Systemic benefits of periodontal therapy in patients with obesity and periodontitis: a systematic review

MENEZES, Cláudia Callegaro de; BARBIRATO, Davi da Silva; FOGACCI, Mariana Fampa; MARAÑÓN-VÁSQUEZ, Guido Artemio; CARNEIRO, João Régis Ivar; MAIA, Lucianne Copple; BARROS, Maria Cynésia Medeiros de

doi:10.1590/1807-3107bor-2024.vol38.0031

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Systematic Review And Meta-analysis/Periodontics • Braz. oral. res. 38 • 2024 • https://doi.org/10.1590/1807-3107bor-2024.vol38.0031 copy

Systemic benefits of periodontal therapy in patients with obesity and periodontitis: a systematic review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

This systematic review aimed to answer the focused question: “What are the benefits of subgingival periodontal therapy on blood hematological and biochemical index, biomarkers of inflammation and oxidative stress, quality of life, and periodontal pathogen counts in patients with obesity and periodontitis?”. A systematic literature search was performed in six databases: PubMed, Embase, LILACS, Web of Science, Cochrane and SCOPUS and other sources, and a manual search was conducted as well. Inclusion criteria were randomized and non-randomized clinical trials, and before-and-after studies on patients with obesity subjected to periodontal therapy. The results were synthesized qualitatively. Risk of bias within studies was assessed using RoB 2 and ROBINS-I tools. The certainty of evidence was evaluated following the GRADE approach. Three randomized controlled trials and 15 before-and-after studies were included. Randomized controlled trials were considered to have a low risk of bias, as compared to before-and-after studies assessed as having low, serious, and critical risks of bias. Non-surgical periodontal therapy plus azithromycin, chlorhexidine, and cetylpyridinium chloride reduced blood pressure and decreased serum levels of HbA1c, hsCRP, IL-1β, and TNF-α. Salivary resistin level also decreased in patients with obesity and periodontitis after therapy and chlorhexidine mouth rinse. Before-and-after data suggest an improvement in total cholesterol, LDL, triglycerides, insulin resistance, C3, GCF levels of TNF-α, chemerin, vaspin, omentin-1, visfatin, 8-OHdG, and periodontal pathogen counts after therapy.

Keywords
Periodontal diseases; Periodontitis; Obesity; Dental scaling; Root planing

Author, year	Country/Study design	Elegibility criteria	Participants	Diagnostic criteria		Intervention	Control group	Periodontal maintenance phase \| Follow-up
Author, year	Country/Study design	Elegibility criteria	Participants	Obesity	Periodontitis	Intervention	Control group	Periodontal maintenance phase \| Follow-up
Al-Zahrani and AlGhamdi, 2012¹¹	Kingdon of Saudi Arabia/BAS	IC: female, ≥ 35 years old, generalized moderate/severe chronic periodontitis and at least 20 remaining teeth	n = 20	BMI ≥ 30 kg/m²	≥ 30 % of the sites with CAL ≥ 3 mm	NSPT and OHI	Before NSPT	NA
Al-Zahrani and AlGhamdi, 2012¹¹	Kingdon of Saudi Arabia/BAS	EC: systemic diseases or infection, periodontal therapy in the previous 12 months, systemic antibiotic in the previous 3 months, pregnancy or lactation, smokers, antibiotic prophylaxis before periodontal treatment	Mean age: 44. ± 8.4 years	BMI ≥ 30 kg/m²	≥ 30 % of the sites with CAL ≥ 3 mm	NSPT and OHI	Before NSPT	2-months follow-up
Altay et al., 2013³⁷	Turkey/BAS	IC: > 25 years old, and ≥ 15 natural remaining teeth	n = 22	BMI ≥ 30 kg/m²	≥ 5 teeth with ≥ 1 sites with PD ≥ 5 mm and CAL ≥ 2 mm	FMD	Before NSPT	0.12 % chlorhexidine mouth rinse, b.i.d., for 14 days after NSPT
		EC: antibiotic therapy within the previous 6 months and anti-inflammatory drugs within the previous 3 months, pregnancy or use of contraceptives or any other hormone therapy, periodontal treatment within the previous 24 months, and any systemic problem or treatment during the evaluation period of 3 months before and after periodontal treatment	Males: 5 (22.7 %) Females: 17 (77.3 %)	WC > 102 cm (males) and > 88 cm (females)				Plaque control and OHR at days 1, 7, 14, and 30
			Mean age: 45.6 ± 23.8 years; and Age range: 35–68 years					3-months follow-up
