Table 1 Overview of included studies: description of study characteristics and extracted data, stratifies by microbiological (A), immunological (B) and biochemical (C) outcomes
From: Resistance and resilience to experimental gingivitis: a systematic scoping review
First author, yearreference | Study population | Design set up | Parameters | Results resilience |
|---|---|---|---|---|
A. Microbiological outcomes | ||||
 Lie, 1998 [6] | N = 25 Age: 19–27 years, mean: 22 Sex: M: 12, F:13 Groups: 1 group non-dental university students Ethnicity: NR Smoking: 11 (M:6; F:5) Average cigarettes: 15.6 a day General health: Good general health Oral health: 24 teeth, > 30% bleeding on probing, pockets < 5 mm. | Pre-trial phase: Length: NR Treatment: OHI, PP Induction phase: Length: 14 days Treatment: PP at the end Resolution phase: N/A Samples: supragingival plaque, approximal plaque, subgingival plaque, tongue scrape | - Total CFU - P. micros - Streptococcus spp. - A. actinomycetemcomitans - C. rectus - F. nucleatum - P. intermedia - Actinomyces spp. | Supragingival plaque No difference found in groups and over time in total CFU, P. micros, Streptococcus spp. Actinomyces spp. and F. nucleatum, P. intermedia increased from day 0 to day 14 in non-smokers group. C. rectus increased in both groups. Subgingival plaque No difference was found over time and between P. micros, Streptococcus spp., A. actinomycetemcomitans, C. rectus, F. nucleatum groups in abundance. Total CFU in smokers was at day 14 higher compared to baseline. Actinomyces spp. and P. intermedia increased significantly over time in both groups. Approximal plaque: Total CFU, A. actinomycetemcomitans, Actinomyces spp., C. rectus (in smokers) and F. nucelatum (in non-smokers), P. micros, streptococci spp. did not change over time. Actinomyces spp. and C. rectus increased over time in non-smokers group and F. nucleatum in smokers group. |
 Salvi, 2005 [7] | N = 22 Age: mean 24.7 (2.2 SD) years Sex: M:7, F:15 Groups: smokers (N = 11) and control group of non-smokers (N = 11) all students. Ethnicity: NR Smoking: 11, > 5 years of smoking General health: No relevant medical conditions, general good health Oral health: > 24 permanent teeth, pockets < 4 mm | Pre-trial phase: Length: 21 days Treatment: PP and OHI Induction phase: Length: 21 days Treatment: none Resolution phase: Length: 14 days Treatment: OHI, PP Sample: subgingival plaque | - P. gingivalis - T. denticola - T. forsythia | Bacteria in smokers and non-smokers did not differ over time. At day 35 smokers had fewer bacteria compared to day 21. |
B. Immunological outcomes | ||||
 Belstrom, 2017 [9] | N = 29 Age: 22–29 years Sex: M: 5, F:24 Groups: dental students Ethnicity: NR Smoking: non-smokers General health: Systemically healthy Oral health: No active caries, no gingivitis or periodontitis, no hyposalivation or medication use. | Pre-trial phase: Length: none Treatment: NA Induction phase: Length: 10 days Treatment: none Resolution phase: Length: 14 days Treatment: none Samples: stimulated saliva | - IL-1β - IL-8 - MCP-1 - VEGF | IL-1β, IL-8, MCP-1, and VEGF levels all reduced during induction phase compared to baseline levels. And IL-8 remained low after resolution phase. |
 Brecx, 1988 [10] | N = 8 Age: 22–26 years Sex: NR Groups: dental students Ethnicity: NR Smoking: NR General health: NR Oral health: NR | Pre-trial phase: Length: 14 days Treatment: PP Induction phase: Length: 21 days Treatment: none Resolution phase: Length: 8 days Samples: gingival biopsy | - Lymphocytes - Macrophages - PMNs - Plasma cells | Levels of lymphocytes, plasma cells and macrophages did not change at day 8 of the resolution phase compared to end of EG, except PMNs: they increased significantly at day 8 (18.1% at end of EG, 21.9% at day 8 of resolution |
