Skip to content

Advertisement

You're viewing the new version of our site. Please leave us feedback.

Learn more

BMC Oral Health

Open Access
Open Peer Review

This article has Open Peer Review reports available.

How does Open Peer Review work?

Influence of obesity on the outcome of non-surgical periodontal therapy - a systematic review

  • Fabienne A. Gerber1,
  • Philipp Sahrmann1,
  • Oliver A. Schmidlin2,
  • Christian Heumann3,
  • Jürg Hans Beer2 and
  • Patrick R. Schmidlin1Email author
BMC Oral HealthBMC series – open, inclusive and trusted201616:90

https://doi.org/10.1186/s12903-016-0272-2

Received: 28 January 2016

Accepted: 11 August 2016

Published: 2 September 2016

Abstract

Background

Obesity and periodontitis are important chronic health problems. Obesity is associated with an increased prevalence of periodontitis. Whether obesity also affects the outcome of non-surgical periodontal therapy is to date still unclear.

Methods

A systematic review of studies referenced in SCOPUS, MEDLINE, PubMed, Cochrane, CINAHL, Biosis and Web of Science was performed. Titles, abstracts and finally full texts were scrutinized for possible inclusion by two independent investigators. Quality and heterogeneity of the studies were assessed and the study designs were examined. Probing pocket depth reduction was analyzed as primary surrogate parameter for therapeutic success after non-surgical periodontal therapy.

Results

One-hundred-and-fifty-nine potentially qualifying studies were screened. Eight studies fulfilled the inclusion criteria and were analyzed. Three of eight studies failed to show an influence of obesity on pocket depth reduction after non-surgical therapy. The remaining five studies documented a clear negative effect on the outcome of non-surgical periodontal therapy. The finally included studies did not correspond to the highest level of quality (RCTs). Due to the heterogeneity of the data a meta-analysis was not possible.

Conclusion

The literature on the effect of obesity on the treatment outcome of non-surgical periodontal therapy remains controversial. The data, however, support that obesity is not only a factor associated with poorer periodontal health but might also result in inferior response to non-surgical treatment of periodontitis.

Keywords

ObesityChronic periodontitisNon-surgical periodontal therapyOutcome

Background

The prevalence of obesity is increasing worldwide and is becoming one of the most important health hazards [1], as obesity is highly associated with increased overall morbidity and mortality [2].

Obesity is defined with a body mass index (BMI; body weight in kilogram divided by the square of the height in meters (kg/m2)) of at least 30.0 kg/m2 [3], whereas overweight is defined with a BMI of 25–29.9 kg/m2. Normal weight is characterized by a BMI ranging between 19 to 24.9 kg/m2 [4]. In this context, BMI seems a valuable parameter to predict obesity-related disease risks in a wide range of populations [2]. There are, however, some limitations: Firstly, risk assessment by BMI is less applicable in persons over 65 years of age because they generally have a higher body fat content for the same BMI. Secondly, the abdominal (central, visceral, android) type of obesity, which is more often seen in men, is associated with higher morbidity than the rather female type of gluteofemoral (peripheral, gynoid) obesity and, thirdly, the BMI cut-off points for overweight and obesity are too high for Asian people [2]. In addition, current large studies have indicated that measurement of waist circumference (WC) or waist-to-hip-ratio (WHR) may be a better disease risk predictor than BMI [5, 6]. There is, however, currently intensive research and debate as to whether BMI, WC, WHR, or all of them should be used to assess disease risk [2].

For the purpose of this systematic review, however, only BMI is the most frequently reported data of obesity in a large number of studies.

Adipose tissue contains usually 5-10 % macrophages, but the adipose tissue of obese patients shows up to 60 % macrophage infiltration [4]. Adipocytes secrete bioactive molecules called adipokines, that can modify or trigger inflammation and fat metabolism locally or systemically as signaling molecules to liver, muscle and endothelium [4]. Therefore, the adipose tissue can be considered as an important metabolically active endocrine organ [4].

This explains how obesity acts as a risk factor for several chronic diseases: Hypertension, type 2 diabetes, dyslipidemia, and coronary heart disease are so closely related to obesity that obesity itself is often considered to be a systemic disease. This disease also affects dental health [7]. Accordingly obese persons require attention of physicians and dentists [2].

Among dental pathologies, periodontitis is a very common, primarily bacterial inflammatory disease, which destroys teeth surrounding soft tissues and bone. It leads to pocket formation and ultimately to loss of teeth if no effective treatment is applied [8]. Periodontitis is no longer considered only an oral health issue but also a public health problem, as it constitutes a risk factor for cardiovascular conditions, poor glycemic control in diabetics and adverse outcome of pregnancy [4, 8]. These correlations coincide with obesity and general health.

Recently, it has been suggested that obesity is a possible risk factor for periodontitis [8]. One study identified obesity even as the second strongest risk factor for periodontitis preceded only by smoking [9]. The first report on the relationship between obesity and periodontal disease appeared in 1977. Perlstein and co-workers [10] found greater alveolar bone resorption in obese than in non-obese rats. Under healthy oral conditions, obesity itself did not promote periodontal damage, but in the presence of bacterial plaque accumulation periodontal inflammation was more severe in obese than in non-obese animals. With concomitant arterial hypertension, plaque accumulation caused even more pronounced periodontal destruction than with obesity alone. These results suggest that a combination of risk factors, such as the one defined by the metabolic syndrome, elicit a more severe periodontal effect [10, 11]. Chaffee et al. [12] found in their meta-analysis an increased prevalence odds ratio for obesity among subjects with periodontal disease of approximately one-third, a greater mean clinical attachment loss (CAL) among obese individuals, a higher BMI among subjects with periodontal disease, and a trend for linear increase in the odds of periodontal disease with increasing BMI [4, 12]. Finally the association reported between obesity and periodontitis was less strong than that reported between periodontal disease and adverse pregnancy outcomes [12, 13] or cardiovascular events [12, 14]. There seems, however, to be a stronger obesity-periodontitis association in women, non-smokers and younger individuals than in the general adult populations [12]. In addition, smoking remains another well-studied predisposing factor for periodontitis [12, 15, 16]. Thus, BMI and smoking share a complex relationship [17]. This relationship can be inverse in certain populations [12, 18, 19].

The biological mechanism by which obesity predisposes to periodontitis is not fully understood [8]. Compared to individuals with normal weight individuals with obesity have higher levels of circulating tumor necrosis factor-α (TNF-α) and interleukin-6 (IL-6), which are also secreted from adipose tissue and are involved in the pathophysiology of both obesity and periodontitis. Not surprisingly, serum levels of these cytokines decrease with loss of weight [20].

The objective of this systematic review was to study the hypothesis whether the clinical outcome, in terms of pocket depth reduction, after non-surgical periodontal therapy in non-obese is better than in obese individuals. To verify this hypothesis, we systematically reviewed all retrievable, qualitatively adequate clinical investigations, which focused on this topic.

Methods

The review was conducted according to the PRISMA criteria [21]. The research question was explored using the PICO method [22). The focused question addressed was:

Does non-surgical periodontal therapy (I) have a different outcome in obese chronic periodontitis patients (P), than in non-obese chronic periodontitis patients (C), regarding periodontal pocket depth reduction as the main clinical periodontal parameter (O).

Search strategy and review process

An electronic search of SCOPUS, MEDLINE, PubMed, Cochrane, CINAHL, Biosis and Web of Science was carried out considering articles published up to January 2016 in English or German language. The search was performed in two steps. The first electronic search started at 20.11.14 and an update has been done at 5.1.16.

This is shown in Table 1. For the database search, a combination of subject headings (MeSH terms and CINAHL headings) and free text search was used. An example of a detailed strategy (Medline/OvidSP) is shown in Table 2.
Table 1

Search protocols with the respective number of references dated from November 11 2014 (1) and January 1 2016 (2)

 

References 1 & 2

References after deduplication 1 & 2

Scopus

40 + 14

9 + 5

Medline

42 + 8

39 + 7

PubMed

6 + 11

2 + 11

Cochrane

12 + 2

2 + 1

CINAHL

48 + 15

42 + 13

Biosis

25 + 7

10 + 1

Web of Science

38 + 13

16 + 1

Pool

211 + 70

120 + 39

After deduplication 159 references

Table 2

Medline search strategy

Step

Query

Hits

1

Exp Periodontitis/AND (adult OR chronic*).ti,ab.

5703

2

Chronic periodontitis/OR periodontal pocket/

7004

3

2 OR 3

10454

4

((adult OR chronic*) adj3 periodontiti*).ti,ab.

5352

5

(attachment adj3 loss).ti,ab. AND ((clinical OR periodontal) adj3 attachment).ti,ab.

1305

6

(periodontal adj3 pocket).ti,ab.

1066

7

OR/3-7

12910

8

Dental scaling/ OR “root planing”/

3479

9

((subgingival OR root OR supragingival) adj3 (scaling* OR planing*)).ti,ab.

2288

10

(deep adj3 (scaling* OR cleaning)).ti,ab.

62

11

((conventional OR inital OR “non surgical” OR non-surgical OR nonsurgical) adj3 (treatment OR therapy)).ti,ab.

33417

12

OR/8-11

37131

13

7 AND 12

2184

14

Exp Obesity/

154540

15

Exp Body Weight/

369850

16

(overweight OR obese OR obesity OR adiposit* OR BMI OR “body mass index”).ti,ab.

300847

17

(cardiolipin OR lipid* OR leptin).ti,ab.

395517

18

“waist to hip”.ti,ab.

9048

19

(body adj3 weight).ti,ab.

163760

20

OR/14-19

954233

21

13 AND 20

42

The asterisk represents a wildcard and can be used in all search fields that allow words and phrases

The same search protocol was applied to all databases.

Two of the authors (FAG, PRS) screened the titles for potential eligibility according to the inclusion criteria. Based on the abstract screening, 18 studies were selected for full text review. Scores were independently allocated by both authors to each publication according to their suitability for the present review (see inclusion criteria). Any discrepancies were resolved by consensus.

Inclusion criteria

To be included studies had to be clinical interventional studies regarding the outcome of non-surgical periodontal therapy in obese or non-obese patients. The studies had to display the diagnosis of chronic periodontitis. Key parameters to be reported were data for pocket probing depth (PPD) and BMI.

Exclusion criteria

Studies were excluded for the following reasons: animal studies, case reports, commentaries, unsuitable exposure or outcome measures, confounding medical diagnoses (e.g. pregnancy or any systemic disease, such as diabetes, in addition to metabolic syndrome), confounding systemic medical treatments such as immunosuppressive treatments, cortisone or antibiotic treatment as well as confounding local treatments such as treatment of peri-mucositis, gingival overgrowth or surgical periodontal treatment. Studies including either the diagnosis of aggressive periodontitis or of peri-implantitis were excluded as well.

Outcome measures

The primary outcome measure is PPD after non-surgical periodontal treatment.