Gonçalves et al., 2015a³⁸	Brazil / BAS	IC: > 30 years old, and ≥ 15 remaining teeth excluding third molars and teeth with advanced decay indicated for exodontia, generalized chronic periodontitis, HbA1c < 6.5 %, FPG 70-99 mg/dL, and CRP < 6 mg/L	n = 18	BMI ≥ 30 and < 40 kg/m²	> 30 % of the sites with PD and CAL ≥ 4 mm or ≥ 6 teeth with ≥ 1 site with PD and CAL ≥ 5 mm and BOP	NSPT	Before NSPT	Professional plaque control, OHR and SRP of deep sites presenting BOP 3- and 6-months post-therapy
		EC: pregnancy, lactation, current smoking and smoking within the past 10 years, prophylactic antibiotic coverage before dental treatment, subgingival periodontal therapy in the previous 12 months, antimicrobial, anti-inflammatory, immunosuppressive, and lipid-lowering therapies in the previous 6 months, regular use of mouth rinses containing antimicrobials, orthodontic appliances, and presence of systemic conditions that could affect the progression of periodontitis and/or gain/loss of weight	Males: 72.2 % Females: 27.8 %	WHR ≥ 0.9 (males) and ≥ 0.85 (females)				6-months follow-up
			Mean age: 48.8 ± 5.9 years
Gonçalves et al., 2015b³⁹	Brazil / BAS	IC: > 30 years old, and ≥ 15 remaining teeth excluding third molars and teeth with advanced decay indicated for exodontia, generalized chronic periodontitis, HbA1c < 6.5 %, FPG 70-99 mg/dL, and CRP < 6 mg/L	n = 20	BMI ≥ 30 and < 40 kg/m²	> 30 % of the sites with PD and CAL ≥ 4 mm or ≥ 6 teeth with ≥ 1 site with PD and CAL ≥ 5 mm and BOP	NSPT	Before NSPT	Periodontal maintenance (non-specified) every 3 months post-therapy
		EC: pregnancy, lactation, current smoking and smoking within the past 10 years, prophylactic antibiotic coverage before dental treatment, subgingival periodontal therapy in the previous 12 months, antimicrobial, anti-inflammatory, immunosuppressive, and lipid-lowering therapies in the previous 6 months, regular use of mouth rinses containing antimicrobials, orthodontic appliances, and presence of systemic conditions that could affect the progression of periodontitis and/or gain/loss of weight	Males: 11 (55 %)	WHR ≥ 0.9 (males) and ≥ 0.85 (females)				12-months follow-up
			Females: 9 (45 %)
			Mean age: 50 ± 4.5 years
Balli et al., 2016a	Turkey /BAS	IC: 30–49 years old, > 20 remaining teeth HbA1c < 6.5 %, and FPG < 100 mg/dL	n = 20	BMI ≥ 30 and < 40 kg/m²	PD and CAL ≥ 5mm with bone loss affecting > 30 % of existing teeth on clinical/radiographic examination	NSPT	Before NSPT	NA
		EC: aggressive periodontitis, periapical pathologies, exposure to mechanical force as a result of occlusion/orthodontics, systemic diseases such as cancer, HIV, diabetes mellitus or additional diseases which may interfere with adipokines levels and the periodontal conditions high-grade steroid therapies, radiation/immuno-suppressive therapies, pregnancy, lactation, smoking over the past five years, allergic reaction to any kind of drug, no history of either periodontal or drug therapies within the preceding six months, namely anti-inflammatory treatments, and antibiotic courses or other pharmacological treatments	Males: 9 (45 %)	WHR ≥ 0.9 (males) and ≥ 0.85 (females)				6-weeks follow-up
			Females: 11 (55 %)
			Mean age: 40.56 ± 4.11 years
Balli et al., 2016a	Turkey /BAS	IC: 30–49 years old, > 20 remaining teeth HbA1c < 6.5 %, and FPG < 100 mg/dL	n = 20	BMI ≥ 30 and < 40 kg/m²	PD and CAL ≥ 5mm with bone loss affecting > 30 % of existing teeth on clinical/radiographic examination	NSPT	Before NSPT	NA
		EC: aggressive periodontitis, periapical pathologies, exposure to mechanical force as a result of occlusion/orthodontics, systemic diseases such as cancer, HIV, diabetes mellitus or additional diseases which may interfere with adipokines levels and the periodontal conditions high-grade steroid therapies, radiation/immuno-suppressive therapies, pregnancy, lactation, smoking over the past five years, allergic reaction to any kind of drug, no history of either periodontal or drug therapies within the preceding six months, namely anti-inflammatory treatments, and antibiotic courses or other pharmacological treatments	Males: 9 (45 %)	WHR ≥ 0.9 (males) and ≥ 0.85 (females)				6-weeks follow-up
			Females: 11 (55 %)
			Age: 42 (36–46) years
