Introduction
In this study, we aimed to investigate the efficacy of combined orthodontic-periodontic treatment in the treatment of patients with periodontitis and its effects on the levels of inflammatory cytokines.
Methods
A total of 117 patients with periodontitis were randomly assigned to the basic group (receiving basic periodontic treatment, n = 58) and the combined group (receiving combined orthodontic-periodontic treatment, n = 59). In addition, 52 healthy people without periodontal disease were selected as the normal group. Probing depth, tooth mobility, plaque index, clinical attachment level, and sulcus bleeding index were recorded. ELISA was applied to detect gingival crevicular fluid (GCF) and serum levels of inflammatory cytokines. A 2-year clinical follow-up was conducted.
Results
Before treatment, the periodontal parameters (probing depth, tooth mobility, plaque index, clinical attachement level, and sulcus bleeding index) and GCF and serum levels of inflammatory cytokines (high-sensitivity C-reactive protein, interleukin-1β, interleukin-5, interleukin-6, interleukin-8, tumor necrosis factor-α, and prostaglandin E2) in the combined and basic groups were higher than those in the normal group. After 6 and 18 months of treatment, the periodontal parameters and GCF and serum levels of inflammatory cytokines decreased in the combined and basic groups. The periodontal parameters and the GCF and serum levels of inflammatory cytokines in the combined group were significantly lower than those in the basic group after 18 months of treatment. The combined group had a lower recurrence rate compared with the basic group.
Conclusions
Combined orthodontic-periodontic treatment had good clinical efficacy in the treatment of periodontitis and could effectively decrease the levels of inflammatory cytokines.
Highlights
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After 18 months of combined treatment, the periodontal status of patients improved.
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Inflammation of gingival crevicular fluid (GCF) was improved after combined treatment.
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Inflammation of serum was also improved after combined treatment.
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Inflammatory cytokine levels in GCF and serum decreased after combined treatment.
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Combined periodontal orthodontic treatment showed good clinical efficacy.
Periodontitis is an infectious inflammatory disease of tooth-supporting tissues with high morbidity and alternative occurrence of remission and acute exacerbation. There are 2 main causes of periodontitis. One is the sedimentation of dental plaque bacteria, intercellular substances, exfoliated epithelial cells, and food debris deposited on the tooth surfaces, and the other is a deficiency of vitamins and minerals or an abnormality of the immune reaction caused by systemic disease. Periodontitis occurs with the intrusion of microorganisms in the periodontal pocket to the blood system through the damaged epithelium. The humoral immunity and cellular immunity activate the mononuclear macrophages and release a number of inflammatory cytokines, such as high-sensitivity C-reactive protein, interleukin-1β, interleukin-5, interleukin-6, interleukin-8, tumor necrosis factor-α, and prostaglandin E2. Overexpressions of inflammatory cytokines can worsen the periodontal inflammation, which is closely related to the development and progression of periodontal diseases.
The diagnosis of periodontitis is based on routine examinations of visual inspection, probing diagnosis and occlusal therapy, and bacterial plaque microbiologic examination, and gingival crevicular fluid (GCF) factor inspection can also reflect the occurrence of periodontitis. Clinical treatments of periodontitis have gradually diversified into drug treatment, orthodontic treatment, and periodontic treatment. Periodontic treatment includes the removal of bacterial plaque and treatment of the traumatic occlusion, which can effectively improve the patient’s gingival bleeding, periodontal abscess, and other periodontal symptoms. Orthodontic treatment can suppress pathologic tooth migration, control bacterial plaque, and establish a good occlusion to promote the restoration of the periodontal tissues. We aimed to compare the efficacy of the combined orthodontic-periodontic treatment and basic periodontic treatment for patients with periodontitis and to investigate the effects of combined orthodontic-periodontic treatment on levels of inflammatory cytokines.
Materials and methods
This study was performed with the approval of the ethnic committee of Dongyang People’s Hospital, Dongyang, China. Informed consent was obtained from all subjects.