Data extraction

A list with exclusion reasons for each paper was generated. Total number of patients, demographic data, origin of study, outcome measurements 2, 3, 6 and 12 months after therapy and the impact of obesity on the treatment-outcome were extracted. In addition, the exact definition of chronic periodontitis, the assessment of the periodontal disease and the number of smokers included in the studies were summarized. Data on the individual definition of obesity and the systemic examinations were also collected. Non-surgical periodontal treatment measures, treatment time, periodontal maintenance and adverse events were also recorded for each study separately (Tables 3, 4, 5, 6 and 7).
Table 3

Excluded studies

Excluded studies

Reason for exclusion

Europerio 4 2003 [37)

Not addressing research question

Abstracts for the Royal Australian and New Zealand College of Psychiatrists 2005 [38]

Not addressing research question

5th Joint Meeting of the European Tissue Repair Society and the Wound Healing Society 2009 [39]

Not addressing research question

Recently published abstracts [40]

Not addressing research question

DENTSPLY Posters 2012 [41]

Not addressing research question

HealthBeat 2007 [42]

Not addressing research question

Abstracts for Poster Presentations 2011 [43]

Not addressing research question

Abstracts for the International Symposium on Dental Hygiene 2013 [44]

Not addressing research question

Abou Sulaiman et al. 2010 [45]

Not addressing research question

Acharya et al. 2010 [46]

No PPD reduction data

Akpinar et al. 2013 [47]

Not addressing research question

Altay et al. 2013 [20]

No PPD reduction data

Armstrong et al. 2010 [48]

Not addressing research question

Arora et al. 2013 [49]

Not addressing research question

Basegmez et al. 2011 [50]

Not addressing research question

Bresolin et al. 2013 [51]

Not addressing research question

Bresolin et al. 2014 [52]

Not addressing research question

Caspersen et al. 2012 [53]

Not addressing research question

Caula et al. 2014 [54]

No comparison

Caula et al. 2014 [54]

Duplicate

Chapple et a. 2006 [55]

Not addressing research question

Chapple et al. 2007 [56]

Not addressing research question

Chandni et al. 2015 [57]

Not addressing research question

Chaston et al. 2014 [58]

Not addressing research question

Chee et al. 2008 [59]

Inclusion of diabetes

Chee et al. 2013 [60]

Missed intervention, inclusion of diabetes

Chen et al. 2012 [61]

Inclusion of diabetes

D’Aiuto et al. 2004 [62]

Not addressing research question

D’Aiuto et al. 2004 [63]

Not addressing research question

D’Aiuto et al. 2005 [23]

No comparison

D’Aiuto et al. 2006 [64]

Not addressing research question

Deppe et al. 2010 [65]

Not addressing research question

Dodington et al. 2015 [66]

No obesity data

Draper et al. 2010 [67]

Not addressing research question

Duan et al. 2009 [24]

Written in Chinese

Edwards et al. 2006 [68]

Not addressing research question

Efurd et al. 2012 [69]

Not addressing research question

Elliott-Smith et al. 2011 [70]

Not addressing research question

Engebretson et al. 2014 [71]

Not addressing research question

Fairfield et al. 2010 [72]

Not addressing research question

Fang et al. 2015 [73]

Inclusion of end-stage renal disease patients

Fentoglu et al. 2010 [74]

Statin intake

Fine et al. 2007 [75]

Not addressing research question

Fokkema et al. 2012 [76]

Not addressing research question

Fu et al. 2015 [77]

No comparison

Garcia et al. 2010 [78]

Not addressing research question

Giblin et al. 2014 [79]

Inclusion of prediabetes

Giblin et al. 2014 [79]

Duplicate

Gluch et al. 2007 [80]

Inclusion of diabetes

Goldie et al. 2002 [81]

Not addressing research question

Goldie et al. 2004 [82]

Not addressing research question

Goldie et al. 2005 [83)

Not addressing research question

Griffin et al. 2012 [84]

Not addressing research question

Gurenlian et al. 2006 [85]

Not addressing research question

Gurenlian et al. 2009 [86]

Not addressing research question

Hammaker et al. 2010 [87]

Not addressing research question

Horwitz et al. 2007 [88]

Not addressing research question

Hovliaras-Delozier et al. 2008 [89]

Not addressing research question

Ide et al. 2004 [90]

No obesity data

Ide et al. 2007 [91]

Not addressing research question

Iwamoto et al. 2003 [25]

Application of antibiotics

Jahn et al. 2004 [92]

Not addressing research question

Jahn et al. 2015 [93]

Not addressing research question

Jaiswal et al. 2015 [94]

No treatment (SRP)

Janket et al. 2014 [95]

Meta-analysis

Janket et al. 2014 [95]

Duplicate

Jared et al. 2008 [96]

Not addressing research question

Jared et al. 2008 [96]

Duplicate

Jiang et al. 2013 [97]

Not addressing research question

Kamil et al. 2011 [98]

No obesity data

Kamilov et al. 1998 [99]

Not addressing research question

Kapellas et al. 2013 [100]

No obesity data

Kardeşler et al. 2010 [26]

Inclusion of diabetes

Keller et al. 2015 [101]

Systematic review

Kiany et al. 2014 [102]

No obesity data

Kiany et al. 2015 [103]

Duplicate

Kipp et al. 2003 [104]

Not addressing research question

Kudva et al. 2010 [105]

Inclusion of diabetes

Kumar et al. 2015 [106]

Inclusion of diabetes

Kurti et al. 2007 [107]

Not addressing research question

Kurtis et al. 2007 [108]

Duplicate

Lee et al. 2014 [109]

Not addressing research question

Li et al. 2013 [110]

No obesity data

Ling et al. 2012 [111]

Inclusion of diabetes

Lo et al. 2011 [112]

Not addressing research question

Malhotra et al. 2012 [113]

No obesity data

Mancl et al. 2013 [114]

Not addressing research question

Martinez et al. 2014 [115]

Supplementation of ω-3 eicosapetaenoic acid

Martinez et al. 2014 [116]

One year of omega-3 supplementation

Matlock et al. 2012 [117]

No treatment (SRP)

McDaniel et al. 2013 [118]

Not addressing research question

Meharwade et al. 2014 [119]

Local drug delivery

Merchant et al. 2014 [120]

Inclusion of diabetes

Michalowicz et al. 2014 [121]

Inclusion of diabetes

Mizrak et al. 2006 [122]

Not addressing research question

Moeintaghavi et al. 2012 [123]

Inclusion of diabetes

Moravec et al. 2011 [124]

No treatment (SRP)

Muthu et al. 2015 [125]

No obesity data

Nassar et al. 2012 [126]

Inclusion of diabetes

Newton et al. 2011 [127]

Not addressing research question

Nichols et al. 2001 [128]

Not addressing research question

Nielsen et al. 2000 [129]

Not addressing research question

Novakovic et al. 2013 [130]

Not addressing research question

Novakovic et al. 2014 [131]

Not addressing research question

Oliveira et al. 2011 [132]

Not addressing research question

Olsen et al. 2006 [133]

Not addressing research question

Paquette et al. 2008 [134]

Not addressing research question

Perayil et al. 2014 [135]

No obesity data

Perayil et al. 2014 [136]

Duplicate

Phillips et al. 2013 [137]

Not addressing research question

Pradeep et al. 2007 [138]

Not addressing research question

Price et al. 2010 [139]

Not addressing research question

Qiqiang et al. 2012 [140]

No obesity data

Radafshar et al. 2012 [141]

Not addressing research question

Radnai et al. 2009 [142]

Not addressing research question

Raghavendra et al. 2012 [143]

Not addressing research question

Ramirez et al. 2011 [144]

No obesity data

Rasch et al. 1995 [145]

Not addressing research question

Sadatmansouri et al. 2006 [146]

Not addressing research question

Saffi et al. 2013 [147]

Inclusion of patients with coronary disease

Saffi et al. 2013 [147]

Duplicate

Saffi et al. 2014 [148]

Inclusion of patients with coronary artery disease

Shruti et al. 2010 [27]

No obesity data

Sembene et al. 2000 [149]

Not addressing research question

Sengupta et al. 1990 [150]

Not addressing research question

Sgolastra et al. 2013 [36]

Meta-Analysis

Shimada et al. 2010 [151]

No comparison

Shimoe et al. 2011 [152]

Case report

Singh et al. 2014 [153]

Not addressing research question

Siqueira et al. 2013 [154]

Not addressing research question

Stewart et al. 2001 [155]

Inclusion of diabetes

Talbert et al. 2006 [156]

Inclusion of diabetes

Tamaki et al. 2009 [157]

No obesity data

Tamaki et al. 2011 [158]

No obesity data

Tawfig et al. 2015 [159]

No comparison

Teles et al. 2012 [160]

No comparison

Toker et al. 2012 [161]

Not addressing research question

Tuter et al. 2007 [162]

Inclusion of patients with systemic disease

Vardar et al. 2003 [163]

Not addressing research question

Van Dyke et al. 2015 [164]

Not addressing research question

Vyas et al. 2000 [165]

Not addressing research question

Wahid et al. 2013 [166]

Not addressing research question

Wang et al. 2013 [167]

Inclusion of aggressive periodontitis

Wehmeyer et al. 2013 [168]

Not addressing research question

Wei et al. 2010 [169]

No obesity data

Williams et al. 2007 [148]

No obesity data

Williams et al. 2009 [170]

Not addressing research question

Williams et al. 2009 (171]

Not addressing research question

Wood et al. 2006 [172)

Not addressing research question

Wu et al. 2015 [173)

Not addressing research question

Zare et al. 2014 [174)

Not addressing research question

Zhou et al. 2013 [175]

Inclusion of patients with systemic disease

Zuza et al. 2011 [176)

No PPD reduction data

Table 4

Probing pocket depth (PPD [mm]) as primary outcome variable

Author & year

Total number of patients

Age (mean ± SD)

Country

Outcome after 2 months

mean (± SD) at baseline – mean (± SD) at reassessment

Outcome after 3 months

mean (± SD) at baseline –

mean (± SD) at reassessment

Outcome after 6 months

mean (± SD)at baseline – mean (± SD) at reassessment

Outcome after 12 months

mean (± SD)at baseline – mean (± SD) at reassessment

Impact of obesity on the treatment - outcome

mean – reduction of PPD (± SD)

Al – Zahrani et al. 2012 [8]

Total number of patients:

40 (only women)

Normal-weight: 20

Obese: 20

Age:

Normal-weight: 43.4 (±7.8)

Obese: 44 (±8.4)

Country:

Saudi Arabia

Total sample:

2.65 (±0.47) – 2.44 (±0.41) p-value = 0.001

n.r.

n.r.

n.r.

Normal-weight:

0.19 (±0.27)

Obese:

0.23 (±0.33)

p-value = 0.663 (n. sig.)

Bouaziz et al. 2015 [28]

Total number of patients:

36

Normal-weight: 18

Obese: 18

Age:

Range from 22 to 78

Normal-weight: 51.00 (±13.1)

Obese: 51.3 (±16.7)

p-value: n. sig.

Country:

France

n.r.

Normal-weight: 3.33 (±0.92) – 2.71 (±0.40)

p-value: n. sig.

Obese: 3.22 (±0.76) – 2.78 (±0.55)

p-value: n. sig.

Normal-weight: 3.33 (±0.92) 2.45 (±0.53)

p-value < 0.05

Obese: 3.22 (±0.76) – 2.43 (±0.49)

p-value < 0.05

n.r.

Summary of Multivariable Analysis

Results (Coefficient, 95 % Cl):

%PD > 5mm after 3 months to obese

(Model 2):

p-value = 0.02

%PD > 5mm after 6 months to obese

(Model 2):

p-value = 0.005

Nb PD > 2mm after 3 months to Obese

(Model 2);

p-value = 0.02

Nb PD > 2mm after 6 months to Obese

(Model 2);

p-value = 0.06 (n.sig.)

Duzagac et al. 2015 [29]

Total number of patients:

45

Normal weight patients with periodontitis (CPNW): 15

Obese patients with periodontitis (CPO):

15

Normal weight periodontally healthy control subjects (PHNW): 15

Age:

Range from 28 to 52

CPNW: 41.06 (±7.10)

CPO: 40.66 (±7.98)

PHNW: 39.66 (±6.53)

p-value: n. sig.

Country:

Turkey

n.r.

CPNW: 3.19 (±0.38) –2.51 – (±0.06)

p-value = 0.001

CPO: 4.10 (±0.50) – 2.55 (±0.45)

p-value = 0.001

n.r.

n.r.

Number of sites with PD < 4 mm:

Baseline:

CPO: 1706

CPNW: 1766

3 months:

CPO: 2214

CPNW: 2206

% of sites with PD < 4 mm:

Baseline:

CPO: 75.4

CPNW: 77.9

3 months:

CPO: 97.9

CPNW: 97.3

Similar clinical healing;

(n. sig.)

Number of sites with PD ≥ 4 mm:

Baseline:

CPO: 556

CPNW: 502

3 months:

CPO: 48

CPNW: 32

% of sites with PD ≥ 4 mm:

Baseline:

CPO: 48

CPNW: 22.1

3 months:

CPO: 2.1

CPNW: 2.7

Similar clinical

healing;

(n. sig.)

Eldin et al. 2013 [30]

Total number of patients:

26

Overweight: 12

Obese: 14

Age:

Range from 35 to 48

Country:

Egypt

n.r.

Overweight: 0.6 (±1.29) – 0.75 (±2.12)

p-value: n.r.

Obese: 3.15 (±2.43) – 1.59 (±2.34)

p-value: n.r.

n.r.

n.r.

