2011;42:69–71. microspheres: a controlled trial. J Periodontol 2001;72:1535–
60. DeSanctis M, Murphy KG. The role of resective periodontal 44.
surgery in the treatment of furcation defects. Periodontol 79. Grossi SG, Goodson JM, Gunsolley JC, et al. Mechanical ther-
2000 2000;22:154–68. apy with adjunctive minocycline microspheres reduces red-
61. Richman C. Is gingival recession a consequence of an ortho- complex bacteria in smokers. J Periodontol 2007;78:1741–50.
dontic tooth size and/or tooth position discrepancy? “A para- 80. Matesanz-Pe rez P, Garcıa-Gargallo M, Figuero E, et al. A sys-
digm shift. Compend Contin Educ Dent 2011;32:e73–9. tematic review on the effects of local antimicrobials as
62. Kassab MM, Cohen RE. The etiology and prevalence of gingi- adjuncts to subgingival debridement, compared with sub-
val recession. J Am Dent Assoc 2003;134:220–5. gingival debridement alone, in the treatment of chronic peri-
63. Kwon T, Levin L. Cause-related therapy: a review and sug- odontitis. J Clin Periodontol 2013;40:227–41.
gested guidelines. Quintessence Int 2014;45:585–91. 81. Machtei EE, Hirsh I, Falah M, et al. Multiple applications of
64. Kwon T, Salem DM, Levin L. Nonsurgical periodontal therapy flurbiprofen and chlorhexidine chips in patients with
based on the principles of cause-related therapy: rationale chronic periodontitis: a randomized, double blind, parallel,
and case series. Quintessence Int 2019;50:370–6. 2-arms clinical trial. J Clin Periodontol 2011;38:1037–43.
65. Kwon T, Kim DM, Levin L. Successful nonsurgical manage- 82. Lecic J, Cakic S, Janjic Pavlovic O, et al. Different methods for
ment of post-orthodontic gingival enlargement with inten- subgingival application of chlorhexidine in the treatment of
sive cause-related periodontal therapy. N Y State Dent J patients with chronic periodontitis. Acta Odontol Scand
2015;81:21–3. 2016;74:502–7.
66. Kwon T, Wang JCW, Levin L. Home care is therapeutic. 83. Caton JG, Ciancio SG, Blieden TM, et al. Treatment with sub-
Should we use the term “Home-care Therapy” Instead of antimicrobial dose doxycycline improves the efficacy of scal-
“Instructions”? Oral Health Prev Dent 2020;18:397–8. ing and root planing in patients with adult periodontitis. J
67. Oosterwaal PJ, Matee MI, Mikx FH, et al. The effect of subgin- Periodontol 2000;71:521–32.
gival debridement with hand and ultrasonic instruments on 84. Caton JG, Ciancio SG, Blieden TM, et al. Subantimicrobial
the subgingival microflora. J Clin Periodontol 1987;14:528–33. dose doxycycline as an adjunct to scaling and root planing:
68. Matia JI, Bissada NF, Maybury JE, et al. Efficiency of scaling of post-treatment effects. J Clin Periodontol 2001;28:782–9.
the molar furcation area with and without surgical access. 85. El-Sharkawy H, Aboelsaad N, Eliwa M, et al. Adjunctive treat-
Int J Periodontics Restorative Dent 1986;6:24–35. ment of chronic periodontitis with daily dietary supplemen-
69. Winkel EG, Van Winkelhoff AJ, Timmerman MF, et al. Amox- tation with omega-3 Fatty acids and low-dose aspirin. J
icillin plus metronidazole in the treatment of adult peri- Periodontol 2010;81:1635–43.
odontitis patients. A double-blind placebo-controlled study. 86. Castro Dos Santos NC, Andere NM, Araujo CF, et al. Omega-3
J Clin Periodontol 2001;28:296–305. PUFA and aspirin as adjuncts to periodontal debridement in
70. Haffajee AD, Socransky SS, Gunsolley JC. Systemic anti- patients with periodontitis and type 2 diabetes mellitus: ran-
infective periodontal therapy. A systematic review. Ann domized clinical trial [published online ahead of print Feb
Periodontol 2003;8:115–81. 26, 2020]. J Periodontol 2020. doi: 10.1002/JPER.19-0613.