 Giannopoulou, 2003 [11] | N = 22 Age: 19–33 years, mean 26 Sex: M: 14, F: 8 Groups: dental students, 2 groups non-smokers and smokers Ethnicity: NR Smoking: N = 10 General health: Systemically healthy Oral health: Smokers > 10 cigarettes a day, > 24 permanent teeth, GI < 1 | Pre-trial phase: Length: 12 days Treatment: PP, OHI Induction phase: Length: 10 days Treatment: PP, OHI Resolution phase: N/A Samples: GCF | - IL-1β - IL-4 - IL-8 | IL-1β increased significantly in the induction phase in both smokers and non-smokers. IL-4 at baseline is significantly lower in smokers compared to non-smokers and does not change over time. In non-smokers IL-4 decreases significantly over time and stays higher compared to smokers. IL-8 levels at baseline is significantly higher compared to non-smokers, this applies also at day 10. In both smokers as non-smokers the levels of IL-8 increase significantly. |
 Heasman, 1992 [12] | N = 7 Age: 18–21 year Sex: NR Groups: NR Ethnicity: NR Smoking: NR General health: NR Oral health: > 20 permanent teeth, < 3 mm pocket depth, no bone loss | Pre-trial phase: Length: 7 days Treatment: PP Induction phase: Length: 28 days Treatment: PP Resolution phase: N/A Samples: GCF | - IL-1B - LTB4 - PGE2 - TxB2 | IL-1B increased over time during the induction phase compared to baseline. LTB4 levels differed significantly only in 7 and 28 days, in between the levels stay the same as baseline values. PGE2 and TxB2 values only changed compared to baseline after 28 days, before that the levels stay the same as at baseline. |
 Kinane, 1992 [13] | N = 12 Age: 20–21 years Sex: M: 8, F: 4 Groups: dental students Ethnicity: NR Smoking: NR General health: Unremarkable medical history Oral health: >  26 permanent teeth, healthy gingiva, < 4 mm pocket depth, no attachment loss | Pre-trial phase: Length: 8 weeks Treatment: monitoring oral health Induction phase: Length: 21 days Treatment: PP Resolution phase: Length: 14 days Treatment: none Samples: GCF | - IL-1 | IL-1 levels strongly increase from baseline to day 4 and stay at the same levels until day 14. The IL-1 levels return back to baseline levels at the end of the induction phase. |
 Leishman, 2013 [14] | N = 8 Age: 25.5 (7.1 SD) years Sex: M: 0, F: 8 Groups: university students Ethnicity: NR Smoking: none General health: Systemically healthy, non-pregnant and no use of antibiotics Oral health: No history of periodontal disease | Pre-trial phase: N/A Induction phase: Length: 21 days Treatment: PP and Oral B toothbrush Resolution phase: Length: 14 days Treatment: none Samples: GCF, saliva, blood plasma | - IL-1β - IL-2 - IL-4 - IL-5 - IL-6 - IL-10 - IFN-γ - sICAM-1 - TNF-α | GCF sample: IL-1β significantly decreases after 35 days. IL-2 increases from baseline to day 21 and decreases 10 fold at 35 days. TNF-α decreased in resolution phase and sICAM-1 was significantly higher at day 35 compared to day 14. IL-4, IL-5, IL-10, IL-12 and IF-γ values stayed the same over time. Saliva sample: Only IL-1β significantly decreased at day 35 compared to day 21. Other parameters did not change significantly. Plasma sample: Only sICAM-1 values changed significantly over time and increased from baseline to day 35. However the values between day 21 and 35 were not significantly different. |