Overweight:

0.784

Obese:

0.209

p-value = 0.326 (n. sig.)

Gonçalves et al. 2015 [31]

Total number of patients:

39

Without obesity: 21

With obesity: 18

Age:

Without obesity: 48.4(±9.5)

With obesity: 48.8 (±5.9)

p-value= 0.85 (n. sig.)

Country:

Brazil

n.r.

Without obesity: 3.4 (±0.6) – 3.0 (±0.5)

p-value: sig.

With obesity: 3.6 (±0.6) – 3.3 (±0.6)

p-value: sig.

Without obesity:

3.4 (±0.6)- 2.7 (±0.6)

p-value: sig.

With obesity:

3.6 (±0.6) – 3.0 (±0.5)

p-value: sig.

n.r.

Without obesity

Full-mouth sites:

0-3 months: 0.44 (±0.06)

0-6 months: 0.73 (±0.07)

Initially moderate sites

(PD 4-6mm):

0-3 months: 0.87 (±0.12)

0-6 months: 1.38 (±0.14)

Initially deep sites

(PD ≥ 7mm):

0-3 months: 1.86 (±0.25)

0-6 months: 3.00 (±0.23)

With obesity

Full-mouth sites:

0-3 months: 0.30 (±0.06)

0-6 months: 0.54 (±0.07)

Initially moderate sites

(PD 4-6mm):

0-3 months: 0.70 (±0.13)

0-6 months: 1.10 (±0.15)

Initially deep sites

(PD ≥ 7mm):

0-3 months: 1.22 (±0.26)

0-6 months: 2.30 (±0.24)

p-value

(<0.05)

0.08

0.04

0.31

0.16

0.07

0.04

Gonçalves et al. 2015 [32]

Total number of patients:

40

Non-obese: 20

Obese: 20

Age:

Non-obese: 48.5 (±9.3)

Obese: 50.0 (±4.5)

p-value = 0.52 (n. sig.)

Country:

Brazil

n.r.

Non-obese: 3.4 (±0.6) – 2.9 (±0.6)

p-value: sig.

Obese: 3.6 (±0.6) – 3.3 (±0.5)

p-value: sig.

Non-obese: 3.4 (±0.6) – 2.7 (±0.6)

p-value: sig.

Obese: 3.6 (±0.6) – 3.0 (±0.5)

p-value: sig.

Non-obese: 3.4 (±0.6) – 2.6 (±0.6)

p-value: sig.

Obese: 3.6 (±0.6) – 2.9 (±0.4)

p-value: sig.

Mean PPD values (± SD):

After 3 months:

Non-obese: 2.9 (±0.6)

Obese: 3.3 (±0.5)

p = 0.25 (n. sig.)

After 6 months:

Non-obese: 2.7 (±0.6)

Obese: 3.0 (±0.5)

p = 0.04

After 12 months:

Non-obese: 2.6 (±0.6)

Obese: 2.9 (±0.4)

p = 0.03

Lakkis et al. 2011 [33]

Total number of patients:

30

Surgery: 15

Control: 15

Age:

Surgery: 45.6 (±11.1)

Control: 48.5 (±12.0)

p-value = 0.778 (n. sig.)

Country:

USA (Cleveland, Ohio)

4-6 weeks after therapy!

Surgery:

2.6 (±0.6) – 2.2 (±0.5)

p-value < 0.001

Control:

3.1 (±0.8) – 2.8 (±0.7)

p-value < 0.001

n.r.

n.r.

n.r.

Surgery:

0.45

Control:

0.28

p-value = 0.007

Suvan et al. 2014 [34]

Total number of patients:

260

Normal: 112

Overweight: 93

Obese: 55

Age:

Normal: 46.30 (±8.38)

Overweight: 47.27 (±8.93)

Obese: 46.55 (±6.87)

p-value = 0.701 (n. sig.)

Country:

Great Britain (London)

Summary of univariable GEE Analysis Results (Coefficient, 95 % Cl):

BMI [kg/m2] to PPD at 2 months

p-value = 0.055

Overweight to PPD at 2 months

p-value = 0.372 (n. sig.)

Obese to PPD at 2 months

p-value = 0.064 (n. sig.)

Summary of Multivariable GEE Analysis Results (Coefficient, 95 % Cl):

BMI [kg/m2] to PPD at 2 months

p-value = 0.013

Overweight to PPD at 2 months

p-value = 0.63 (n. sig.)

Obese to PPD at 2 months

p-value = 0.031

n.r.

n.r.

n.r.

BMI and obesity were sig. associated with mean PPD after 2 months. (p = 0.055)

Overweight was not sig. associated with PPD after 2 months (p = 0.372)

BMI had a stat. sig. linear relationship with mean PPD after 2 months (p = 0.013).

Overweight compared with normal BMI status did not demonstrate a stat. sig. association with mean PPD after 2 months (p = 0.63). Obesity compared with normal BMI status remained a stat. sig. predictor of mean PPD (p = 0.031) at 2 months in the same multivariable model.

CI confidence interval, CPNW normal weight patients with periodontitis, CPO obese patients with periodontitis, kg kilogram, m meter, mm millimeter, Nb ∆ PD number of improving PD, n.r. not reported, PD probing depth, PHNW normal weight periodontally healthy control subjects, PPD periodontal pocket depth, p probability, SD standard deviation, (n.) sig. (not) significant, stat. statistically, WHO world health organisation

Table 5

Definition of periodontitis, periodontal assessment and definition of smoking

Author & year

Definition of chronic periodontitis

Periodontal assessment

Smokers

Al – Zahrani et al. 2012 [8]

≥ 20 teeth,

CAL ≥ 3 mm at ≥ 30 of the sites

(generalized moderate/severe chronic periodontits)

Full-mouth periodontal examination on all teeth excluding 3rd molars and partially erupted teeth

Smokers excluded

Bouaziz et al. 2015 [28]

≥ 12 teeth,

≥ 30 % of sites with CAL ≥ 3 mm

(moderate-to-severe generalized chronic periodontitis)

Full-mouth clinical measurements included the following:

1) PI,

2) BOP,

3) PD (mm),

4) CAL (mm),

PI, BOP, PD, and CAL measurements were performed using a manual periodontal probe at 6 sites per tooth,

PD was defined as the distance from the free gingival margin to the bottom of the pocket/sulcus, and CAL was defined as the distance from the cemento-enamel junction to the bottom of the pocket/sulcus

Non-smoker or former smoker since ≥ 5 years

Duzagac et al. 2015 [29]

≥ 20 teeth,

PD ≥ 4 mm in ≥ 30 % of periodontal sites,

BOP in ≥ 50 % of periodontal sites,

interproximal CAL > 2 mm in ≥ 20 % of periodontal sites,

radiographic evidence of bone loss, as described

by Armitage [177]

A Williams-type periodontal probe (UNC15, Hu-Friedy, Chicago, IL, USA) was used for the measurements of periodontal parameters, including PI (Silness–Löe) [178], GI (Löe–Silness) [179], BOP, PD and CAL,

all clinical periodontal measurements were performed at 6 sites per tooth (mesiobuccal, mid-buccal, distobuccal, mesiolingual, mid-lingual and distolingual),

excluding third molars

Smokers excluded

Eldin et al. 2013 [30]

n.r.

(chronic periodontitis)

Full-mouth,

4 sites per tooth (mesio-buccal, mid-buccal, disto-buccal, mid-lingual) around each tooth

n.r.

Gonçalves et al. 2015 [31]

≥ 15 teeth excluding 3rd molars and teeth with advanced decay indicated for exodontia,

>30 % of the sites with concomitant PD and

CAL ≥4 mm and a minimum of 6 teeth distributed in the different quadrants presenting at least one site with PD and CAL ≥ 5 mm and BOP at baseline

(generalized chronic periodontitis)

6 sites per tooth on all teeth excluding 3rd molars (distance between the gingival margin and the bottom of the sulcus/pocket [mm])

Smokers excluded

Gonçalves et al. 2015 [32]

≥ 15 teeth excluding 3rd molars and teeth with advanced decay indicated for exodontia,

>30 % of the sites with concomitant PD and

CAL ≥ 4 mm and a minimum of 6 teeth distributed in the different quadrants presenting at least one site with PD and CAL ≥ 5 mm and BOP at baseline

(generalized chronic periodontitis)

6 sites per tooth (mesio-buccal, mid-buccal, disto-buccal, mesio-lingual, mid-lingual, disto-lingual) excluding third molars, with a manual periodontal probe (UNC15, Hu-Friedy, Chicago, IL, USA)

Current smokers excluded, smoking within the past 10 years excluded

Lakkis et al. 2011 [33]

≥ 20 teeth,

mean CAL ≥ 2 mm

(chronic periodontitis)

6 sites per tooth

n.r.

Suvan et al. 2014 [34]

PD > 5 mm and marginal alveolar bone loss > 30 % with > 50 % of the teeth affected

(generalized severe periodontitis)

6 sites per tooth on all teeth present

Normal-group = 47 % smokers

Overweight-group = 25 % smokers

Obese-group = 15 % smokers

p - value = 0.045 (sig. on p ≤ 0.05)

BoP bleeding on probing, CAL clinical attachment level, GI gingival index, mm millimeter, n.r. not reported, p probability, PD probing depth, PI plaque index, sig. significant

Table 6

Definition of obesity and systemic examination

Author & year

Definition of obesity

Systemic examination

Al – Zahrani et al. 2012 [8]

Normal-weight: BMI: 18.5 to < 25 kg/m2

Obese: BMI ≥ 30 kg/m2

Weight in kilograms and height in meters were measured;

BMI: (weight/height2 [kg/m2])

Bouaziz et al. 2015 [28]

Normal-weight: BMI ≥ 18.5 kg/m2 and ≤ 25 kg/m2

Obese: BMI ≥ 30 kg/m2

Weight (kg), height (m), waist/hip circumferences (cm)

weight was obtained using a calibrated scale,,

height was measured using a measuring board,

BMI: (weight/height2 [kg/m2]),

waist measurements were taken at the level of the umbilicus (cm)

hip measurements were taken at the greatest circumference with a measuring tape,

WHR: ratio of waist to hip circumference

Duzagac et al. 2015 [29]

Normal-weight (CPNW): n.r.

Obese (CPO): BMI ≥ 30 % and WHR > 0.95 for males and 0,80 for females

One trained examiner performed all anthropometric measurements:

weight (kg), height (m), waist (cm), hip (cm),

BMI: (weight/height2 [kg/m2]),

WHR: ratio of waist to hip circumference,

anthropometric measurements were repeated before the final follow-up visit to assess

whether there was any change in BMI or WHR

Eldin et al. 2013 [30]

Overweight: BMI: 25-29.9 kg/m2

Obese: BMI ≥ 30 kg/m2

According to the WHO (3)

n.r.

Gonçalves et al. 2015 [31]

Without obesity: BMI 20-29.9 kg/m2 and

WHR < 0.85 for females and < 0.9 for males

With obesity: BMI ≥ 30 kg/m2 and < 40 kg/m2 and

WHR ≥ 0.85 for females and WHR ≥ 0.9 for males

BMI: (weight/height2 [kg/m2])

WHR: ratio of waist to hip circumference

Non-obese: BMI: 20-24.9 kg/m2 and WHR below that determined for obesity (i.e. WHR < 0.85 for women and

WHR < 0.90 for men) (World Health Organization 2008)

Obese: BMI ≥ 30 and < 40 kg/m2 and concomitant WHR

≥0.85 for women and WHR ≥ 0.90 for men.