71. Liaw A, Miller C, Nimmo A. Comparing the periodontal tissue 87. Botero JE, Yepes FL, Ochoa SP, et al. Effects of periodontal
response to non-surgical scaling and root planing alone, non-surgical therapy plus azithromycin on glycemic control
adjunctive azithromycin, or adjunctive amoxicillin plus met- in patients with diabetes: a randomized clinical trial. J Peri-
ronidazole in generalized chronic moderate-to-severe peri- odontal Res 2013;48:706–12.
odontitis: a preliminary randomized controlled trial. Aust 88. Haas AN, Seleme F, Segatto P, et al. Azithromycin as an
Dent J 2019;64:145–52. adjunctive treatment of aggressive periodontitis: radio-
72. Borges I, Faveri M, Figueiredo LC, et al. Different antibi- graphic findings of a 12-month randomized clinical trial. Am
otic protocols in the treatment of severe chronic peri- J Dent 2012;25:215–9.
odontitis: a 1-year randomized trial. J Clin Periodontol 89. Mascarenhas P, Gapski R, Al-Shammari K, et al. Clinical
2017;44:822–32. response of azithromycin as an adjunct to non-surgical peri-
73. McGowan K, McGowan T, Ivanovski S. Optimal dose and odontal therapy in smokers. J Periodontol 2005;76:426–36.
duration of amoxicillin-plus-metronidazole as an adjunct to 90. O’Rourke VJ. Azithromycin as an adjunct to non-surgical
non-surgical periodontal therapy: a systematic review and periodontal therapy: a systematic review. Aust Dent J
meta-analysis of randomized, placebo-controlled trials. J 2017;62:14–22.
Clin Periodontol 2018;45:56–67. 91. Oliveira AMSD, Costa FO, Nogueira LMR, et al. Azithromycin
74. Zandbergen D, Slot DE, Niederman R, et al. The concomitant and full-mouth scaling for the treatment of generalized
administration of systemic amoxicillin and metronidazole stage III and IV periodontitis: a 6-month randomized com-
compared to scaling and root planing alone in treating parative clinical trial. Braz Dent J 2019;30:429–36.
 management of periodontitis 475

92. Baltacioglu E, Aslan M, Saraç O, € et al. Analysis of clinical 110. Stahl SS, Froum SJ, Kushner L. Periodontal healing following
results of systemic antimicrobials combined with nonsurgi- open debridement flap procedures. II. Histologic observa-
cal periodontal treatment for generalized aggressive peri- tions. J Periodontol 1982;53:15–21.
odontitis: a pilot study. J Can Dent Assoc 2011;77:b97. 111. Stahl SS, Froum SJ, Kushner L. Healing responses of human
93. Machtei EE, Younis MN. The use of 2 antibiotic regimens in intraosseous lesions following the use of debridement, grafting
aggressive periodontitis: comparison of changes in clinical and citric acid root treatment. II. Clinical and histologic obser-
parameters and gingival crevicular fluid biomarkers. Quin- vations: one year postsurgery. J Periodontol 1983;54:325–38.
tessence Int 2008;39:811–9. 112. Yukna RA, Bowers GM, Lawrence JJ, et al. A clinical study of
94. Akincibay H, Orsal SO, Sengu € n D, et al. Systemic adminis- healing in humans following the excisional new attachment
tration of doxycycline versus metronidazole plus amoxicil- procedure. J Periodontol 1976;47:696–700.
lin in the treatment of localized aggressive periodontitis: a 113. Ramfjord SP, Nissle RR. The modified widman flap. J Perio-
clinical and microbiologic study. Quintessence Int 2008;39: dontol 1974;45:601–7.
e33–9. 114. Ramfjord SP, Knowles JW, Nissle RR, et al. Results following
95. Salvi GE, Stahli A, Schmidt JC, et al. Adjunctive laser or anti- three modalities of periodontal therapy. J Periodontol 1975;
microbial photodynamic therapy to non-surgical mechani- 46:522–6.
cal instrumentation in patients with untreated periodontitis: 115. Carnevale G, Kaldahl WB. Osseous resective surgery. Perio-
a systematic review and meta-analysis. J Clin Periodontol dontol 2000 2000;22:59–87.
2020;47:176–98. 116. Canakçi CF, Canakçi V. Pain experienced by patients under-
96. Roncati M, Gariffo A. Systematic review of the adjunctive use going different periodontal therapies. J Am Dent Assoc
of diode and Nd:YAG lasers for nonsurgical periodontal 2007;138:1563–73.
instrumentation. Photomed Laser Surg 2014;32:186–97. 117. Clark D, Levin L. Non-surgical management of tooth hyper-
97. Sgolastra F, Severino M, Gatto R, et al. Effectiveness of diode sensitivity. Int Dent J 2016;66:249–56.
laser as adjunctive therapy to scaling root planning in the 118. Feller L, Lemmer J. Tooth mobility after periodontal surgery.
treatment of chronic periodontitis: a meta-analysis. Lasers SADJ 2004;59:409–11.