Between January 2011 and January 2013, a total of 117 patients with periodontitis were selected from our hospital. They included 67 men and 50 women, with a mean age of 35.7 ± 5.9 years (range, 22-46 years). There were 59 patients with pathologic tooth migration characterized by tooth elongation, tooth displacement, gingival bleeding, and loose teeth. The disease course of patients (from gingival bleeding and swelling to periodontal pocket formation, periodontal abscess, and loose teeth) was 12.5 ± 3.5 months (range, 6-18 months). According to the clinical attachment level of periodontitis, the patients were classified into 3 categories: mild (1-2 mm, n = 48), moderate (3-4 mm, n = 39), and severe (≥5 mm, n = 30). These 117 patients were randomly assigned to the basic group (receiving basic periodontic treatment, n = 58) and the combined group (receiving combined orthodontic-periodontic treatment, n = 59). The combined treatment group included all patients with pathologic tooth migration (38 men, 21 women; mean age, 36.5 ± 5.8 years) who received orthodontic treatment. The basic treatment group contained all patients without pathologic tooth migration (30 men 28 women; mean age, 34.8 ± 6.1 years). The general information of the patients in the 2 groups was not significantly different ( P >0.05), suggesting comparability. Inclusion criteria were the following: (1) all patients met the diagnostic criteria of periodontitis, with no more than 2 missing teeth ; (2) they did not receive periodontal treatment within at least 3 months and did not take any antibiotics or nonsteroidal anti-inflammatory drugs within 1 month; and (3) they did not use a mouthwash that contained antibacterial, antimicrobial, and anti-inflammatory drugs. Exclusion criteria were the following: (1) patients with poor compliance; (2) patients with systemic diseases, such as coronary heart disease, diabetes, chronic nephritis, and so on; (3) patients with severe mental disorders; (4) patients with severe liver and kidney dysfunctions; and (5) women in the gestation or lactation period, or with intended pregnancy during the treatment. In addition, 52 healthy people (29 men, 23 women; mean age, 36.8 ± 6.7 years) without periodontal disease were selected as the normal group. All subjects received primary prevention and regular scaling and were educated about the correct method of brushing teeth. These healthy people were matched with the patients in the combined and basic groups for sex and age.
Patients in the basic group were given basic periodontic treatment to remove local risk factors. The relevant knowledge of periodontal diseases, dos and don’ts in orthodontic treatment, precautionary measures, and the importance of oral hygiene were all introduced to the patients. The basic periodontic treatment was implemented to completely eliminate periodontal pathogenic factors. Their periodontal health was monitored, and regular tooth maintenance, supragingival scaling, subgingival scaling, and root planing were performed within 6 months. After basic periodontic treatment, periodontal flap surgery was further applied for patients with deep periodontal pockets caused by severe bone loss to completely eliminate the damaged periodontal tissue. The periodontal situation was reexamined after 3 months of treatment. Patients in the combined group continued to receive orthodontic-surgical treatment after the basic periodontic treatment. Functional and fixed appliances were used to maintain the elimination of occlusal trauma, relieve tooth crowding, and recover the esthetics and function of the teeth. Three months after the basic periodontic treatment, the periodontal situation was reexamined. The localized periodontal inflammation disappeared, and the alveolar bone resorption was static in the panoramic x-ray radiographs (dental panoramic x-ray machine; Weifang Newheek Medical Image Equipment, Weifang, Shandong, China). The morphologic features of the teeth of the orthodontic patients were observed with the assistance of cone-beam computed tomography (Changzhou Golden Dental Instrument & Medical, Changzhou, Jiang, China). Straight-wire appliances (Hangzhou ORJ Medical Instrument & Material, Hangzhou, China) were used with light forces to minimize periodontal tissue injuries. A reexamination of the periodontal parameters (probing depth, tooth mobility, plaque index, clinical attachement level, and sulcus bleeding index) was performed every 4 weeks after treatment, and tooth adjustments were implemented according to tooth mobility. If the periodontitis could not be relieved, supragingival scaling, subgingival scaling, or root planing were used to control the inflammatory response. The periodontal status was monitored, and regular periodontal care was conducted within 6 months. After the active orthodontic treatment, a vacuun-formed retainer was used to maintain the integrity of the teeth for a long time or permanently. The whole process of treatment was completed within 6 months.