One trained examiner performed

all anthropometric measurements:

weight (kg), height (m), waist (cm) and

hip circumferences (cm)

BMI: (weight/height2 [kg/m2]),

WHR: ratio of waist to hip circumference,

anthropometric measurements were reassessed at all follow-up visits to verify that the patients did not change their obese or non-obese status during the course of the study

Lakkis et al. 2011 [33]

Control: obese (BMI ≥ 30 kg/m2)

Did not have the bariatric surgery nor did they lose weight to serve as a control group

Surgery: obese (BMI ≥ 30 kg/m2) and

≥ 40 % loss of their excess weight at ≥ 6 months after bariatric surgery

BMI: (weight/height2 [kg/m2])

Percentage of weight loss after BS

Suvan et al. 2014 [34]

Normal: BMI: 18.5-24.99 kg/m2

Overweight: BMI: 25-29.99 kg/m2

Obese: BMI ≥ 30 kg/m2

BMI: (weight/height2 [kg/m2])

Based upon height and weight of the individual measured with a wall-mounted height measure and mechanical scales

BF body fat, BMI body mass index, BS bariatric surgery, cm centimeter, CPNW normal weight patients with periodontitis, CPO obese patients with periodontitis, HDL high-density lipoprotein, kg kilogram, m meter, n. r. not reported, WC waist circumference, WHO world health organization, WHR waist-hip-ratio

Table 7

Non-surgical periodontal treatment, treatment time and limitations

Author & Year

Non-surgical periodontal treatment

Treatment time;

periodontal maintenance

Limitations

Al – Zahrani et al. 2012 [8]

Oral hygiene instructions,

SRP performed by one operator

n.r.;

n.r.

n.r.

Bouaziz et al. 2015 [28]

Oral hygiene instructions (brushing technique: Bass technique, use of interproximal hygiene devices, CHX mouthwash (0.12 %) twice a day for 7 days),

SRP under local anesthesia using an ultrasonic device and manual curets,

aim of each session was to remove biofilms and calculus of scaled roots,

treatment protocol did not include antibiotic treatment,

all treatments procedures were performed by the same periodontist (WB)

2-3 sessions for probing depth (PD) > 5 mm lasting 1 h each within 7 days;

Oral hygiene was controlled at each appointment,

hygiene instructions were repeated if needed

at the 3-month examination, reinstruction of oral hygiene methods was performed if needed, and residual pockets ≥ 4 mm were systematically scaled and planed

During the study, two patients dropped out in each group for the following reasons:

1) two patients migrated;

2) one missed the 3-month examination;

3) one missed the final examination

Duzagac et al. 2015 [29]

Oral hygiene instructions,

all kinds of dental treatments, such as fillings and adjustment of overhanging restorations, were completed immediately after patient enrollment,

SRP using a reduced Gracey curette set (Gracey, SAS 5-6, SAS 7-8, SAS 11-12, SAS13- 14, Hu-Friedy) with an ultrasonic device (Dentsply/Cavitron, SPS, 30 K, TFI 1000, Dentsply, York, PA, USA) under local anesthesia,

endpoint of treatment: a smooth tooth surface,

patients received no adjunctive therapy (local or systemic antibiotics, NSAI, laser, ozonotherapy and mouth rinses),

an experienced periodontist (EC) performed all treatment procedures

(SRP, providing oral hygiene instructions and organizing patient recalls)

SRP in 4 sequential visits with 2 or 3 days intervals

completed within 12 days,

each appointment lasted 45 min;

all patients received monthly periodontal maintenance, including oral hygiene reinforcement, scaling and polishing as necessary

8 were excluded for several reasons

did not return for 3 months follow-up,

pregnancy,

weight loss

Eldin et al. 2013 [30]

Oral hygiene instructions,

SRP

n.r.;

periodontal maintenance (re-examination) performed weekly for 3 months after therapy

n.r.

Gonçalves et al. 2015 [31]

Oral hygiene instructions,

Supragingival plaque and calculus removal, exodontia, filling overhang removal and provisional restoration as necessary,

trained periodontist performed SRP with manual curets and ultrasonic device under local anesthesia,

endpoint for each SRP appointment was “smoothness of the scaled roots.”

4 to 6 appointments lasting ≈ 1 h each,

periodontal therapy was completed in 14 days;

periodontal maintenance at 3 and 6 months after

therapy

3 patients from the group without obesity and 6 from the group with obesity did not return for the 3-months follow-up visit and were excluded.

Author & Year

Non-surgical periodontal treatment

Treatment time; periodontal maintenance

Adverse events

Gonçalves et al. 2015 [32]

Oral hygiene instructions regarding brushing technique and

use of dental floss,

supragingival plaque and calculus removal, exodontia, provisional restoration and filling overhang removal, as necessary,

trained periodontist performed SRP using manual curettes (Hu-Friedy, Chicago, IL, USA) and ultrasonic device (Cavitron Select SPC, Dentsply professional, York, PA, USA), under local anaesthesia,

without use of local and/or systemic antimicrobials.

4 to 6 appointments lasting approximately 1 h each, Periodontal therapy completed within 2 weeks;

All patients received periodontal maintenance

every 3 months post-therapy

There were no patient and sampled site dropouts during the course of the study.

Lakkis et al. 2011 [33]

Oral hygiene instructions,

SRP

n.r.;

n.r.

n.r.

Suvan et al. 2014 [34]

Oral hygiene instructions,

full-mouth mechanical periodontal debridement with hand and ultrasonic instruments performed with local anesthesia by the same clinician

Within a 24-h period of time;

n.r.

No individuals in the sample had missing data for any of the covariates listed in this study.

CHX chlorhexidine, min minute, mm millimeter, n.r. not reported, PD pocket depth, SRP scaling and root planing

The quality of the included studies was assessed through the Newcastle-Ottawa Quality Assessment Scale (Table 8).
Table 8

Newcastle – Ottawa Quality Assessment Scale

Stars represent “awards” for each quality item and serve as a quick visual assessment. A maximum of one ‘star’ for each item within the ‘Selection’/‘Exposure’ categories and a maximum of two ‘stars’ for ‘Comparability’ can be awarded

Results

Selection of studies

Initially, 159 studies were identified by electronic search by the two reviewers (FAG, PRS). Full text analysis of the 18 potentially qualified reports led to exclusion of 10 other studies. Additional five titles [2327] were identified by hand search but after full text analysis, all these articles had to be excluded based on the inclusion and exclusion criteria (Table 3). Therefore, eight publications [8, 2834] from the electronic and hand search fulfilled the criteria. However, it was not possible to compare the raw data so that we had to reduce our analysis to a qualitative analysis. This process is summarized in a flow-chart (Fig. 1).
Fig. 1

PRISMA 2009 flow diagram

Summary of studies: characteristics (PICO)

Total number of patients, demographic data, origin of study, outcome measurements 2, 3, 6 and 12 months after therapy and the impact of obesity on the treatment-outcome are summarized in Table 4.

Definition of chronic periodontitis, periodontal assessment and the amount of smokers included are depicted in Table 5.

The definition of obesity and systemic examination were summarized in Table 6. Non-surgical periodontal treatment, treatment time, periodontal maintenance and limitations are shown in Table 7.

Population

Of the eight finally analyzed studies, clinical trials comprised 516 participants. One study [8] enrolled only women. The prevalence of smoking among male patients affected with periodontitis was so high that Al-Zahrani and co-workers [8] were unable to correct for smoking in the male population. Accordingly, only women were included in their study. Overall the studies comprised between 26 up to 260 subjects (Table 4).

The inclusion criteria “age” was defined in all but one study [30]. Three investigations [28, 33, 34] defined the age ≥18 years. The other studies defined a minimum age of 30 years [31, 32] or 35 years [8]. Duzagac et al. defined an age range from 25 to 55 years (Table 4).

Suvan et al. [34] included smokers into their study. Lakkis et al. [33] and Eldin et al.(30] did not mention the smoking status of the patients. All other studies [8, 28, 29, 31, 32] excluded smokers (Table 5).

Patients with diabetes, another important modifier of periodontal health or disease [35] were excluded in seven studies [8, 2832, 34]. Lakkis et al. [33] did not report the presence or absence of diabetes.

Intervention/Comparison

Each paper described the periodontal intervention as a non–surgical therapy. All studies [8, 2834] applied scaling and root planing. Ultrasonic instruments and/or hand instruments were used in all studies (Table 7).

Two papers (8,34] reassessed the PPD 2 months after therapy. Two studies [29, 30] reassessed their patients after 3 months. Another two papers [28, 31] re-evaluated the patients after 3 and 6 months and one study [32] reassessed the PPD three, six and 12 months after therapy. Only Lakkis et al. [33] measured the periodontal pocket depths already 4 to 6 weeks after non-surgical therapy (Table 3). Oral hygiene was instructed additionally to the non–surgical periodontal therapy in all studies (Table 7).

Due to the heterogeneity of the study designs with respect to outcome measures and treatment protocol, as well as variation in study population, sample size, and/or statistical methods, a statistical synthesis of the results of the included studies was not possible. So the authors decided to analyze the papers on a qualitative way [22]. A meta-analysis was not possible.

Outcome

Generally obese patients were found to have deeper periodontal pockets at baseline in all studies.

Three [8, 29, 30] of the eight papers [8, 2834] reported no major negative impact of obesity on response to periodontal therapy in terms of PPD reduction (mm). Al-Zahrani et al. [8] assessed the reduction of PPD (mm) comparing obese with normal–weighted women. There was no statistically significant effect of obesity on treatment outcome. Duzagac et al. [29] assessed the clinical response to non-surgical periodontal treatment, according to the severity of periodontitis based on probing depth < 4 mm vs. ≥ 4 mm. Patients with and without obesity showed similar clinical healing in terms of percentage and number of sites with probing depth < 4 mm and ≥ 4 mm. So they failed to show an effect of obesity on the treatment outcome dependent on the severity of the disease. Eldin et al. [30] also found no effect when comparing an overweight group with an obese group. The difference between the groups in reduction of PPD was not significant (Table 4).

Five [28, 3134] of the eight papers showed a negative effect of obesity on the healing after non-surgical periodontal therapy. Bouaziz et al. [28] revealed that normal-weight patients had a better response to periodontal treatment than obese patients. This effect was specially observed for moderate-to-deep pockets. This fact suggests that the more severe the periodontitis the more pronounced is the negative effect of obesity on periodontal treatment outcome. They showed in the multivariate analysis that obesity was significantly associated with percentage changes of PD > 5 mm and numbers of improving sites (p ≤ 0.05). In the univariate analysis all periodontal parameters improve more in patients suffering from more severe periodontitis at baseline. Other patient characteristics, like age, sex, obesity, and WHR, were not associated with periodontal parameter changes. Gonçalves et al. [31] showed that patients with obesity and chronic periodontitis had a lower PDD reduction than patients without obesity. The measurement of the reduction in PPD (mm) at full-mouth sites showed after 3 months a not statistically significant difference (p = 0.08) between the obese group compared to the group without obesity. However after 6 months there was a statistically significant difference (p = 0.04). At this time point, especially deep sites (PPD ≥ 7 mm) showed a significantly better result in the group without obesity (p = 0.04). Another study of Gonçalves et al. [32] reported that patients with obesity had a significantly greater mean PD (6 months p-value = 0.04, 12 months p value = 0.03) than patients without obesity at six and 12 months post-therapy. The data of a study by Suvan et al. [34] corroborated these findings and showed that obesity was an independent impact value of poorer periodontal treatment outcome 2 months after therapy. The extent of the association between poorer periodontal treatment and obesity was similar to that of smoking (p = 0.02). They worked with 260 patients. This secondary analysis consisted of individuals participating in five clinical studies of non-surgical periodontal therapy over a 7-year period. Lakkis et al. [33] selected 30 patients who were obese; 15 of them had previously undergone bariatric surgery, whereas the other half (n = 15) did not loose any weight and served as a control group. The bariatric surgery group reached a statistically significant greater mean PPD reduction (0.45 mm versus 0.28 mm) compared with the control (no surgery) group (p = 0.007; Table 4).

Limitations

Some patients could not be reviewed or discontinued the study for personal reasons [28, 29, 31]. Weight loss and pregnancy were additional reasons to be excluded in the study of Duzagac et al. [29] (Table 7).

The quality of the included studies was evaluated through the Newcastle-Ottawa Quality Assessment Scale (Table 8).

Discussion

This review focused on obesity and the outcome after non-surgical periodontal therapy and has shown that currently there is no really robust scientific evidence to reach solid conclusions and recommendations.

Three papers [8, 29, 30] were found, which did not find any statistically significant negative impact of obesity on the response to non-surgical periodontal therapy, whereas five papers [28, 3134] showed the opposite, i.e. a clearly negative influence of obesity on the treatment outcomes.

With regard to the quality of evidence, seven included papers [8, 28, 29, 3134] reported some limitations.