 Lie, 2002 [15] | N = 25 Age: 19–27 mean 22 year Sex: M: 12, F:13 Groups: 1, non-dental university students Ethnicity: NR Smoking: N = 11 General health: Good general health Oral health: > 24 permanent teeth, < 4 mm pocket depth, no attachment loss | Pre-trial phase: Length: NR Treatment: PP Induction phase: Length: 14 days Treatment: PP Resolution phase: N/A Samples: stimulated saliva | - Total parotid salivary IgA | No change in salivary-IgA over time or difference between groups. |
 Norman, 1979 [16] | N = 10 Age: NR Sex: Male Groups: dental students Ethnicity: NR Smoking: none General health: Healthy Oral health: No periodontitis | Pre-trial phase: Length: NR Treatment: PP Induction phase: Length: 21 days Treatment: PP Resolution phase: N/A Samples: Blood and GCF | - IgA - IgM - IgG | IgG, IgM, IgA, showed no significant changes during the induction phase. |
 Reuland-Bosma, 1987 [17] | N = 16 Age: NR Sex: NR Groups: 2, 1 down syndrome children, 1 healthy control children. Ethnicity: NR Smoking: none General health: NR Oral health: NR | Pre-trial phase: N/A Induction phase: Length: 21 days Treatment: none Resolution phase: N/A Samples: gingival biopsies | - Leukocytes - PMNs | Number of PMNs and leukocytes did not change over time in the induction phase compared to baseline. |
 Seemann, 2004 [18] | N = 14 Age: 22–37, mean 27 years Sex: M:14, F: 0 Groups: 1 Ethnicity: NR Smoking: none General health: Clinically healthy Oral health: > 24 teeth, pockets depth < 4 mm, no active caries, good general health | Pre-trial phase: Length: 2 days Treatment: none Induction phase: Length: 12 days Treatment: PP Resolution phase: N/A Samples: (un)stimulated saliva | - Parotid IgA concentration - Parotid IgA secretion - SM/SL IgA concentration - SM/SL IgA secretion | Parotid IgA concentration, stayed the same during the trial. Parotid IgA secretion in stimulated saliva increased significantly from baseline to end of induction phase. SM/SL IgA concentration and secretion remained stable during the experiment. |
 Tsalikis, 2010 [19] | N = 10 Age: 20–22 (N = 5) and 61–65 years (N = 5) Sex: M:6, F: 4 Groups: 2, young adults and old adults Ethnicity: Caucasians Smoking: none General health: Clinically healthy Oral health: healthy periodontum, no bone loss, > 20 permanent teeth, attachment loss < 3 mm, bleeding on probing < 10%, plaque index < 20% | Pre-trial phase: N/A Induction phase: Length: 21 days Treatment: none Resolution phase: Length: 7 days Treatment: PP Samples: GCF | - IL-6 - IL-8 - TNF- α | Young group: TNF- α did not change over time. IL-6 and IL-8 increased from baseline to induction and to resolution phase. Old group: TNF- α increased from baseline to end of induction phase, and IL-6 from end induction phase to end of resolution phase. |
 Wahaidi, 2009 [20] | N = 156 Age: 18–31 years Sex: NR Groups: non smoking Ethnicity: NR Smoking: none General health: healthy Oral health: No periodontitis, < 4 mm probing depth, no caries | Pre-trial phase: Length: 21 days Treatment: OHI Induction phase: Length: 21 days Treatment: PP, OHI Resolution phase: Length: 21 days Treatment: none Samples: peripheral blood | - White blood cells - PMNs | No significant change in either parameter over time. |