Öngöz Dede et al., 2016b⁴²	Turkey /BAS	IC: ≥ 20 remaining teeth excluding third molars, non-smokers who had never smoked, no history of systemic disease, had not undergone periodontal therapy or taken medicine for at least 6 months before the study, no pregnancy or lactation, and no alcohol or antioxidant vitamin consumption	n = 15	BMI ≥ 30 kg/m²	PD and CAL ≥ 5mm with bone loss affecting > 30 % of existing teeth on clinical/radiographic examination	Intensive hygiene phase and full-mouth NSPT, and the maintenance and monitoring of oral hygiene	Before NSPT	Periodontal maintenance and monitoring of oral hygiene (non-specified)
			Males: 8 (53.3 %)					4-weeks follow-up
			Females: 7 (46.7 %)
			Mean age: 47.13 ± 7.17 years; and Age range: 34–60 years
Taşdemir et al., 2016⁴³	Turkey /BAS	IC: > 25 years old, chronic periodontitis, obesity, ≥ 15 remaining teeth, and type 2 diabetes mellitus (in diabetes group)	n = 14	BMI ≥ 30 kg/m²	≥ 5 teeth with ≥ 1 sites with PD ≥ 5 mm and CAL ≥ 2 mm	Intensive full-mouth NSPT	Before FMT	NA
		EC: antibiotic or anti-inflammatory drug use within the previous 6 months, pregnancy or lactation, periodontal therapy within the previous 6 months, smoking or history of smoking, alcohol consumption, and lipid lowering medications	Males: 9 (64.3 %) Females: 5 (35.7 %)	WC > 102 cm (males) and > 88 cm (females)				6-months follow-up
			Mean age: 49.2 ± 9.2; and Age range: 30–62 years
Zuza et al., 2016⁴⁴	Brazil / BAS	IC: 35–55 years old, both sexes, chronic periodontitis, and ≥ 20 remaining teeth	n = 28	BMI ≥ 30 and < 40 kg/m²	≥ 6 teeth with PD ≥5 mm and CAL ≥ 3 mm and BOP	NSPT and OHI and motivation	Before NSPT	3-months follow-up
		EC: smokers or former smokers, antibiotics or anti-inflammatory in prior 3 months, diabetes, or other systemic diseases, pregnant or lactating women, use of hormones, mental or physical limitations, and periodontal therapy in the previous 12 months	Males: 6 (21.4 %)	WHR ≥ 0.9 (males) and ≥ 0.85 (females)
			Females: 22 (78.6 %)	WC >102 cm (male) and >88 cm (female)
			Mean age: 45.7 ± 8.4 years	% of body fat ≥25% (male) ≥35% (female)
^{Akram et al., 2017}69. Akram Z, Baharuddin NA, Vaithilingam RD, et al. Effect of nonsurgical periodontal treatment on clinical periodontal variables and salivary resistin levels in obese Asians. J Oral Sci. 2017; 59(1): 93-102. doi: 10.2334/josnusd.16-0127. https://doi.org/10.2334/josnusd.16-0127... ⁶⁷	Malaysia/RCT	IC: 30–66 years old, chronic periodontitis, and ≥ 12 remaining teeth excluding third molars	n = 62	BMI ≥ 27.5 kg/m²	≥ 2 interproximal sites with PD ≥ 5 mm (different teeth) or ≥ 2 interproximal sites with CAL ≥ 4 mm (different teeth)	NSPT, OHI and 0.12 % chlorhexidine mouth rinse	No periodontal therapy or oral hygiene instruction	Professional prophylaxis, re-motivation and OHR
		EC: pregnant or lactating mothers medical condition requiring prophylactic antibiotic administration before dental treatment, periodontal treatment during the previous 6 months, intellectual disability that might interfere with oral hygiene procedures, not Malaysian, presence of systemic conditions that could affect progression of periodontitis, or weight gain/loss or other inflammatory conditions	CG = 31 and IG = 31	WHR ≥ 0.9 (males) and ≥ 0.85 (females)				6-weeks and 3-months follow-up
			Males: 17 (27.4 %); CG = 9 (32.3 %) and IG = 8 (25.8 %)
			Females: 45 (72.6 %); CG = 22 (67.7 %) and IG = 23 (74.2 %)
			Mean age: CG = 44.84 ± 9.02 years and IG = 44.68 ± 10.63 years
Basher et al., 2017³⁵	Malaysia/RCT	IC: malaysians, ≥ 30 years old, chronic periodontitis, obesity, and ≥ 12 remaining teeth	n = 62	BMI ≥ 27.5 kg/m²	≥ 2 interproximal sites with PD ≥ 4 mm and ≥ 2 interproximal sites with CAL ≥ 3 mm (different teeth) or one site with PD ≥ 5 mm	NSPT, OHI and 0.12 % chlorhexidine mouth rinse	No periodontal therapy or oral hygiene instruction	Professional prophylaxis, re-motivation and OHR
		EC: periodontal treatment within the past 6 months, antibiotic treatment within the past 4 months, require prophylactic antibiotic coverage, use of systemic or topical NSAIDs for the past 4 months, pregnant or intend to and lactating mothers, mentally handicapped, rheumatic heart disease, and valve replacement	CG = 31 and IG = 31					3-months follow-up
			Males: 18 (29 %); CG = 10 (32.25 %) and IG = 8 (25.8 %)