Al-Zahrani et al. [8] included only women. Gonçalves and co-workers [31] did not consistently apply the accepted definitions of overweight and obesity, but rather included the waist-to-hip-ratio (WHR) for their definitions, probably leading to inclusion of patients with a BMI inferior to 30 kg/m2 into the obesity group. Thus the results are difficult to interpret and compare with the other studies and are therefore not applicable for patients with a BMI ≥40 kg/m2 [31]. Nonetheless, these studies still show a clearly better tendency with regard to the treatment response for patients without obesity as defined in their study. Lakkis et al. [33] chose another interesting way to find an impact of obesity on the outcome of non-surgical periodontal treatment. They compared obese people who had undergone bariatric surgery (BS) with obese who did not. After weight loss in the BS group, a reduction in total adipocytes might have resulted in a decrease in adipokines and pro-inflammatory mediators released by those adipose cells. This systemic inflammatory reduction might have played a role in reducing the insulin resistance resulting in a better outcome after periodontal therapy as suggested by the authors [33]. Some limitations in the specific profile of the obese patients (nondiabetic, non-smoker) in the paper of Bouaziz et al. (28) may restrict the extrapolation of the results to the whole obese population. Furthermore, the small sample size may also limit the power of this study. Duzagac et al. [29] failed to include a control group of periodontally healthy controls with obesity. Additionally the mean periodontitis parameters were within the limits of “moderate” periodontitis, and the WHR and BMI values of these obese patients were predominantly below those characterizing morbid obesity. So, the results of this study may not be extrapolated to those with severe periodontitis or morbid obesity. The second included study of Gonçalves and co-workers [32] assumes that the high inter-patient variance in adipokine levels may reduce the statistical power to detect treatment effects, as previously reported. The results presented by Suvan et al. [34] may have been influenced by study limitations linked with unequal numbers in BMI categories and sample size. In addition, there may have been limitations with regard to the interpretation associated with the post hoc secondary analysis experimental design, although variation in clinical assessment and treatment was minimized by examiner and treatment clinician stability. This study did not constitute a higher level of evidence in the context of evidence-based health care levels of scientific evidence [34].

Overall, obesity is an obvious, visible stigma so that the studies cannot be considered blinded. This may be another possible bias in each of the studies.

Five studies [8, 28, 29, 31, 32] excluded smokers. Since smoking influences periodontal health these studies are biased [9] and may not be fully representative for the typical overall population. Overall it appears, however, that a positive effect of normal weight is present in non-smokers [28, 31, 32] and in smokers [34].

As mentioned before, the included studies differed in statistical methods, populations, sample sizes, definition of chronic periodontitis, definition of obesity, time of outcome measurement, smoking status, periodontal assessment and non-surgical periodontal therapy. Therefore, it was not only impossible to perform a meta-analysis but also draw clear conclusions.

Nonetheless there is a consensus in the studies that obesity is associated with different baseline PPD levels. The large cohort in the study of Suvan et al. [34] and the long term results of Gonçalves et al. [31, 32] may lead to the conclusion that obesity is an important negative factor which influences non-surgical periodontal therapy.

In summary, all studies [8, 28, 29, 3134] included in this review validated the efficacy of non-surgical periodontal therapy, except the study of Eldin and co-workers [30] who did not report any efficacy of the therapy (Table 3). Clinically, it appears obvious that a therapy is necessary to reach periodontal health independent of the patient’s body mass index.

Because this systematic review provided only moderate evidence that obesity is an important factor for non-surgical periodontal therapy, future prospective cohort studies are needed to confirm these findings [36]. Such trials should be of high methodological quality. They should control important confounding factors such as smoking status, severity of chronic periodontitis, severity of obesity. Every patient should get the same periodontal treatment and periodontal maintenance. Overall, there is a possibility to solve the research question even though blinding of the examiners to obesity or non-obesity status is not practically possible.

Clinicians should know that obesity may have some influence on periodontal status and are likely to have a negative impact on the clinical outcome of conservative treatment, even if this systematic review found only five [28, 3134] out of eight papers [8, 2834] corroborating the influence of obesity on the clinical periodontal outcome focusing on PPD as surrogate parameter for periodontal healing.

Clinicians might consider a weight reduction diet as an additional treatment for periodontal health with a positive effect expected after 6 and 12 months [31, 32]. Also it should not be neglected that weight control has substantial other beneficial health effects which on their own justify such a recommendation.

Conclusion

This systematic review indicates a possible negative relationship between obesity and poorer treatment outcome in obese patients after non-surgical therapy based on the results of five out of eight studies. Three of these studies denied an impact of obesity on the treatment. The potentially inferior healing response could be based on pathophysiological inflammatory models.

Baseline levels showed also a poorer periodontal health in patients with obesity compared with non-obese patients.

No study found any better dental health parameters in obese than in non-obese individuals, and although dental health may not be the most important target for arriving at a near normal body weight, a person who can keep his or her body weight near normal might, in addition to all other established health benefits, count on having better periodontal health than if they are obese.

Declarations

Acknowledgment

The authors would like to thank Mrs. Dr. Martina Gosteli, librarian of the main library of the University of Zurich who performed the electrical literature search.

This study was supported by the Clinic of Preventive Dentistry, Periodontology and Cariology (Center of Dental Medicine) of the University of Zurich.

Authors’ contributions

FAG and PRS conceived the study, participated in its design, did the literature search and drafted the manuscript. PS helped to supervise the methodological correctness of the performed study and the coordination. OAS and JHB provided the required medical theoretical background for this study and participated in the study design. CH helped with the statistical evaluation of the papers and the tables. All authors carefully read and approved the final text.

Competing interest

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Clinic of Preventive Dentistry, Periodontology and Cariology, Center of Dental Medicine, University of Zurich
(2)
Department of Internal Medicine, Cantonal Hospital Baden
(3)
Department of Statistics, Ludwig-Maximilians-University of Munich