Med Sci 2013;28:1393–402. 119. Checchi L, Montevecchi M, Checchi V, et al. A modified
98. Invernici MM, Salvador SL, Silva PHF, et al. Effects of Bifido- papilla preservation technique, 22 years later. Quintessence
bacterium probiotic on the treatment of chronic periodonti- Int 2009;40:303–11.
tis: a randomized clinical trial. J Clin Periodontol 2018;45: 120. Villar CC, Cochran DL. Regeneration of periodontal tissues:
1198–210. guided tissue regeneration. Dent Clin North Am 2010;54:73–92.
99. Ikram S, Hassan N, Raffat MA, et al. Systematic review and 121. Chavda S, Levin L. Human studies of vertical and horizontal
meta-analysis of double-blind, placebo-controlled, random- alveolar ridge augmentation comparing different types of
ized clinical trials using probiotics in chronic periodontitis. J bone graft materials: a systematic review. J Oral Implantol
Investig Clin Dent 2018;9:e12338. 2018;44:74–84.
100. de Andrade DP, Carvalho ICS, Gadoi BH, et al. Subgingival 122. Cortellini P, Pini Prato G, Tonetti MS. Periodontal regenera-
irrigation with a solution of 20% propolis extract as an tion of human infrabony defects. I. Clinical measures. J
adjunct to non-surgical periodontal treatment: a preliminary Periodontol 1993;64:254–60.
study. J Int Acad Periodontol 2017;19:145–51. 123. Cortellini P, Pini Prato G, Tonetti MS. Periodontal regenera-
101. El-Sharkawy HM, Anees MM, Van Dyke TE. Propolis tion of human infrabony defects. II. Re-entry procedures and
improves periodontal status and glycemic control in bone measures. J Periodontol 1993;64:261–8.
patients with type 2 diabetes mellitus and chronic peri- 124. Tonetti MS, Pini Prato G, Williams RC, et al. Periodontal
odontitis: a randomized clinical trial. J Periodontol regeneration of human infrabony defects. III. Diagnostic
2016;87:1418–26. strategies to detect bone gain. J Periodontol 1993;64:269–77.
102. Zhao H, Hu J, Zhao L. Adjunctive subgingival application of 125. Tonetti MS, Pini-Prato G, Cortellini P. Periodontal regenera-
Chlorhexidine gel in nonsurgical periodontal treatment for tion of human intrabony defects. IV. Determinants of heal-
chronic periodontitis: a systematic review and meta-analy- ing response. J Periodontol 1993;64:934–40.
sis. BMC Oral Health 2020;20:34. 126. Reynolds MA, Kao RT, Camargo PM, et al. Periodontal regenera-
103. Sanz M, Herrera D, Kebschull M, et al. Treatment of stage I-III tion - intrabony defects: a consensus report from the AAP
periodontitis-The EFP S3 level clinical practice guideline. J Regeneration Workshop. J Periodontol 2015;86(2 Suppl):S105–7.
Clin Periodontol 2020;47(Suppl 22):4–60. 127. Nevins M, Camelo M, Nevins ML, et al. Periodontal regenera-
104. Rabbani GM, Ash MM, Caffesse RG. The effectiveness of sub- tion in humans using recombinant human platelet-derived
gingival scaling and root planing in calculus removal. J Perio- growth factor-BB (rhPDGF-BB) and allogenic bone. J Perio-
dontol 1981;52:119–23. dontol 2003;74:1282–92.
105. Stambaugh RV, Dragoo M, Smith DM, et al. The limits of 128. Camelo M, Nevins ML, Schenk RK, et al. Periodontal regener-
subgingival scaling. Int J Periodontics Restorative Dent ation in human Class II furcations using purified recombi-
1981;1:30–41. nant human platelet-derived growth factor-BB (rhPDGF-BB)
106. Steffensen B, Webert HP. Relationship between the radio- with bone allograft. Int J Periodontics Restorative Dent
graphic periodontal defect angle and healing after treat- 2003;23:213–25.
ment. J Periodontol 1989;60:248–54. 129. Khoshkam V, Chan H-L, Lin G-H, et al. Outcomes of regener-
107. Papapanou PN, Wennstro € m JL. The angular bony defect as ative treatment with rhPDGF-BB and rhFGF-2 for periodontal
indicator of further alveolar bone loss. J Clin Periodontol intra-bony defects: a systematic review and meta-analysis. J
1991;18:317–22. Clin Periodontol 2015;42:272–80.
108. Schluger S. Osseous resection; a basic principle in periodon- 130. Miron RJ, Chandad F, Buser D, et al. Effect of enamel
tal surgery. Oral Surg Oral Med Oral Pathol 1949;2:316–25. matrix derivative liquid on osteoblast and periodontal lig-
109. Froum SJ, Coran M, Thaller B, et al. Periodontal healing fol- ament cell proliferation and differentiation. J Periodontol
lowing open debridement flap procedures. I. Clinical assess- 2016;87:91–9.
ment of soft tissue and osseous repair. J Periodontol 1982; 131. Miron RJ, Bosshardt DD, Laugisch O, et al. In vitro evaluation
53:8–14. of demineralized freeze-dried bone allograft in
476 kwon et al.