			Females: 44 (71 %); CG = 21 (67.75 %) and IG = 23 (74.20 %)
			Mean age: CG = 44.85 ± 9.02 years and IG = 45.03 ± 10.72 years
Martínez-Herrera et al., 2018a⁴⁶	Spain/BAS	EC: aggressive periodontitis, < 14 remaining teeth, infectious or other inflammatory diseases, periodontal therapy in the last 6 months or antibiotics in the last 3 months, treatment with systemic anti-inflammatory drugs, pregnancy or lactation, secondary obesity, antibiotic treatment before the dental intervention, and diabetes mellitus	At baseline, n = 96	BMI ≥ 30 kg/m²	≥ 4 teeth with ≥1 sites with PD ≥ 4 mm and CAL ≥ 3 mm	Intensive full-mouth NSPT, OHI and 0.12 % chlorhexidine mouth rinse	Before NSPT	Periodontal examinations at 3 months post-therapy
			Males: 29 %					3-months follow-up
			Females: 71 %
			Mean age: 42.7 ± 10.2 years
			After 3 months, n = 74
Martínez-Herrera et al., 2018b⁴⁷	Spain/BAS	EC: aggressive periodontitis, < 14 remaining teeth, infectious or other inflammatory diseases, periodontal therapy in the last 6 months or antibiotics in the last 3 months, treatment with systemic anti-inflammatory drugs, pregnancy or lactation, secondary obesity, antibiotic treatment before the dental intervention, and diabetes mellitus	n = 47	BMI ≥ 30 kg/m²	≥ 4 teeth with ≥ 1 sites with PD ≥ 4 mm and CAL ≥ 3 mm	Intensive full-mouth NSPT, OHI and 0.12 % chlorhexidine mouth rinse	Before NSPT	Periodontal examinations at 3-months post-therapy
			Males: 31.9 %					3-months follow-up
			Females: 68.1 %
			Mean age: 44.4 ± 10.4 years
Çetiner et al., 2019⁴⁵	Turkey /BAS	IC: > 20 years old, > 22 remaining teeth, and no systemic diseases	n = 21	BMI ≥ 30 kg/m²	≥ 30 % of the sites with bone loss and ≥ 2 non-adjacent teeth with ≥ 1 sites with PD ≥ 5 mm and CAL ≥ 5 mm in each quadrant and BOP	Intensive full-mouth NSPT	Before FMT	NA
		EC: localized chronic periodontitis, receiving periodontal therapy/surgery in the last 6 months, pregnancy or use of any hormone therapy, antibiotic or anti-inflammatory drug therapy within the last 6 months, smoker, lactating, aggressive periodontitis, and periapical pathologies	Females: 100 %	WC > 102 cm (males) and > 88 cm (females)				3-months follow-up
			Mean age: 44.67 ± 10.87 years
Peralta et al., 2020⁴⁸	Brazil / BAS	IC: ≥ 45 years old, both sexes, moderate, severe, and advanced periodontitis, and ≥ 12 remaining teeth	n = 55	BMI ≥ 30 kg/m²	Stage II: interdental PD ≤ 5 mm, CAL 3 to 4 mm, and radiographic bone loss at coronal third between 15 % to 33 %	FMD	Before NSPT	0.12 % chlorhexidine mouth rinse for 14 days post-therapy
		EC: orthodontic devices, pregnancy or breast-feeding, systemic diseases or other conditions that could influence the periodontal status (other than diabetes), alcohol abuse, prophylactic antibiotic coverage, systemic antibiotics and/or anti-inflammatory drugs six months prior to the study, and periodontal therapy within six months prior to the study	Males: 19 (34.5 %)	WC > 102 cm (males) and > 88 cm (females)	Stage III and IV: PD ≥ 6 mm, interdental CAL ≥ 5 mm, and radiographic bone loss extending to mild-third of the root			Every 3-months, OHR, supragingival dental scaling and professional prophylaxis
			Females: 36 (65.5 %)
			Mean age: 48.9 ± 7.8 years
Md Tahir et al., 2020⁴⁹	Malaysia/BAS	IC: > 30 years old, obesity and normal weight, and ≥ 12 remaining teeth	n = 18	BMI ≥ 30 kg/m²	≥ 2 interproximal sites with PD ≥ 4 mm and ≥ 2 interproximal sites with CAL ≥ 3 mm (different teeth) or one site with PD ≥ 5 mm	Intensive full-mouth NSPT and OHI	Before NSPT	15 mL 0.12 % chlorhexidine mouth rinse, t.i.d., for 14 days post-therapy
		EC: history of periodontal therapy in last 6 months, on antibiotics and topical/systemic steroid treatment in last 4 months, pregnancy, lactating mothers, mentally handicapped, and valve replacement and rheumatic heart disease which require antibiotic coverage	Males: 6 (33.3 %)			Root surface debridement at sites with PD ≥ 5mm		3-months follow-up
			Females: 12 (66.7 %)			Periodontal pockets irrigated with 0.12 % chlorhexidine
			Mean age: 44.7 ± 2.4 years			0.12 % chlorhexidine mouth rinse