References

  1. Saito T, Shimazaki Y, Koga T, Tsuzuki M, Ohshima A. Relationship between upper body obesity and periodontitis. J Dent Res. 2001;80:1631–6.PubMedGoogle Scholar
  2. Pischon N, Heng N, Bernimoulin JP, Kleber BM, Willich SN, Pischon T. Obesity, inflammation, and periodontal disease. J Dent Res. 2007;86:400–9.PubMedGoogle Scholar
  3. Francesco Branca HNuTL. Die Herausforderung Adipositas und Strategien zu ihrer Bekämpfung in der Europäischen Region der WHO. 2007.Google Scholar
  4. Suresh S, Mahendra J. Multifactorial relationship of obesity and periodontal disease. J Clin Diagn Res. 2014;8:ZE01–03.PubMedPubMed CentralGoogle Scholar
  5. Wang Y, Rimm EB, Stampfer MJ, Willett WC, Hu FB. Comparison of abdominal adiposity and overall obesity in predicting risk of type 2 diabetes among men. Am J Clin Nutr. 2005;81:555–63.PubMedGoogle Scholar
  6. Yusuf S, Hawken S, Ounpuu S, Bautista L, Franzosi MG, Commerford P, et al. Obesity and the risk of myocardial infarction in 27,000 participants from 52 countries: a case-control study. Lancet. 2005;366:1640–9.PubMedGoogle Scholar
  7. Słotwińska S. Host response, obesity, and oral health. Cent Eur J Immunol. 2015;40:201–5.PubMedPubMed CentralGoogle Scholar
  8. Al-Zahrani MS, Alghamdi HS. Effect of periodontal treatment on serum C- reactive protein level in obese and normal-weight women affected with chronic periodontitis. Saudi Med J. 2012;33:309–14.PubMedGoogle Scholar
  9. Nishida NTM, Hayashi N, Nagata H, Takeshita T, Nakayama K, et al. Determination of smoking and obesity as periodontitis risks using the classification and regression tree method. J Periodontol. 2005;76:923–8.PubMedGoogle Scholar
  10. Perlstein MI, Bissada NF. Influence of obesity and hypertension on the severity of periodontitis in rats. Oral Surg Oral Med Oral Pathol. 1977;43:707–19.PubMedGoogle Scholar
  11. Koletsky S. Obese Spontaneously Hypertensive Rats-A Model for Study of Atherosclerosis. Exp Mol Pathol. 1973;19:53–60.PubMedGoogle Scholar
  12. Chaffee BW, Weston SJ. Association between chronic periodontal disease and obesity: a systematic review and meta-analysis. J Periodontol. 2010;81:1708–24.PubMedPubMed CentralGoogle Scholar
  13. Wimmer GPB. A critical assessment of adverse pregnancy outcome and periodontal disease. J Clin Periodontol. 2008;35:380–97.PubMedGoogle Scholar
  14. Blaizot A, Vergnes JN, Nuwwareh S, Amar J, Sixou M. Periodontal diseases and cardiovascular events: metaanalysis of observational studies. Int Dent J. 2009;59:197–209.PubMedGoogle Scholar
  15. Tomar SL, Asma S. Smoking-attributable periodontitis in the United States: findings from NHANES III. National Health and Nutrition Examination Survey. 2000;71:743–51.Google Scholar
  16. Tonetti MS. Cigarette smoking and periodontal diseases: etiology and management of disease. Ann Periodontol. 1998;1:88–101.Google Scholar
  17. Arnaud Chiolero DF, Fred P, Jacques C. Consequences of smoking for body weight, body fat distribution, and insulin resistance. Am J Clin Nutr. 2008;87:801–9.PubMedGoogle Scholar
  18. Fei Xu, BEcon, Xiao-Mei Yin BM, Youfa Wang. The association between amount of cigarettes smoked and overweight, central obesity among Chinese adults in Nanjing, China. Asia Pac J Clin Nutr. 2007;16:240-247.Google Scholar
  19. Hou X, Jia W, Bao Y, Lu H, Jiang S, Gu H, Xiang K. Risk factors for overweight and obesity, and changes in body mass index of Chinese adults in Shanghai. BMC Public Health. 2008;8:389.PubMedPubMed CentralGoogle Scholar
  20. Altay U, Gurgan CA, Agbaht K. Changes in inflammatory and metabolic parameters after periodontal treatment in patients with and without obesity. J Periodontol. 2013;84:13–23.PubMedGoogle Scholar
  21. David Moher AL, Tetzlaff J, Altman DG. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. J Clin Epidemiol. 2009;62:1006–12.PubMedGoogle Scholar
  22. Buset SL, Zitzmann NU, Weiger R, Walter C. Non-surgical periodontal therapy supplemented with systemically administered azithromycin: a systematic review of RCTs. Clin Oral Investig. 2015;19(8):1763–75.Google Scholar
  23. D’Aiuto F, Nibali L, Parkar M, Suvan J, Tonetti MS. Short-term effects of intensive periodontal therapy on serum inflammatory markers and cholesterol. J Dent Res. 2005;84:269–73.PubMedGoogle Scholar
  24. Duan JY, O-YX, Zhou YX. Effect of periodontal initial therapy on the serum level of lipid in the patients with both periodontitis and hyperlipidemia. Bejing Da Xue Xue Bao. 2009;41:36-39.Google Scholar
  25. Iwamoto Y, Nishimura F, Soga Y, Takeuchi K, Kurihara M, Takashiba S, et al. Antimicrobial periodontal treatment decreases serum C-reactive protein, tumor necrosis factor-alpha, but not adiponectin levels in patients with chronic periodontitis. J Periodontol. 2003;74:1231–6.PubMedGoogle Scholar
  26. Kardeşler BN, Cetinkalp S, Kinane DF. Adipokines and inflammatory mediators after initial periodontal treatment in patients with type 2 diabetes and chronic periodontitis. J Periodontol. 2010;81:24–33.PubMedGoogle Scholar
  27. Tandon S, Lamba AK, Verma M, Munjal A, Faraz F. Effect of Periodontal Therapy on Serum Lipid Levels. Indian J Med. 2010;1:19–25.Google Scholar
  28. Bouaziz W, Davideau JL, Tenenbaum H, Huck O. Adiposity Measurements and Non-Surgical Periodontal Therapy Outcomes. J Periodontol. 2015;86:1030–7.PubMedGoogle Scholar
  29. Duzagac E, Cifcibasi E, Erdem MG, Karabey V, Kasali K, Badur S, et al. Is obesity associated with healing after non-surgical periodontal therapy? A local vs. systemic evaluation. J Periodontal Res. 2015. [Epub ahead of print]Google Scholar
  30. Eldin AM, Nasr SA, Hassan NE. Effect of non-surgical periodontal therapy on interleukin-8(il-8) level in gingival crevicular fluid in overweight and obese subjects with chronic periodontitis. World J Med Sci. 2013;9:173–9.Google Scholar
  31. Goncalves TE, Feres M, Zimmermann GS, Faveri M, Figueiredo LC, Braga PG, et al. Effects of scaling and root planing on clinical response and serum levels of adipocytokines in patients with obesity and chronic periodontitis. J Periodontol. 2015;86:53–61.PubMedGoogle Scholar
  32. Goncalves TE, Zimmermann GS, Figueiredo LC, Souza Mde C, da Cruz DF, Bastos MF, et al. Local and serum levels of adipokines in patients with obesity after periodontal therapy: one-year follow-up. J Clin Periodontol. 2015;42:431–9.PubMedGoogle Scholar
  33. Lakkis D, Bissada NF, Saber A, Khaitan L, Palomo L, Narendran S, et al. Response to periodontal therapy in patients who had weight loss after bariatric surgery and obese counterparts: a pilot study. J Periodontol. 2012;83:684–9.PubMedGoogle Scholar
  34. Suvan J, Petrie A, Moles DR, Nibali L, Patel K, Darbar U, et al. Body mass index as a predictive factor of periodontal therapy outcomes. J Dent Res. 2014;93:49–54.PubMedPubMed CentralGoogle Scholar
  35. Genco RJ, Ho A, Nishimura F, Murayama Y. A proposed model linking inflammation to obesity, diabetes, and periodontal infections. J Periodontol. 2005;76:2075–84.PubMedGoogle Scholar
  36. Sgolastra F, Severino M, Pietropaoli D, Gatto R, Monaco A. Effectiveness of Periodontal Treatment to Improve Metabolic Control in Patients With Chronic Periodontitis and Type 2 Diabetes: A Meta-Analysis of Randomized Clinical Trials. J Periodontol. 2013;84:958–73.PubMedGoogle Scholar
  37. Europerio 4, Berlin, Germany, 19-21 June 2003. J Clin Periodontol. 2003;30:5-100.Google Scholar
  38. Abstracts for the Royal Australian and New Zealand College of Psychiatrists 40th Congress. Psychiatry in a Changing World, Sydney, Australia, Sunday 22-Thursday 26 May, 2005. Aust N Z J Psychiatry. 2005;39:A97–186.Google Scholar
  39. 5th Joint Meeting of the European Tissue Repair Society and the Wound Healing Society. Wound Repair Regen. 2009;17:A54–87.Google Scholar
  40. Recently published abstracts. Altern Med Rev. 2010;15:369–80.Google Scholar
  41. DENTSPLY. Posters. J Dent Hyg. 2012;86:322–6.Google Scholar
  42. HealthBeat. Dent Assist. 2007;76:59–63. 55p.Google Scholar
  43. Abstracts for Poster Presentations. 2nd North American/ Global Dental Hygiene Research Conference Bethesda, MD, October 20-22, 2011. J Dent Hyg. 2012;86:39–53. 15p.Google Scholar
  44. Abstracts for the International Symposium on Dental Hygiene, Cape Town, South Africa, August 14-17, 2013. Int J Dent Hyg. 2013;11:156–73.Google Scholar
  45. Abou Sulaiman AE, Shehadeh RMH. Assessment of Total Antioxidant Capacity and the Use of Vitamin C in the Treatment of Non-Smokers With Chronic Periodontitis. J Periodontol. 2010;81:1547–54.PubMedGoogle Scholar
  46. Acharya A, Bhavsar N, Jadav B, Parikh H. Cardioprotective effect of periodontal therapy in metabolic syndrome: a pilot study in Indian subjects. Metab. 2010;8:335–41.Google Scholar
  47. Akpinar A, Toker H, Ozdemir H, Bostanci V, Aydin H. The effects of non-surgical periodontal therapy on oxidant and anti-oxidant status in smokers with chronic periodontitis. Arch Oral Biol. 2013;58:717–23.PubMedGoogle Scholar
  48. Armstrong BL, Sensat ML, Stoltenberg JL. Halitosis: a review of current literature. J Dent Hyg. 2010;84:65–74.PubMedGoogle Scholar
  49. Arora N, Avula H, Avula JK. The adjunctive use of systemic antioxidant therapy (lycopene) in nonsurgical treatment of chronic periodontitis: A short-term evaluation. Quintessence Int. 2013;44:399–409.Google Scholar
  50. Basegmez C, Berber L, Yalcin F. Clinical and Biochemical Efficacy of Minocycline in Nonsurgical Periodontal Therapy: A Randomized Controlled Pilot Study. J Clin Pharmacol. 2011;51:915–22.PubMedGoogle Scholar
  51. Bresolin AC, Pronsatti MM, Pasqualotto LN, Nassar PO, Jorge AS, da Silva EAA, et al. Lipid profiles and inflammatory markers after periodontal treatment in children with congenital heart disease and at risk for atherosclerosis. Vasc Health Risk Manage. 2013;9:703–9.Google Scholar
  52. Bresolin AC, Pronsatti MM, Pasqualotto LN, Nassar PO, Jorge AS, Da Silva EAA, et al. Effectiveness of periodontal treatment on the improvement of inflammatory markers in children. Arch Oral Biol. 2014;59:639–44.PubMedGoogle Scholar
  53. Caspersen CJ, Thomas GD, Boseman LA, Beckles GLA, Albright AL. Aging, Diabetes, and the Public Health System in the United States. Am J Public Health. 2012;102:1482–97.PubMedPubMed CentralGoogle Scholar
  54. Caula AL, Lira-Junior R, Tinoco EM, Fischer RG. The effect of periodontal therapy on cardiovascular risk markers: a 6-month randomized clinical trial. J Clin Periodontol. 2014;41:875–82.PubMedGoogle Scholar
  55. Chapple ILC. Oxidative stress, nutrition and neutrogenomics in periodontal health and disease. Int J Dent Hyg. 2006;4:15–21.PubMedGoogle Scholar
  56. Chapple ILC, Brock GR, Milward MR, Ling N, Matthews JB. Compromised GCF total antioxidant capacity in periodontitis: cause or effect? J Clin Periodontol. 2007;34:103–10.PubMedGoogle Scholar
  57. Chandni R, Mammen J, Joseraj MG, Joseph R. Effect of Nonsurgical Periodontal Therapy on Insulin Resistance in Patients with Type 2 Diabetes Mellitus and Chronic Periodontitis. Diabetes. 2015;64:A692.Google Scholar
  58. Chaston R, Sabatini R, Koertge TE, Brooks CN, Schenkein HA. Serum anticardiolipin concentrations in patients with chronic periodontitis following scaling and root planing. J Periodontol. 2014;85:683–7.PubMedGoogle Scholar
  59. Chee HK, Lim LP, Tay F, Thai AC, Sum CF. Non-surgical periodontal treatment and lipid levels in diabetic patients. Ann R Australas Coll Dent Surg. 2008;19:183.PubMedGoogle Scholar
  60. Chee B, Park B, Bartold P. Periodontitis and type II diabetes: a two-way relationship. Int J Evid-Based Healthcare. 2013;11:317–29. 313p.Google Scholar
  61. Chen L, Luo G, Xuan D, Wei B, Liu F, Li J, et al. Effects of non-surgical periodontal treatment on clinical response, serum inflammatory parameters, and metabolic control in patients with type 2 diabetes: a randomized study. J Periodontol. 2012;83:435–43.PubMedGoogle Scholar
  62. D’Aiuto F, Parkar M, Andreou G, Brett PM, Ready D, Tonetti MS. Periodontitis and atherogenesis: causal association or simple coincidence? A pilot intervention study. J Clin Periodontol. 2004;31:402–11.PubMedGoogle Scholar
  63. D’Aiuto F, Ready D, Tonetti MS. Periodontal disease and C-reactive protein-associated cardiovascular risk. J Periodontal Res. 2004;39:236–41.PubMedGoogle Scholar