 Zhou, 2012 [21] | N = 11 Age: years Sex: M: 11, F: 0 Groups: 1 group non-smoking dental students Ethnicity: NR Smoking: none General health: Unremarkable medical history Oral health: No periodontal disease, > 24 permanent teeth, healthy gingiva, good oral hygiene | Pre-trial phase: N/A Induction phase: Length: 21 days Treatment: none Resolution phase: Length: 7 days Treatment: none Samples: unstimulated whole saliva | - IL-6 - IL-1β | IL-6 showed increase at day 21 and returned to baseline values during the resolution phase. IL-1 β was significantly higher at day 14 and 21 compared to baseline, and returns to baseline values in resolution phase. |
C. Biochemical outcomes | ||||
 Aboodi, 2015 [8] | N = 5 Age: 20–36 year Sex: M:2, F:3 Groups: NR Ethnicity: NR Smoking: none General health: Systemically healthy Oral health: Periodontally healthy | Pre-trial phase: Length: 7 days Treatment: PP, OHI Induction phase: Length: 21 days Treatment: none Resolution phase: Length: 14 days Treatment: OHI, PP Sample: whole saliva | Proteome (fold change): - SPARC-like protein 1 (2.10) - Calmodulin-like protein 3 (2.11) - Mucin-6 (2.13) - Cystatin-S (2.14) - LOC349136 (2.18) - Tetratricopeptide repeat protein 28 (2.20) - Androgen receptor (2.21) - Serine 13 (2.21) - Carbonic anhydrase 6 (2.23) - Kinesin-like protein KIF3B (2.23) adenocarcinoma factor (2.25) - Thioredoxin (2.29) - cDNA FLJ38275 (2.31) - Apolipoprotein A-1 (2.32) - Pancreatic - Albumin (2.33) - Cystatin-SN (2.33) - OLIG2 (2.47) - Vitamine D-binding protein (2.78) - IG kappa chain C region (2.87) - G-protein r98 (3.41) - Lactoferrin (a.k.a. lactotransferrin) (3.50) - Beta-globin (3.75) - Anenxin A1 (4.15) - KIAA1539 (4.72) - Collagen alpha-1 (7.35) | All reported proteins changed over time and have a fold change > 2. |
 Adonogianaki, 1994 [22] | N = 6 Age: 22–23 year Sex: M:5, F:1 Groups: dental students Ethnicity: NR Smoking: NR General health: NR Oral health: < 3 mm pocket depth, no periodontal attachment loss | Pre-trial phase: Length: 10 days Treatment: PP, OHI Induction phase: Length: 21 days Treatment: none Resolution phase: Length: 14 days Treatment: none Samples: GCF | - Alpha2-macroglobulin - Alpha1-antitrypsin - Transferrin - Lactoferrin | Alpha1-antitrypsin, Alpha2-macroglobulin and transferrin increased during the induction phase and stayed elevated in the resolution phase. Lactoferrin increased also during the induction phase, but dropped again almost to baseline levels during the resolution phase. |
 Lie, 2001 [23] | N = 25 Age: 17–27 mean 22 years Sex: NR Groups: 2 groups, non-smokers and smokers Ethnicity: NR Smoking: 11 General health: Good general health Oral health: having gingivitis > 30% bleeding upon probing, < 5 mm of pockets, absence of approximal attachment loss. When treated in the pre-trial phase, patients with < 20% approximal bleeding sites entered the trial | Pre-trial phase Length: NR Treatment: OHI and PP Induction phase: Length: 14 days Treatment: none Resolution phase: N/A Samples: saliva | - Total protein (mg/ml) - Cystatin activity (units/ml) - Cystatin C (μg/ml) - Output cystatin activity (units/min) - Output cystatin C (μg/min) | Mean protein values remained stable over time. Cystatin activity significantly decreased at day 14 compared to baseline in smokers. Cystatin C was at day 14 significantly higher in non-smokers, and decreased during induction in smokers. Output cystatin activity was at day 14 higher in non-smokers. Output cystatin C decreased during induction in non-smokers and was significantly higher in smokers at day 14 |