Montero et al., 2020³⁶	Spain/RCT	IC: 35–65 years old, metabolic syndrome [MetS (at least, 3 risk factors: WC ≥ 94 cm in men and ≥ 80 cm in women, triglycerides ≥150 mg/dL, HDL < 40 mg/dL in males and < 50 mg/dL in females, BP systolic ≥ 130 and/or diastolic ≥ 85 mm Hg, FPG ≥ 100 mg/dL)], stages III-IV generalized periodontitis, and ≥ 16 remaining teeth	n = 63	WC ≥ 94 cm (males) and ≥ 80 cm (females)	≥ 8 sites with PD ≥ 6 mm and 4 sites with CAL ≥ 5 mm in ≥ 2 different quadrants	NSPT, OHI and administration of a systemic antibiotic (azithromycin 500 mg, q.d., for 3 days), administered at the last session of SRP	Minimal periodontal therapy (supragingival professional mechanical plaque and calculus removal) + administration of placebo medication for 3 days + OHI	0.12 % chlorhexidine and 0.05 % cetylpyridinium chloride mouth rinse for 14 days post-therapy
		EC: uncontrolled systemic diseases other than diabetes or hypertension, surgical treatment in the previous 3 months, alcoholism or psychiatric disorders, systemic antibiotic in the previous 3 months, NSPT in the previous 6 months, or surgical periodontal treatment over the previous 12 months	CG = 31 and IG = 32					professional prophylaxis in both groups at the 3- and 6-months post-therapy
			Males: 44 (69.8 %); CG = 22 (70.9 %) and IG = 22 (68.8 %)					6-months follow-up
			Females: 19 (30.2 %); CG = 9 (29.1 %) and IG = 10 (31.2 %)
			Mean age: CG = 58.3 ± 5.8 years and IG = 56.7 ± 6.5 years
Cortelli et al., 2021⁵⁰	Brazil / BAS	IC: ≥ 45 years old, both genders, moderate to advanced generalized periodontitis (Stage II-IV), and ≥ 12 remaining teeth	n = 55	BMI ≥ 30 kg/m²	Interproximal CAL detectable in ≥ 2 teeth (non-adjacent)	FMD	Before NSPT	0.12 % chlorhexidine mouth rinse for 14 days post-therapy
		EC: chronic renal failure, stroke history, not controlled diabetes, rheumatism, osteoporosis, HIV, acute myocardial infarction 6 months before the study, pregnant and lactating, and periodontal treatment in last year	Males: 19 (34.5 %)	WC > 102 cm (males) and > 88 cm (females)	or			Every 3 months, OHR, professional prophylaxis and supragingival debridement
			Females: 36 (65.5 %)		PD > 3 mm and CAL ≥ 3 mm in ≥ 2 teeth			6-months follow-up
			Mean age: 48.9 ± 7.8 years

Object of investigation	Follow-up	Akram et al., 2017⁶⁷		Basher et al., 2017³⁵		Montero et al., 2020³⁶
Object of investigation	Follow-up	CG (n=31)	IG (n=31)	CG (n=31)	IG (n=31)	CG (n=31)	IG (n=32)
Blood hematological and biochemical index
High-sensitivity C-reactive protein (hsCRP) - mg/L	Baseline	-	-	-	-	3.9 ± 3.4^A	3.9 ± 2.9^A
	3 months	-	-	-	-	3.9 ± 0.6^B	2.7 ± 0.4^B
	6 months	-	-	-	-	4 ± 0.8^B	2.9 ± 0.4^B
Fibrinogen - mg/dL	Baseline	-	-	-	-	398.5 ± 89.1^A	419.7 ± 108.7^A
	3 months	-	-	-	-	398.3 ± 17.9^B	421.8 ± 20.4^B
	6 months	-	-	-	-	400.5 ± 16.1^B	419.6 ± 21.8^B
White blood cells count - K/µL	Before	-	-	-	-	7.5 ± 1.7^A	7.8 ± 1.9^A
	3 months	-	-	-	-	7.8 ± 0.3^B	7.5 ± 0.4^B
	6 months	-	-	-	-	7.6 ± 0.2^B	7.9 ± 0.7^B
Glycated hemoglobin (Hba1c) - %	Before	-	-	-	-	6 ± 1^A	6.3 ± 1.2^A
	3 months	-	-	-	-	6.1 ± 0.2^A	5.9 ± 0.1^A
	6 months	-	-	-	-	6.1 ± 0.2^A	6 ± 0.1^A
Fasting plasma glucose - mg/dL	Before	-	-	-	-	133 ± 51.7^A	128.6 ± 30.3^A
	3 months	-	-	-	-	130 ± 8.8^B	123.3 ± 7.9^B
	6 months	-	-	-	-	130.5 ± 9.7^B	121 ± 6.3^B
Fasting insulin - mIU/L	Before	-	-	-	-	14.5 ± 9.3^A	19.3 ± 10.8^A
	3 months	-	-	-	-	14.1 ± 1.4^B	17.2 ± 2.9^B
	6 months	-	-	-	-	14.4 ± 1.7^B	14.3 ± 2.1^B
Total cholesterol - mg/dL	Before	-	-	-	-	189.4 ± 48.4^A	174.8 ± 34.7^A
	3 months	-	-	-	-	180.6 ± 8.1^B	184 ± 8.4^B
	6 months	-	-	-	-	189.9 ± 9.2^B	183.5 ± 7.5^B
High density lipoprotein cholesterol (HDL) - mg/dL	Before	-	-	-	-	46.9 ± 12.4^A	46.1 ± 13.3^A
	3 months	-	-	-	-	47.1 ± 3.1^B	46.2 ± 3.8^B
	6 months	-	-	-	-	48.4 ± 2.7^B	47.2 ± 2.7^B
Low density lipoprotein cholesterol (LDL) - mg/dL	Before	-	-	-	-	105.7 ± 44.9^A	114.3 ± 34.7^A
	3 months	-	-	-	-	103.5 ± 7^B	109.6 ± 8.5^B
	6 months	-	-	-	-	107.5 ± 8.3^B	107.6 ± 6.6^B
Triglycerides - mg/dL	Before	-	-	-	-	136.6 ± 42.5^A	129.5 ± 52.3^A
	3 months	-	-	-	-	155.4 ± 17.5^B	136.5 ± 9.7^B
	6 months	-	-	-	-	131.7 ± 8.3^B	125.6 ± 9.7^B
Creatinine - mg/dL	Before	-	-	-	-	0.9 ± 0.3^A	0.9 ± 0.5^A
	3 months	-	-	-	-	0.9 ± 0.1^B	1.0 ± 0.1^B
	6 months	-	-	-	-	1 ± 0.1^B	1.0 ± 0.1^B
α-1 antitrypsin - mg/dL	Before	-	-	-	-	138.5 ± 28.1^A	145.6 ± 29.7^A
	3 months	-	-	-	-	130 ± 5^B	138.4 ± 6.2^B