combination with enamel matrix derivative. J Periodontol 142. Ferreira SD, Silva GLM, Cortelli JR, et al. Prevalence and risk
2013;84:1646–54. variables for peri-implant disease in Brazilian subjects. J Clin
132. Koop R, Merheb J, Quirynen M. Periodontal regeneration Periodontol 2006;33:929–35.
with enamel matrix derivative in reconstructive peri- 143. Renvert S, Aghazadeh A, Hallstro € m H, et al. Factors related to
odontal therapy: a systematic review. J Periodontol 2012; peri-implantitis - a retrospective study. Clin Oral Implants
83:707–20. Res 2014;25:522–9.
133. Nevins M, Kim S-W, Camelo M, et al. A prospective 9-month 144. Swierkot K, Lottholz P, Flores-de-Jacoby L, et al. Mucositis,
human clinical evaluation of Laser-Assisted New Attach- peri-implantitis, implant success, and survival of implants
ment Procedure (LANAP) therapy. Int J Periodontics Restor- in patients with treated generalized aggressive periodontitis:
ative Dent 2014;34:21–7. 3- to 16-year results of a prospective long-term cohort study.
134. Nevins ML, Camelo M, Schupbach P, et al. Human clinical J Periodontol 2012;83:1213–25.
and histologic evaluation of laser-assisted new attachment 145. Cho-Yan Lee J, Mattheos N, Nixon KC, et al. Residual peri-
procedure. Int J Periodontics Restorative Dent 2012;32: odontal pockets are a risk indicator for peri-implantitis in
497–507. patients treated for periodontitis. Clin Oral Implants Res
135. Mills MP, Rosen PS, Chambrone L, et al. American Academy 2012;23:325–33.
of Periodontology best evidence consensus statement on the 146. Kwon T, Bain PA, Levin L. Systematic review of short- (5−10
efficacy of laser therapy used alone or as an adjunct to non- years) and long-term (10 years or more) survival and success
surgical and surgical treatment of periodontitis and peri- of full-arch fixed dental hybrid prostheses and supporting
implant diseases. J Periodontol 2018;89:737–42. implants. J Dent 2014;42:1228–41.
136. Cohen RE. Research, Science and Therapy Committee, Amer- 147. Clark D, Levin L. In the dental implant era, why do we still
ican Academy of Periodontology. Position paper: periodontal bother saving teeth? Dent Traumatol 2019;35:368–75.
maintenance. J Periodontol 2003;74:1395–401. 148. Monsarrat P, Blaizot A, Ke moun P, et al. Clinical research
137. Surveillance Report 2018 − Dental Checks. Intervals activity in periodontal medicine: a systematic mapping of
between Oral Health Reviews (2004) NICE Guideline CG19. trial registers. J Clin Periodontol 2016;43:390–400.
London: National Institute for Health and Care Excellence 149. Williams RC, Offenbacher S. Periodontal medicine: the emer-
(UK). Available from: http://www.ncbi.nlm.nih.gov/books/ gence of a new branch of periodontology. Periodontol 2000
NBK551810/. Accessed January 4, 2020. 2000;23:9–12.
138. Wilson TG, Glover ME, Malik AK, et al. Tooth loss in mainte- 150. Sanz M, Ceriello A, Buysschaert M, et al. Scientific evidence
nance patients in a private periodontal practice. J Periodon- on the links between periodontal diseases and diabetes: con-
tol 1987;58:231–5. sensus report and guidelines of the joint workshop on peri-
139. Wang H-L, Greenwell H, Fiorellini J, et al. Periodontal regen- odontal diseases and diabetes by the International Diabetes
eration. J Periodontol 2005;76:1601–22. Federation and the European Federation of Periodontology. J
140. Atieh MA, Alsabeeha NHM, Faggion CM, et al. The frequency Clin Periodontol 2018;45:138–49.
of peri-implant diseases: a systematic review and meta- 151. Lamster IB, Pagan M. Periodontal disease and the metabolic
analysis. J Periodontol 2013;84:1586–98. syndrome. Int Dent J 2017;67:67–77.
141. Levin L, Ofec R, Grossmann Y, et al. Periodontal disease as a 152. Beck JD, Slade G, Offenbacher S. Oral disease, cardiovascular
risk for dental implant failure over time: a long-term histori- disease and systemic inflammation. Periodontol 2000 2000;
cal cohort study. J Clin Periodontol 2011;38:732–7. 23:110–20.