 Norman, 1979 [16] | N = 10 Age: NR Sex: M: 10, F:0 Groups: dental students Ethnicity: NR Smoking: NR General health: NR Oral health: periodontally healthy | Pre-trial phase: Length: NR Treatment: PP Induction phase: Length: 21 days Treatment: PP Resolution phase: N/A Samples: Blood and GCF | - Alpha-antitrypsin - C4 - C3 - CH50 - Factor B - Transferrin | C3, Factor B, Alpha-antitrypsin and transferrin showed no significant changes during the induction phase. CH50 and C4 increased significantly at day 21 compared to baseline values. |
 Ozdemir, 2009 [24] | N = 12 Age: 19–21 years Sex: M: 12; F:0 Groups: dental students Ethnicity: NR Smoking: none General health: NR Oral Health: > 24 permanent teeth, systemic healthy, < 4 mm pocket depth, no attachment loss | Pre-trial phase: Length: 14 days Treatment: OHI, PP Induction phase: Length: 14 days Treatment: OHI, PP Resolution phase: Length: 21 days Treatment: none Samples: GCF, peripheral blood | - Lactoferrin | Lactoferrin in GCF and blood increased during the induction phase and returned to baseline in the resolution phase. |
 Que, 2004 [25] | N = 15 Age: 18–30 years Sex: M: 6, F: 9 Groups: NR Ethnicity: NR Smoking: none General health: Systemically healthy no NSAIDs use. Oral health:  < 5 mm pocket depth, no attachment loss | Pre-trial phase: Length: 11 days Treatment: PP and OHI Induction phase: Length: 10 days Treatment: PP Resolution phase: N/A Samples: GCF | - Total protein (ng/site) - Calprotectin (MRP8/14) (ng/site) - subunit MRP 8 (ng/site) - subunit MRP 14 (ng/site) | Total protein, calprotectin, MRP 8 and 14 did not change from baseline to day 10. However 1 day after cleaning this did increase significantly. |
 Siegel, 2007 [24] | N = 14 Age: 18–30 and 46–77 years Sex: M: 9, F: 5 Groups: 2 groups, 18–30 year old subject and 47–77 year old. Ethnicity: NR Smoking: none General health: No systemic diseases Oral health: < 3 mm pocket depth, no bleeding on probing, non-susceptible for periodontitis, > 20 permanent teeth, no systemic disease | Pre-trial phase: Length: 21 days Treatment: OHI and PP Induction phase: Length: 14 days Treatment: PP Resolution phase: N/A Samples: gingival biopsy | - Cyclooxygenase − 1 - Cyclooxygenase − 2- Cyclooxygenase − 3 - Microsomal prostaglandin e synthese-1 | Cyclooxygenase − 1 expression in Langerhans’cells increased in both study groups but was not significant. Cyclooxygenase − 2 expression in basal epithelial cells were significantly lower in the older age group. Cyclooxygenase − 3 was not detected in tissue samples. Microsomal prostaglandin E synthese-1 was detected in epithelial, endothelial and fibroblast-like connective tissue cells, however no significant difference was found between ages. |
 Uitto, 1996 [26] | N = 12 Age: NR Sex: NR Groups: 2 groups, student hygienists and healthy adults Ethnicity: NR Smoking: NR General health: NR Oral health: healthy periodontium | Pre-trial phase: N/A Induction phase: Length: 10 days Treatment: none Resolution phase: N/A Samples: saliva samples; water rinses | - Elastase | No significant changes in salivary elastase levels during the experiment. |
 Zhou, 2012 [21] | N = 11 Age: 21–22 years Sex: M: 11, F: 0 Groups: 1 group non-smoking dental students Ethnicity: NR Smoking: none General health: Unremarkable medical history Oral health: No periodontal disease, > 24 permanent teeth, healthy gingiva, good oral hygiene | Pre-trial phase: N/A Induction phase: Length: 21 days Treatment: none Resolution phase: Length: 7 days Treatment: none Samples: unstimulated whole saliva | - Calprotectin - Elastase activity | Calprotectin showed only change at day 21,and returned to baseline levels. Elastase activity was higher in the induction phase compared to resolution phase. |