	6 months	-	-	-	-	127.6 ± 5.2^B	137.5 ± 5.7^B
Homeostatic model assessment 2 (HOMA2) β-cell function	Before	-	-	-	-	92.7 ± 50.6^A	104.8 ± 69^A
	3 months	-	-	-	-	87.2 ± 10.6^B	106 ± 14.8^B
	6 months	-	-	-	-	100.4 ± 11.9^B	106.1 ± 14^B
Homeostatic model assessment 2 (HOMA2) insulin sensitivity	Before	-	-	-	-	62.6 ± 28^A	59 ± 55.3^A
	3 months	-	-	-	-	57.9 ± 5.4^B	67 ± 13.6^B
	6 months	-	-	-	-	59.7 ± 5.3^B	65.8 ± 11.6^B
Homeostatic model assessment 2 (HOMA2) insulin resistance	Before	-	-	-	-	2 ± 1.2^A	2.6 ± 1.4^A
	3 months	-	-	-	-	2 ± 0.2^B	2.3 ± 0.4^B
	6 months	-	-	-	-	2 ± 0.2^B	2.2 ± 0.3^B
Systemic biomarkers of inflammation
Resistin - ng/mL (blood serum)	Baseline	14.25 ± 4.58^A	12.26 ± 1.24^A	-	-	-	-
Resistin - ng/mL (blood serum)	3 months	13.47 ± 5.20^A	11.62 ± 0.90^A	-	-	-	-
Interlukin-1β (IL-1β) - pg/mL (blood serum)	Baseline	-	-	-	-	1.9 ± 1.2^A	1.5 ± 0.9^A
	3 months	-	-	-	-	2.3 ± 0.5^B	0.9 ± 0.1^B
	6 months	-	-	-	-	1.5 ± 0.2^B	1.5 ± 0.2^B
Interleukin-6 (IL-6) - pg/mL (blood serum)	Baseline	-	-	-	-	2.8 ± 1.9^A	2.2 ± 1.8^A
	3 months	-	-	-	-	2.6 ± 0.4^B	1.9 ± 0.4^B
	6 months	-	-	-	-	2.5 ± 0.4^B	2.0 ± 0.4^B
Interleukin-8 (IL-8) - pg/mL (blood serum)	Baseline	-	-	-	-	5.4 ± 3^A	6.9 ± 9.7^A
	3 months	-	-	-	-	5.4 ± 0.8^B	4.6 ± 1.1^B
	6 months	-	-	-	-	6 ± 1.2^B	5 ± 1.2^B
Tumor necrosis factor-α (TNF-α) - pg/mL (blood serum)	Baseline	-	-	-	-	8.7 ± 8.6^A	7.9 ± 6.2^A
	3 months	-	-	-	-	10 ± 2.3^B	6.4 ± 0.8^B
	6 months	-	-	-	-	8.2 ± 1.4^B	6.3 ± 0.8^B
Quality of Life
Oral Health Impact Profile (OHIP PI)	Baseline	-	-	19 ± 61.29^A	21 ± 67.74^A	-	-
Oral Health Impact Profile (OHIP PI)	3 months	-	-	12 ± 38.71^A	10 ± 32.26^A	-	-
Oral Health Impact Profile (OHIP SS)	Baseline	-	-	58.29 ± 6.12^A	57.2 ± 8.61^A	-	-
Oral Health Impact Profile (OHIP SS)	3 months	-	-	60.95 ± 6.64^A	61.89 ± 7.04^A	-	-
Oral Health Impact Profile (OHIP EI)	Baseline	-	-	1.5 ± 1.53^A	1.62 ± 1.84^A	-	-
Oral Health Impact Profile (OHIP EI)	3 months	-	-	0.65 ± 1.02^A	0.47 ± 0.91^A	-	-
Periodontal pathogens count/group
Porphyromonas gingivalis (log of CFU)	Baseline	-	-	-	-	13.3 ± 2.1^A	11.3 ± 5.7^A
	3 months	-	-	-	-	11.8 ± 1^B	3.8 ± 0.9^B
	6 months	-	-	-	-	11.8 ± 1.1^B	4.5 ± 1^B
Prevotella intermedia (log of CFU)	Baseline	-	-	-	-	11.2 ± 3.7^A	10.3 ± 5.1^A
	3 months	-	-	-	-	10.3 ± 1^B	4.2 ± 1^B
	6 months	-	-	-	-	9.9 ± 1^B	6.2 ± 1^B
Aggregatibacter actinomycetemcomitans (log of CFU)	Baseline	-	-	-	-	0	0.9 ± 2.8^A
	3 months	-	-	-	-	0.4 ± 0.4^B	0
	6 months	-	-	-	-	0	0.1 ± 0.1^B
Tannerella forsythia (log of CFU)	Baseline	-	-	-	-	6.3 ± 6.1^A	6.7 ± 6.3^A
	3 months	-	-	-	-	6.1 ± 1.3^B	0.3 ± 0.3^B
	6 months	-	-	-	-	5.2 ± 1.3^B	2.4 ± 0.8^B
Parvimonas micra (log of CFU)	Baseline	-	-	-	-	1.3 ± 3.4^A	2 ± 4.6^A
	3 months	-	-	-	-	1.8 ± 0.9^B	1.4 ± 0.7^B
	6 months	-	-	-	-	0.7 ± 0.5^B	0.3 ± 0.3^B
Fusobacterium nucleatum (log of CFU)	Baseline	-	-	-	-	10 ± 4.1^A	8 ± 5.6^A
	3 months	-	-	-	-	9.4 ± 1.1^B	6.4 ± 0.9^B
	6 months	-	-	-	-	8.3 ± 1.2^B	6.1 ± 0.9^B
Campylobacter rectus (log of CFU)	Baseline	-	-	-	-	NA	1.1 ± 3.4^A
	3 months	-	-	-	-	0.9 ± 0.6^B	0.7 ± 0.5^B
	6 months	-	-	-	-	0	1.0 ± 0^B
Eikenella corrodens (log of CFU)	Baseline	-	-	-	-	2.4 ± 4.7^A	1.9 ± 4.2^A
	3 months	-	-	-	-	2.4 ± 0.9^B	1.2 ± 0.6^B
	6 months	-	-	-	-	3.3 ± 1^B	1.2 ± 0.6^B
Capnocytophaga spp. (log of CFU)	Baseline	-	-	-	-	1.7 ± 4.1^A	1.3 ± 3.5^A
	3 months	-	-	-	-	2 ± 0.8^B	1 ± 0.6^B
	6 months	-	-	-	-	0.4 ± 0.4^B	1.2 ± 0.6^B

Object of investigation	Follow-up	Al-Zahrani and AlGhamdi, 2012¹¹	Altay et al., 2013³⁷	Gonçalves et al., 2015a³⁸	Gonçalves et al., 2015b³⁹	Balli et al., 2016a⁴⁰	Balli et al., 2016b⁴¹	Öngöz-Dede et al., 2016⁴²
Object of investigation	Follow-up	( = 20)	( = 22)	( = 18)	( = 20)	( = 20)	( = 20)	( = 15)
Blood hematological and biochemical index
High-sensitivity C-reactive protein (hsCRP) - mg/L	Baseline	0.96 ± 0.41^A	3.3 (3.2 to 6)^C	-	-	-	-	-
	2 months	D = 0.19 ± 0.32^A	-	-	-	-	-	-
	3 months	-	3 (3.1 to 4.1)^C	-	-	-	-	-
Fasting blood glucose - mg/dL	Before	-	104 (93 to 115)^C	-	-	-	-	-
Fasting blood glucose - mg/dL	3 months	-	97 (83 to 109)^C	-	-	-	-	-
Insulin - µU/mL	Before	-	16.8 (11.5 to 24.8)^C	-	-	-	-	-
Insulin - µU/mL	3 months	-	15.1 (7.1 to 17.8)^C	-	-	-	-	-
Homeostasis model assessment of insulin resistance (HOMA-IR)	Before	-	4.9 (1.1 to 11.8)^C	-	-	-	-	-