  64. D’Aiuto F, Parkar M, Nibali L, Suvan J, Lessem J, Tonetti MS. Periodontal infections cause changes in traditional and novel cardiovascular risk factors: results from a randomized controlled clinical trial. Am Heart J. 2006;151:977–84.PubMedGoogle Scholar
  65. Deppe H, Hohlweg-Majert B, Holzle F, Schneider KT, Wagenpfeil S. Pilot study for periodontal treatment and pregnancy outcome: a clinical prospective study. Quintessence Int. 2010;41:e101–110.PubMedGoogle Scholar
  66. Dodington DW, Fritz PC, Sullivan PJ, Ward WE. Higher Intakes of Fruits and Vegetables, beta-Carotene, Vitamin C, alpha-Tocopherol, EPA, and DHA Are Positively Associated with Periodontal Healing after Nonsurgical Periodontal Therapy in Nonsmokers but Not in Smokers. J Nutr. 2015;145:2512–9.PubMedGoogle Scholar
  67. Draper C. Advances in technology and periodontal therapy. J Calif Dent Hyg Assoc. 2010;25:12–4.Google Scholar
  68. Edwards J. Exploring the link between oral health & systemic disease. Access. 2006;20:15–20.Google Scholar
  69. Efurd MG, Bray KK, Mitchell TV, Williams K. Comparing the Risk Identification and Management Behaviors between Oral Health Providers for Patients with Diabetes. J Dent Hyg. 2012;86:130–40.PubMedGoogle Scholar
  70. Elliott-Smith S. Periodontal Disease: A Patient-by-Patient Approach. Access. 2011;25:28–32.Google Scholar
  71. Engebretson SP, Hyman LG, Michalowicz BS. Hemoglobin a1c levels among patients with diabetes receiving nonsurgical periodontal treatment - Reply. JAMA. 2014;311:1921–2.PubMedGoogle Scholar
  72. Fairfield C. Photodisinfection -- innovative adjuntive therapy. J Calif Dent Hyg Assoc. 2010;25:20–2.Google Scholar
  73. Fang F, Wu B, Qu Q, Gao J, Yan W, Huang X, et al. The clinical response and systemic effects of non-surgical periodontal therapy in end-stage renal disease patients: a 6-month randomized controlled clinical trial. J Clin Periodontol. 2015;42:537–46.PubMedGoogle Scholar
  74. Fentoglu O, Sozen T, Oz SG, Kale B, Sonmez Y, Tonguc MO, et al. Short-term effects of periodontal therapy as an adjunct to anti-lipemic treatment. Oral Dis. 2010;16:648–54.PubMedGoogle Scholar
  75. Fine JB. The influence of periodontal inflammation on systemic diseases and medical conditions. Access. 2007;21:14–9.Google Scholar
  76. Fokkema SJ. Peripheral blood monocyte responses in periodontitis. Int J Dent Hyg. 2012;10:229–35.PubMedGoogle Scholar
  77. Fu YW, Li XX, Xu HZ, Gong YQ, Yang Y. Effects of periodontal therapy on serum lipid profile and proinflammatory cytokines in patients with hyperlipidemia: a randomized controlled trial. Clin Oral Investig. 2015;20:1263–9.Google Scholar
  78. Garcia VG, Takano RY, Fernandes LA, de Almeida JM, Theodoro LH. Treatment of experimental periodontal disease by a selective inhibitor of cyclooxygenase-2 with scaling and root planing (SRP). Inflammopharmacology. 2010;18:293–301.PubMedGoogle Scholar
  79. Giblin LJ, Boyd LD, Rainchuso L, Chadbourne D. Short-term effects of non-surgical periodontal therapy on clinical measures of impaired glucose tolerance in people with prediabetes and chronic periodontitis. J Dent Hyg. 2014;88 Suppl 1:23–30.PubMedGoogle Scholar
  80. Gluch JI. Commentary on “The effect of periodontal therapy on TNF-alpha IL-6 and metabolic control in type 2 diabetics”. Access. 2007;21:26–8.Google Scholar
  81. Goldie MP. Perio trends. Dispelling myths about periodontal disease. Access. 2002;16:40.Google Scholar
  82. Goldie MP. C-reactive protein, cardiovascular disease, and periodontal disease. Int J Dent Hyg. 2004;2:139–41.PubMedGoogle Scholar
  83. Goldie MP. What is new in research? Antioxidants in oral health care: making the connection. Int J Dent Hyg. 2005;3:93–5.PubMedGoogle Scholar
  84. Griffin SO, Jones JA, Brunson D, Griffin PM, Bailey WD. Burden of Oral Disease Among Older Adults and Implications for Public Health Priorities. Am J Public Health. 2012;102:411–8.PubMedPubMed CentralGoogle Scholar
  85. Gurenlian JR. Inflammation: the relationship between oral health and systemic disease. Access. 2006;20:1–9. 9p.Google Scholar
  86. Gurenlian JR. Inflammation: the relationship between oral health and systemic disease. Dent Assist. 2009;78:8.PubMedGoogle Scholar
  87. Hammaker BG. Pharmacologic interventions for controlling the inflammatory cascade in periodontal disease. Access. 2010;24:19.Google Scholar
  88. Horwitz J, Hirsh I, Machtei EE. Oral aspects of Gaucher’s disease: a literature review and case report. J Periodontol. 2007;78:783–8.PubMedGoogle Scholar
  89. Hovliaras-Delozier CA. A common voice. Access. 2008;22:22–9.Google Scholar
  90. Ide M, Jagdev D, Coward PY, Crook M, Barclay GR, Wilson RF. The short-term effects of treatment of chronic periodontitis on circulating levels of endotoxin, C-reactive protein, tumor necrosis factor-alpha, and interleukin-6. J Periodontol. 2004;75:420–8.PubMedGoogle Scholar
  91. Ide M. Intensive periodontal treatment including extractions is associated with more immediate systemic inflammation but improved longer-term endothelial function compared to simple scaling. J Evid Based Dent Pract. 2007;7:162–4. 163p.PubMedGoogle Scholar
  92. Jahn C. Diabetes and periodontal health. Dent Assist. 2004;73:24–9.PubMedGoogle Scholar
  93. Jahn C. STANDARDS. Standard 1: Assessment: III. Risk Assessment. Access. 2015;29:19–23. 15p.Google Scholar
  94. Jaiswal GR, Jain VK, Dhodapkar SV, Kumathalli KI, Kumar R, Nemawat A, et al. Impact of bariatric surgery and diet modification on periodontal status: A six month cohort study. J Clin Diagn Res. 2015;9:ZC43–5.PubMedPubMed CentralGoogle Scholar
  95. Janket SJ. Scaling and root-planing (SRP) may improve glycemic control and lipid profile in patients with chronic periodontitis (CP) and type 2 diabetes (DM2) in a specific subgroup: a meta-analysis of randomized clinical trials. J Evid Based Dent Pract. 2014;14:31–3.PubMedGoogle Scholar
  96. Jared H, Boggess KA. Periodontal diseases and adverse pregnancy outcomes: a review of the evidence and implications for clinical practice. J Dent Hyg. 2008;82:24–41.Google Scholar
  97. Jiang H, Xiong X, Su Y, Zhang Y, Wu H, Jiang Z, et al. A randomized controlled trial of pre-conception treatment for periodontal disease to improve periodontal status during pregnancy and birth outcomes. BMC Pregnancy Childbirth. 2013;13:228.PubMedPubMed CentralGoogle Scholar
  98. Kamil W, Al Habashneh R, Khader Y, Al Bayati L, Taani D. Effects of nonsurgical periodontal therapy on C-reactive protein and serum lipids in Jordanian adults with advanced periodontitis. J Periodontal Res. 2011;46:616–21.PubMedGoogle Scholar
  99. Kamilov KP. Relationship between chronic periodontitis clinical manifestation and lipid peroxidation in saliva. Uzbekiston Tibbiet Zhurnali. 1998;0:37–9.Google Scholar
  100. Kapellas K, Do LG, Mark Bartold P, Skilton MR, Maple-Brown LJ, O’Dea K, et al. Effects of full-mouth scaling on the periodontal health of Indigenous Australians: a randomized controlled trial. J Clin Periodontol. 2013;40:1016–24.PubMedGoogle Scholar
  101. Keller A, Rohde JF, Raymond K, Heitmann BL. Association between periodontal disease and overweight and obesity: a systematic review. J Periodontol. 2015;86:766–76.PubMedGoogle Scholar
  102. Kiany F, Hedayati A. Evaluation of serum anti-cardiolipin antibodies after non-surgical periodontal treatment in chronic periodontitis patients.Odontology. 2014;103:203–9.Google Scholar
  103. Kiany F, Hedayati A. Evaluation of serum anti-cardiolipin antibodies after non-surgical periodontal treatment in chronic periodontitis patients. Odontology. 2015;103:203–9.PubMedGoogle Scholar
  104. Kipp A, Majeski J. New trends in perio. Access. 2003;17:10–5.Google Scholar
  105. Kudva P, Tabasum ST, Garg N. Evaluation of clinical and metabolic changes after non surgical periodontal treatment of type 2 diabetes mellitus patients: A clinico biochemical study. J Indian Soc Periodontol. 2010;14:257–62.PubMedPubMed CentralGoogle Scholar
  106. Kumar M, Bandyopadhyay P, Mishra L, Das S, Kundu PK, Mistry S. Effect of periodontal therapy on glycemic control and circulating TNF-α in type 2 diabetic patients. Int J Diabetes Dev Ctries. 2015;35:96–102.Google Scholar
  107. Kurti B, Tüter G, Serdar M, Pinar S, Demirel I, Toyman U. Gingival crevicular fluid prostaglandin E(2) and thiobarbituric acid reactive substance levels in smokers and non-smokers with chronic periodontitis following phase I periodontal therapy and adjunctive use of flurbiprofen. J Periodontol. 2007;78:104–111.Google Scholar
  108. Kurtis B, Tuter G, Serdar M, Pinar S, Demirel I, Toyman U. Gingival crevicular fluid prostaglandin E-2 and thiobarbituric acid reactive substance levels in smokers and non-smokers with chronic periodontitis following phase I periodontal therapy and adjunctive use of flurbiprofen. J Periodontol. 2007;78:104–11.PubMedGoogle Scholar
  109. Lee HJ, Jun JK, Lee SM, Ha JE, Paik DI, Bae KH. Association between obesity and periodontitis in pregnant females. J Periodontol. 2014;85:e224–231.PubMedGoogle Scholar
  110. Li X, Tse HF, Yiu KH, Zhang C, Jin LJ. Periodontal therapy decreases serum levels of adipocyte fatty acid-binding protein in systemically healthy subjects: a pilot clinical trial. J Periodontal Res. 2013;48:308–14.PubMedGoogle Scholar
  111. Ling A, Wang P-W, Lin R-T, Hsieh C-J, Lee P-Y, Zhuang R-Y, et al. Evaluation of Periodontal Status and Effectiveness of Non-Surgical Treatment in Patients With Type 2 Diabetes Mellitus in Taiwan for a 1-Year Period. J Periodontol. 2012;83:621–8.Google Scholar
  112. Lo JC, O’Ryan F, Yang J, Hararah MK, Gonzalez JR, Gordon N, et al. Oral Health Considerations in Older Women Receiving Oral Bisphosphonate Therapy. J Am Geriatr Soc. 2011;59:916–22. 917p.PubMedGoogle Scholar
  113. Malhotra R, Kapoor A, Grover V, Grover D, Kaur A. Effect of Scaling and Root Planing on Erythrocyte Count, Hemoglobin and Hematocrit in Patients with Chronic Periodontal Disease. J Dent Hyg. 2012;86:195–203.PubMedGoogle Scholar
  114. Mancl KA, Kirsner RS, Ajdic D. Wound biofilms: Lessons learned from oral biofilms. Wound Repair Regen. 2013;21:352–62.PubMedPubMed CentralGoogle Scholar
  115. Martinez GL, Koury JC, Brito F, Fischer RG, Gustafsson A, Figueredo CM. The impact of non-surgical periodontal treatment on serum levels of long chain-polyunsaturated fatty acids: a pilot randomized clinical trial. J Periodontal Res. 2014;49:268–74.PubMedGoogle Scholar
  116. Martinez GL, Koury JC, Martins MA, Nogueira F, Fischer RG, Gustafsson A, et al. Serum level changes of long chain-polyunsaturated fatty acids in patients undergoing periodontal therapy combined with one year of omega-3 supplementation: a pilot randomized clinical trial. J Periodontal Implant Sci. 2014;44:169–77.PubMedPubMed CentralGoogle Scholar
  117. Matlock J, Ferguson K, Calef J, Abbott S. Obesity and Bariatric Surgery: Effects on the Oral Cavity. Access. 2012;26:8–11.Google Scholar
  118. McDaniel JC, Roy S, Wilgus TA. Neutrophil activity in chronic venous leg ulcers-A target for therapy? Wound Repair Regen. 2013;21:339–51. 313p.PubMedPubMed CentralGoogle Scholar
  119. Meharwade VV, Gayathri GV, Mehta DS. Effects of scaling and root planing with or without a local drug delivery system on the gingival crevicular fluid leptin level in chronic periodontitis patients: a clinico-biochemical study. J Periodontal Implant Sci. 2014;44:118–25.PubMedPubMed CentralGoogle Scholar
  120. Merchant AT. Hemoglobin A1c levels among patients with diabetes receiving nonsurgical periodontal treatment [1]. JAMA. 2014;311:1919.PubMedGoogle Scholar
  121. Michalowicz BS, Hyman L, Wei H, Oates Jr TW, Reddy M, Paquette DW, et al. Factors associated with the clinical response to nonsurgical periodontal therapy in people with type 2 diabetes mellitus. JADA. 2014;145:1227–39. 1213p.PubMedGoogle Scholar
  122. Mizrak T, Guncu GN, Caglayan F, Balci TA, Aktar GS, Ipek F. Effect of a controlled-release chlorhexidine chip on clinical and microbiological parameters and prostaglandin E-2 levels in gingival crevicular fluid. J Periodontol. 2006;77:437–43.PubMedGoogle Scholar
  123. Moeintaghavi A, Arab HR, Bozorgnia Y, Kianoush K, Alizadeh M. Non-surgical periodontal therapy affects metabolic control in diabetics: a randomized controlled clinical trial. Aust Dent J. 2012;57:31–37.Google Scholar