	3 months	-	3.6 (0.79 to 7.8)^C	-	-	-	-	-
Total cholesterol - mg/dL	Before	-	194 ± 37^A	-	-	-	-	-
Total cholesterol - mg/dL	3 months	-	188 ± 31^A	-	-	-	-	-
High density lipoprotein cholesterol (HDL) - mg/dL	Before	-	41 ± 9^A	-	-	-	-	-
High density lipoprotein cholesterol (HDL) - mg/dL	3 months	-	41 ± 7^A	-	-	-	-	-
Low density lipoprotein cholesterol (LDL) - mg/dL	Before	-	107 (96 to 134)^C	-	-	-	-	-
Low density lipoprotein cholesterol (LDL) - mg/dL	3 months	-	103 (91 to 128)^C	-	-	-	-	-
Triglycerides - mg/dL	Before	-	167 (135 to 224)^C	-	-	-	-	-
Triglycerides - mg/dL	3 months	-	162 (113 to 202)^C	-	-	-	-	-
Lipoprotein-a - g/L	Baseline	-	0.15 (0.1 to 0.22)^C	-	-	-	-	-
Lipoprotein-a - g/L	3 months	-	0.14 (0.1 to 0.2)^C	-	-	-	-	-
Systemic biomarkers of inflammation
Tumor necrosis factor-α (TNF-α) - mg/L^¢ or pg/mL^¥ (blood serum)	Before	-	5.4 (3 to 9.1)^C¢	-	3 ± 0.8^A¥	-	-	-
	3 months	-	3.3 (2.8 to 5.5)^C¢	-	3.1 ± 1.4^A¥	-	-	-
	6 months	-	-	-	3.1 ± 1^A¥	-	-	-
	12 months	-	-	-	2.9 ± 1^A¥	-	-	-
Tumor necrosis factor-α (TNF-α) - pg/mL (gingival crevicular fluid)	Baseline	-	-	-	-	-	10.8 (6.2 up to 14.2)^D	-
	6 weeks	-	-	-	-	-	3.8 (3.1 up to 4.8)^D	-
Interleukin-6 (IL-6) - ng/L^£ or pg/mL^¥ (blood serum)	Before	-	1.1 (0.8 to 1.9)^C£	-	2.7 ± 1.6^A¥		-	-
	3 months	-	0.6 (0.3 to 1.4)^C£	-	2.9 ± 0.9^A¥	-	-	-
	6 months	-	-	-	2.3 ± 0.8^A¥	-	-	-
	12 months	-	-	-	2.3 ± 0.8^A¥	-	-	-
Interleukin-6 (IL-6) - pg/mL (gingival crevicular fluid)	Baseline	-	-	-	-	2.3 (2 up to 2.7)^D	-	-
Interleukin-6 (IL-6) - pg/mL (gingival crevicular fluid)	6 weeks	-	-	-	-	0.7 (0.3 up to 1.2)^D	-	-
Resistin - ng/mL x 5 (blood serum)	Before	-	-	-	2.9 ± 1.7^A	-	-	-
	3 months	-	-	-	3.3 ± 1.7^A	-	-	-
	6 months	-	-	-	3.3 ± 2^A	-	-	-
	12 months	-	-	-	3.2 ± 2.3^A	-	-	-
Leptin - ng/L^£ or pg/mL^¥ x 100 (blood serum)	Baseline	-	17.5 (4.3 to 43.9)^C£	441.8 ± 213.7^A¥	481.8 ± 415.5^A¥	-	-	-
	3 months	-	14.4 (3.2 to 35.4)^C£	475.7 ±194.8^A¥	381 ± 301.8^A¥	-	-	-
	6 months	-	-	421.8 ± 266.7^A¥	319.3 ± 141.7^A¥	-	-	-
	12 months	-	-	-	400.9 ± 391^A¥	-	-	-
Adiponectin - ng/mL x 100 (blood serum)	Baseline	-	-	52.5 ± 36^A	62.2 ± 43.2^A	-	-	-
	3 months	-	-	49.1 ± 25.6^A	70.7 ± 47.8^A	-	-	-
	6 months	-	-	47.4 ± 34.3^A	56.3 ± 34.6^A	-	-	-
	12 months	-	-	-	71.1 ± 57.1^A	-	-	-
Chemerin (gingival crevicular fluid)	Baseline	-	-	-	-	112.2 (107.9 up to 125.0)^D	-	-
Chemerin (gingival crevicular fluid)	6 weeks	-	-	-	-	47.6 (36.9 up to 53.8)^D	-	-
Vaspin (gingival crevicular fluid)	Baseline	-	-	-	-	-	1.1 (0.8 up to 1.3)^D	-
Vaspin (gingival crevicular fluid)	6 weeks	-	-	-	-	-	0.5 (0.4 up to 0.6)^D	-
Omentin-1 (gingival crevicular fluid)	Baseline	-	-	-	-	-	16.8 (15 up to 18.6)^D	-
Omentin-1 (gingival crevicular fluid)	6 weeks	-	-	-	-	-	25.7 (21.1 up to 31.9)^D	-
Systemic biomarkers of oxidative stress
8-hydroxy-deoxyguanosine (8-OHdG) - Pg/µg DNA (blood serum)	Before	-	-	-	-	-	-	1.9 ± 0.35^A
8-hydroxy-deoxyguanosine (8-OHdG) - Pg/µg DNA (blood serum)	30 days	-	-	-	-	-	-	0.54 ± 0.23^A
8-hydroxy-deoxyguanosine (8-OHdG) - pg/mL (saliva)	Before	-	-	-	-	-	-	927.94 ± 116.66^A
8-hydroxy-deoxyguanosine (8-OHdG) - pg/mL (saliva)	30 days	-	-	-	-	-	-	652.58 ± 139.51^A
8-hydroxy-deoxyguanosine (8-OHdG) - pg/mL (gingival crevicular fluid)	Before	-	-	-	-	-	-	1178.44 ± 97.34^A
	30 days	-	-	-	-	-	-	1003.66 ± 157.85^A
Object of investigation	Follow-up	Taşdemir et al., 2016	Zuza et al., 2016	Martínez-Herrera et al., 2018a	Martínez-Herrera et al., 2018b	Çetiner et al., 2019	Peralta et al., 2020	Md Tahir et al., 2020
Object of investigation	Follow-up	( = 14)	( = 28)	( = 74)	( = 46)	( = 21)	( = 55)	( = 18)
Blood hematological and biochemical index
Retinol-binding protein 4 (RBP4) - mg/L	Baseline	-	-	3.84 ± 1.06^A	3.78 ± 1.11^A	-	-	-
Retinol-binding protein 4 (RBP4) - mg/L	3 months	-	-	3.46 ± 1.01^A	3.44 ± 1.05^A	-	-	-
Glucose - mg/L	Before	86.5 (80.5 to 92.2)^D	99.8 ± 13.4^A	95 ± 12^A	95.2 ± 11.2^A	-	-	-
	3 months	91.5 (78.5 to 96.5)^D	102 ± 15.9^A	94.8 ± 12^A	95.7 ± 11.4^A	-	-	-
	6 months	90.5 (78.5 to 97.5)^D	-	-	-	-	-	-
Glycated hemoglobin (Hba1c) - %	Before	5.3 (5.2 to 5.6)^D	5.4 ± 1^A	-	-	-	-	-
	3 months	5.2 (5.1 to 5.4)^D	4.4 ± 0.8^A	-	-	-	-	-
	6 months	5.2 (5.1 to 5.5)^D	-	-	-	-	-	-
Insulin - µU/mL	Before	18.3 (10.7 to 22.6)^D	-	20 ± 14.6^A	19.5 ± 10.9^A	-	-	-
	3 months	14.7 (7.8 to 18.6)^D	-	19.2 ± 11.3^A	20.9 ± 11.9^A	-	-	-
	6 months	17.1 (8.5 to 23.4)^D	-	-	-	-	-	-
Homeostasis model assessment of insulin resistance (HOMA-IR)	Before	3.93 (2.25 to 5.06)^D	-	4.73 ± 3.8^A	4.58 ± 2.86^A	-	-	-
	3 months	3 (1.8 to 4.18)^D	-	4.61 ± 3.17^A	5.04 ± 3.39^A	-	-	-
	6 months	3.87 (2.05 to 5.37)^D	-	-	-	-	-	-
Total cholesterol - mg/dL	Before	192.5 ± 31.4^A	250 ± 14.1^A	182 ± 34^A	184 ± 33^A	208 ± 34.6^A	-	-
	3 months	200.2 ± 35.2^A	210.6 ± 16.3^A	185 ± 40^A	188 ± 37^A	200.3 ± 38.3^A	-	-
	6 months	192.7 ± 37.6^A	-	-	-	-	-	-
High density lipoprotein cholesterol (HDL) - mg/dL	Before	49.4 ± 15.6^A	51.1 ± 3.5^A	42 ± 11^A	43.1 ± 11.4^A	50.57 ± 9.52^A	-	-
	3 months	46.5 ± 12.2^A	50.4 ± 4.3^A	44 ± 12^A	43.8 ± 12.4^A	55.14 ± 13.28^A	-	-
	6 months	45.4 ± 14.1^A	-	-	-	-	-	-
Low density lipoprotein cholesterol (LDL) - mg/dL	Before	102.6 ± 27.4^A	170.8 ± 11.3^A	121 ± 26^A	116 ± 27^A	128.64 ± 28.5^A	-	-
	3 months	117.4 ± 34.4^A	152.7 ± 14^A	122 ± 31^A	118 ± 29^A	116.14 ± 38.7^A	-	-
	6 months	111.4 ± 36.5^A	-	-	-	-	-	-
Triglycerides - mg/dL	Before	166.4 (116.5 to 212)^C	172.1 ± 14.2^A	128 (98 to 167)^C	126 (86 to 162)^C	136.05 ± 46.2^A	-	-
	3 months	157.9 (120 to 220.1)^C	154.3 ± 15.9^A	119 (98 to 152)^C	132 (106 to 157)^C	138.52 ± 51.64^A	-	-
	6 months	167.5 (73 to 213.6)^C	-	-	-	-	-	-
Systemic biomarkers of inflammation
High-sensitivity C-reactive protein (hsCRP) - mg/L (blood serum))	Baseline	3.4 (3.4 to 5.4)^D	3.75 ± 0.5^A	8.33 ± 7.78^A	4.33 (1.85 to 6.29)^C	-	-	-
	3 months	3.3 (3.2 to 5.4)^D	2.62. ± 0.2^A	8.57 ± 7.92^A	3.64 (1.62 to 6.32)^C	-	-	-
	6 months	3.3 (3.2 to 8.2)^D	-	-	-	-	-	-
Tumor necrosis factor-α (TNF-α) - pg/mL (blood serum)	Before	12.8 (10.5 to 15)^D	-	17.23 ± 9.86^A	19 ± 11.7^A	-	-	-
	3 months	11.3 (7.2 to 16.1)^D	-	13.9 ± 5.37^A	14.4 ± 4.7^A	-	-	-
	6 months	3.8 (2.6 to 6.4)^D	-	-	-	-	-	-
	12 months	-	-	-	-	-	-	-
Tumor necrosis factor-α (TNF-α) - pg/mL (gingival crevicular fluid)	Before	-	-	-	-	9.0 ± 6.1^A	-	-
	3 months	-	-	-	-	7.2 ± 5.9^A	-	-
Interleukin (IL-6) - pg/mL (blood serum)	Before	2.23 (1.8 to 4.6)^D	-	3.79 ± 2.04^A	2.93 ± 1.31^A	-	-	-
	3 months	2.13 (1.8 to 3)^D	-	3.38 ± 2.48^A	2.52 ± 1.44^A	-	-	-
	6 months	2.04 (1.8 to 2.4)^D	-	-	-	-	-	-
	12 months	-	-	-	-	-	-	-
Interleukin (IL-6) - pg/mL (gingival crevicular fluid)	Before	-	-	-	-	3.61 ± 4.43^A	-	-
Interleukin (IL-6) - pg/mL (gingival crevicular fluid)	3 months	-	-	-	-	1.76 ± 2.29^A	-	-
Complement C3 (blood serum)	Before	-	-	-	128 ± 18^A	-	-	-
Complement C3 (blood serum)	3 months	-	-	-	129 ± 28^A	-	-	-
Visfatin - pg/mL (gingival crevicular fluid)	Before	-	-	-	-	21.53 ± 39.55^A	-	-
Visfatin - pg/mL (gingival crevicular fluid)	3 months	-	-	-	-	6.96 ± 3.49^A	-	-
Resistin - ng/mL (blood serum)	Before	-	-	-	-	-	-	14.7 (10.8 to 18.5)^E
Resistin - ng/mL (blood serum)	3 months	-	-	-	-	-	-	17.6 (12.4 to 22.7)^E
Pentraxin-related protein 3 (PTX3) (blood serum)	Before	4.76 (3.1 to 7.9)^D	-	-	-	-	-	-
	3 months	4.50 (3 to 6.9)^D	-	-	-	-	-	-
	6 months	4.62 (3 to 6.8)^D	-	-	-	-	-	-
Periodontal pathogens count
(total bacterial count^† or x 10⁶ copy cells^§)	Before	-	-	-	-	-	17.06 ± 4.62^F†	1.7 (1.5 to 2)^E§
	3 months	-	-	-	-	-	3.65 ± 1.22^F†	1.5 (1.3 to 1.7)^E§
	6 months	-	-	-	-	-	9.81 ± 2.81^F†	-
	9 months	-	-	-	-	-	13.88 ± 5.49^F†	-
(total bacterial count^† or x 10⁶ copy cells^§)	Before	-	-	-	-	-	58.52 ± 18.77^F†	0.6 (0.4 to 0.8)^E§
	3 months	-	-	-	-	-	22.05 ± 7.2^F†	0.7 (0.5 to 0.9)^E§
	6 months	-	-	-	-	-	55.87 ± 16.24^F†	-
	9 months	-	-	-	-	-	33.24 ± 8.79^F†	-
(x 10⁶ copy cells)	Before	-	-	-	-	-	-	1.0 (0.7 to 1.3)^E
	3 months	-	-	-	-	-	-	0.6 (0.4 to 0.9)^E
	6 months	-	-	-	-	-	-	-
	9 months	-	-	-	-	-	-	-
(total bacterial count)	Before	-	-	-	-	-	18.14 ± 6.01^F	-
	3 months	-	-	-	-	-	5.64 ± 1.51^F	-
	6 months	-	-	-	-	-	14.77 ± 4.09^F	-
	9 months	-	-	-	-	-	7.14 ± 2.32^F	-
(total bacterial count)	Before	-	-	-	-	-	92.0 ± 20.7^F	-
	3 months	-	-	-	-	-	65.6 ± 36.6^F	-
	6 months	-	-	-	-	-	48.2± 15.4^F	-
	9 months	-	-	-	-	-	21.1 ± 6.6^F	-
Quality of Life
OHqOL	Baseline	-	-	-	-	-	-	-
OHqOL	6 months	-	-	-	-	-	-	-
OIDP	Baseline	-	-	-	-	-	-	-
OIDP	6 months	-	-	-	-	-	-	-

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[1] Corresponding Author: Maria Cynésia Medeiros de Barros E-mail: cynesiaster@gmail.com