  124. Moravec LJ, Boyd LD. Bariatric Surgery and Implications for Oral Health: A Case Report. J Dent Hyg. 2011;85:166–76.PubMedGoogle Scholar
  125. Muthu J, Muthanandam S, Mahendra J, Namasivayam A, John L, Logaranjini A. Effect of Nonsurgical Periodontal Therapy on the Glycaemic Control of Nondiabetic Periodontitis Patients: A Clinical Biochemical Study. Oral Health Prev Dent. 2015;13:261–6.PubMedGoogle Scholar
  126. Nassar PO, Walker CS, Salvador CS, Felipetti FA, Orrico SRP, Nassar CA. Lipid profile of people with Diabetes mellitus type 2 and periodontal disease. Diabetes Res Clin Pract. 2012;96:35–9.PubMedGoogle Scholar
  127. Newton KM, Chaudhari M, Barlow WE, Inge RE, Theis MK, Spangler LA, et al. A population-based study of periodontal care among those with and without diabetes. J Periodontol. 2011;82:1650–6.PubMedGoogle Scholar
  128. Nichols FC, Levinbook H, Shnaydman M, Goldschmidt J. Prostaglandin E2 secretion from gingival fibroblasts treated with interleukin-1beta: effects of lipid extracts from Porphyromonas gingivalis or calculus. J Periodontal Res. 2001;36:142–52.PubMedGoogle Scholar
  129. Nielsen D, Walser C, Kodan G, Chaney RD, Yonkers T, VerSteeg JD, et al. Effects of treatment with clindamycin hydrochloride on progression of canine periodontal disease after ultrasonic scaling. Vet Ther. 2000;1:150–8.PubMedGoogle Scholar
  130. Novakovic N, Cakic S, Todorovic T, Raicevic BA, Dozic I, Petrovic V, et al. Antioxidative Status of Saliva before and after Non-Surgical Periodontal Treatment. Srp Ark Celok Lek. 2013;141:163–8.Google Scholar
  131. Novakovic N, Todorovic T, Rakic M, Milinkovic I, Dozic I, Jankovic S, et al. Salivary antioxidants as periodontal biomarkers in evaluation of tissue status and treatment outcome. J Periodontal Res. 2014;49:129–36.PubMedGoogle Scholar
  132. Oliveira AM, de Oliveira PA, Cota LO, Magalhaes CS, Moreira AN, Costa FO. Periodontal therapy and risk for adverse pregnancy outcomes. Clin Oral Investig. 2011;15:609–15.PubMedGoogle Scholar
  133. Olsen NC. Health Access. 2006;20:56–7. 52p.Google Scholar
  134. Paquette DW, Ryan ME, Wilder RS. Locally delivered antimicrobials: clinical evidence and relevance. J Dent Hyg. 2008;82:10–5.PubMedGoogle Scholar
  135. Perayil J, Suresh N, Fenol A, Vyloppillil R, Bhaskar A, Menon S. Comparison of Hba1c Levels in Non-Diabetic Healthy Subjects and Subjects With Periodontitis Before and After Non-Surgical Periodontal Therapy. J Periodontol. 2014:85:1658–66.Google Scholar
  136. Perayil J, Suresh N, Fenol A, Vyloppillil R, Bhaskar A, Menon S. Comparison of glycated hemoglobin levels in individuals without diabetes and with and without periodontitis before and after non-surgical periodontal therapy. J Periodontol. 2014;85:1658–66.PubMedGoogle Scholar
  137. Phillips A. Oral complications of diabetes: an under-recognized condition. Pract Nurs. 2013;24:562–6.Google Scholar
  138. Pradeep AR, Manjunath SG, Swati PP, Shikha C, Sujatha PB. Gingival crevicular fluid levels of leukotriene B4 in periodontal health and disease. J Periodontol. 2007;78:2325–30.PubMedGoogle Scholar
  139. Price T. Periodontal disease and adverse pregnancy outcomes: treatment recommendations for the pregnant woman. Access. 2010;24:20–3.Google Scholar
  140. Qiqiang L, Huanxin M, Xuejun G. Longitudinal study of volatile fatty acids in the gingival crevicular fluid of patients with periodontitis before and after nonsurgical therapy. J Periodontal Res. 2012;47:740–9.PubMedGoogle Scholar
  141. Radafshar G, Torabi F, Mirfarhadi N. Short-term effects of intensive non-surgical periodontal therapy and low-dose doxycycline on serum levels of IL-6, TNF-alpha and lipid profile in advanced periodontitis. Afr J Microbiol Res. 2012;6:355–60.Google Scholar
  142. Radnai M, Pal A, Novak T, Urban E, Eller J, Gorzo I. Benefits of periodontal therapy when preterm birth threatens. J Dent Res. 2009;88:280–4.PubMedGoogle Scholar
  143. Raghavendra NM, Pradeep AR, Kathariya R, Sharma A, Rao NS, Naik SB. Effect of non surgical periodontal therapy on gingival crevicular fluid and serum visfatin concentration in periodontal health and disease. Dis Markers. 2012;32:383–8.PubMedPubMed CentralGoogle Scholar
  144. Ramirez JH, Arce RM, Contreras A. Periodontal treatment effects on endothelial function and cardiovascular disease biomarkers in subjects with chronic periodontitis: protocol for a randomized clinical trial. Trials. 2011;12:46.PubMedPubMed CentralGoogle Scholar
  145. Rasch MS, Mealey BL, Prihoda TJ, Woodard DS, McManus LM. The effect of initial periodontal therapy on salivary platelet-activating factor levels in chronic adult periodontitis. J Periodontol. 1995;66:613–23.PubMedGoogle Scholar
  146. Sadatmansouri S, Sedighpoor N, Aghaloo M. Effects of periodontal treatment phase I on birth term and birth weight. J Indian Soc Pedod Prev Dent. 2006;24:23–6.PubMedGoogle Scholar
  147. Saffi MA, Furtado MV, Montenegro MM, Ribeiro IW, Kampits C, Rabelo-Silva ER, et al. The effect of periodontal therapy on C-reactive protein, endothelial function, lipids and proinflammatory biomarkers in patients with stable coronary artery disease: study protocol for a randomized controlled trial. Trials. 2013;14:283.PubMedPubMed CentralGoogle Scholar
  148. Williams KB. Effect of treating periodontal disease on cardiovascular markers. J Dent Hyg. 2007;81:49.Google Scholar
  149. Sembene M, Moreau JC, Mbaye MM, Diallo A, Diallo PD, Ngom M, et al. Periodontal infection in pregnant women and low birth weight babies. Odontostomatol Trop. 2000;23:19–22.Google Scholar
  150. Sengupta S, Fine J, Wu-Wang CY, Gordon J, Murty VLN, Slomiany A, et al. The relationship of prostaglandins to cAMP, IgG, IgM and alpha-2- macroglobulin in gingival crevicular fluid in chronic adult periodontitis. Arch Oral Biol. 1990;35:593–6.PubMedGoogle Scholar
  151. Shimada Y, Komatsu Y, Ikezawa-Suzuki I, Tai H, Sugita N, Yoshie H. The effect of periodontal treatment on serum leptin, interleukin-6, and C-reactive protein. J Periodontol. 2010;81:1118–23.PubMedGoogle Scholar
  152. Shimoe M, Yamamoto T, Iwamoto Y, Shiomi N, Maeda H, Nishimura F, et al. Chronic periodontitis with multiple risk factor syndrome: a case report. [Erratum appears in J Int Acad Periodontol. 2011 Oct;13(3):93]. J Int Acad Periodontol. 2011;13:40–7.PubMedGoogle Scholar
  153. Singh N, Narula SC, Sharma RK, Tewari S, Sehgal PK. Vitamin E Supplementation, Superoxide Dismutase Status, and Outcome of Scaling and Root Planing in Patients With Chronic Periodontitis: A Randomized Clinical Trial. J Periodontol. 2014;85:242–9.PubMedGoogle Scholar
  154. Siqueira MAD, Fischer RG, Pereira NR, Martins MA, Moss MB, Mendes-Ribeiro AC, et al. Effects of non-surgical periodontal treatment on the L-arginine-nitric oxide pathway and oxidative status in platelets. Exp Biol Med. 2013;238:713–22.Google Scholar
  155. Stewart JE, Wager KA, Friedlander AH, Zadeh HH. The effect of periodontal treatment on glycemic control in patients with type 2 diabetes mellitus. J Clin Periodontol. 2001;28:306–10.PubMedGoogle Scholar
  156. Talbert J, Elter J, Jared HL, Offenbacher S, Southerland J, Wilder RS. The effect of periodontal therapy on TNF-alpha, IL-6 and metabolic control in type 2 diabetics. J Dent Hyg. 2006;80:7–7.PubMedGoogle Scholar
  157. Tamaki N, Tomofuji T, Ekuni D, Yamanaka R, Yamamoto T, Morita M. Short-Term Effects of Non-Surgical Periodontal Treatment on Plasma Level of Reactive Oxygen Metabolites in Patients With Chronic Periodontitis. J Periodontol. 2009;80:901–6.PubMedGoogle Scholar
  158. Tamaki N, Tomofuji T, Ekuni D, Yamanaka R, Morita M. Periodontal treatment decreases plasma oxidized LDL level and oxidative stress. Clin Oral Investig. 2011;15:953–8.PubMedGoogle Scholar
  159. Tawfig A. Effects of non-surgical periodontal therapy on serum lipids and C-reactive protein among hyperlipidemic patients with chronic periodontitis. J Int Soc Prev Community Dent. 2015;5:S49–56.PubMedPubMed CentralGoogle Scholar
  160. Teles FR, Teles RP, Martin L, Socransky SS, Haffajee AD. Relationships among interleukin-6, tumor necrosis factor-alpha, adipokines, vitamin D, and chronic periodontitis. J Periodontol. 2012;83:1183–91.PubMedGoogle Scholar
  161. Toker H, Akpinar A, Aydin H, Poyraz O. Influence of smoking on interleukin-1beta level, oxidant status and antioxidant status in gingival crevicular fluid from chronic periodontitis patients before and after periodontal treatment. J Periodontal Res. 2012;47:572–7.PubMedGoogle Scholar
  162. Tuter G, Kurtis B, Serdar M, Aykan T, Okyay K, Yucel A, et al. Effects of scaling and root planing and sub-antimicrobial dose doxycycline on oral and systemic biomarkers of disease in patients with both chronic periodontitis and coronary artery disease. J Clin Periodontol. 2007;34:673–81.PubMedGoogle Scholar
  163. Vardar S, Baylas H, Huseyinov A. Effects of selective cyclooxygenase-2 inhibition on gingival tissue levels of prostaglandin E2 and prostaglandin F2alpha and clinical parameters of chronic periodontitis. J Periodontol. 2003;74:57–63.PubMedGoogle Scholar
  164. Van Dyke TE, Hasturk H, Kantarci A, Freire MO, Nguyen D, Dalli J, et al. Proresolving nanomedicines activate bone regeneration in periodontitis. J Dent Res. 2015;94:148–56.PubMedPubMed CentralGoogle Scholar
  165. Vyas SP, Sihorkar V, Mishra V. Controlled and targeted drug delivery strategies towards intraperiodontal pocket diseases. J Clin Pharm Ther. 2000;25:21–42.PubMedGoogle Scholar
  166. Wahid A, Chaudhry S, Ehsan A, Butt S, Khan AA. Bidirectional relationship between chronic kidney disease & periodontal disease. Pak J Med Sci. 2013;29:211–5.PubMedPubMed CentralGoogle Scholar
  167. Wang XE, Xu L, Meng HX, Lü D, Chen ZB, Lu RF. Long-term clinical and hematologic effects of non-surgical treatment on aggressive periodontitis. Zhonghua Kou Qiang Yi Xue Za Zhi. 2013;48:467–71.PubMedGoogle Scholar
  168. Wehmeyer MM, Kshirsagar AV, Barros SP, Beck JD, Moss KL, Preisser JS, et al. A randomized controlled trial of intensive periodontal therapy on metabolic and inflammatory markers in patients With ESRD: results of an exploratory study. Am J Kidney Dis. 2013;61:450–8.PubMedGoogle Scholar
  169. Wei D, Zhang XL, Wang YZ, Yang CX, Chen G. Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Aust Dent J. 2010;55:70–8.PubMedGoogle Scholar
  170. Williams KB. Periodontal disease and type 2 diabetes. J Dent Hyg. 2009;83:8–44.Google Scholar
  171. Williams KB, Bray KK. Increasing patient engagement in care: motivational i nterviewing. Access. 2009;23:36–9.Google Scholar
  172. Wood N. Oral health -- how to reduce risks of periodontitis. Posit Health. 2006:30-35.Google Scholar
  173. Wu Y, Chen L, Wei B, Luo K, Yan FH. Effect of Non-Surgical Periodontal Treatment on Visfatin Concentrations in Serum and Gingival Crevicular Fluid of Patients With Chronic Periodontitis and Type 2 Diabetes Mellitus. J Periodontol. 2015;86:795–800.PubMedGoogle Scholar
  174. Zare Javid A, Seal CJ, Heasman P, Moynihan PJ. Impact of a customised dietary intervention on antioxidant status, dietary intakes and periodontal indices in patients with adult periodontitis. J Hum Nutr Diet. 2014;27:523–32. 510p.PubMedGoogle Scholar
  175. Zhou SY, Duan XQ, Hu R, Ouyang XY. Effect of non-surgical periodontal therapy on serum levels of TNF-a, IL-6 and C-reactive protein in periodontitis subjects with stable coronary heart disease. Chin J Dent Res. 2013;16:145–51.PubMedGoogle Scholar
  176. Zuza EP, Barroso EM, Carrareto AL, Pires JR, Carlos IZ, Theodoro LH, et al. The role of obesity as a modifying factor in patients undergoing non-surgical periodontal therapy. J Periodontol. 2011;82:676–82.PubMedGoogle Scholar
  177. Armitage GC. Periodontal diagnoses and classification of periodontal diseases. Periodontology 2000. 2004;34:9–21.PubMedGoogle Scholar
  178. Silness J, Löe H. Periodontal Disease in Pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand. 1964;22:121–35.PubMedGoogle Scholar
  179. Löe HSJ. Periodontal disease in pregnancy. I. Prevalance and severity. Acta Odontol Scand. 1963;21:533–51.PubMedGoogle Scholar

Copyright

© The Author(s). 2016

Advertisement