Periodontal health examination was carried out with the Williams periodontal probe (Shanghai Dental Instrument Factory, Shanghai, China) before treatment and 4 weeks after treatment. Probing depth, tooth mobility, plaque index, clinical attachment level, and sulcus bleeding index were recorded by the same doctor (J.Z.). Probing depth was the distance from gingival margin to the gingival crevicular or periodontal pocket bottom; clinical attachemt level was the distance from the bottom of the periodontal pocket to the cementoenamel junction; sulcus bleeding index was classified into 6 degrees according to the bleeding index of Mazza et al and recorded with a range of 0 to 5 scores. The higher the score, the more severe the bleeding. Plaque index was classified into 4 degrees with reference to the plaque index of Silness and recorded with a range of 0 to 3 scores. The higher the score, the more severe the plaque. The periodontal status of the healthy people was determined with the same method after a medical examination. Subgingival irrigation of collagen gel with 2% chlorhexidine in the periodontal pockets was applied once a day for 4 weeks.
GCF was collected at the deepest periodontal pocket in each quadrant with the filter paper absorption method for all patients before treatment and after 6 and 18 months of treatment. We extracted 5 mL venous blood with supernatant after 5 minutes of centrifugation at the speed of 3000 revolutions per minute. The GCF and serum were stored in the refrigerator at −70°C. The double antibody sandwich ELISA was applied to detect the levels of high-sensitivity C-reactive protein, interleukin-1β, interleukin-5, interleukin-6, interleukin-8, tumor necrosis factor-α, and prostaglandin E2 in serum and GCF after all samples were collected with strict references of the kit instructions. Hs-CRP was detected with the high-sensitivity C-reactive protein test kit (Beckman Coulter, Irving, Tex) and implemented with a biochemical analysis by the Beckman special protein automated biochemical analyzer; the interleukin-1β, interleukin-5, interleukin-6, interleukin-8, tumor necrosis factor-α, and prostaglandin E2 test kits were provided by Jingmei Biotechnology (Beijing, China). The GCF and serum of the healthy people were also collected to measure the levels of those inflammatory cytokines.
All patients were followed for 2 years for postoperative relapse. They all were using the correct method of plaque control, including brushing and flossing. The patients’ follow-ups were mainly performed by outpatient services and telephone calls and were scheduled once every 6 months. The follow-ups, including periodontal relapse, occlusion, and tooth migration, started when the patients were discharged from the hospital and ended in June 2015. Relapse-free meant good periodontal maintenance with no obvious periodontal relapse, good maintenance of occlusion, and no tooth migration. Relapse meant tooth inflammation relapse, tooth migration, and changes in occlusal relationship.
Patient follow-ups were mainly performed by outpatient services and telephone calls. With a 3-year statistical period, follow-ups started when patients were discharged from the hospital and ended in January 2016, which included the general situation and relapse. The diagnosis method, recurrence time, and sites were recorded in detail. The life-table method was used to calculate the patients’ survival rate in each group.
Statistical analysis
SPSS statistical software (version 21.0; IBM, Armonk, NY) was used for data analysis. The measurement data were represented as mean ± standard deviation. The homogeneity test of variance was carried out before intragroup comparisons and comparisons between different groups. The t test was applied for homogeneity of variance, and the Wilcoxon rank sum test was performed for heterogeneity of variance. One-way analysis of variance was used to compare the experimental data among the groups. The enumeration data were detected by chi-square test and expressed as integers or percentages. P <0.05 was considered statistically significant.
Results
As shown in Table I , patients in the combined and basic groups were not significantly different in age, sex, education, smoking, drinking, tea or coffee drinking, betel nut chewing, and tooth cleaning frequency (all, P >0.05). The disease duration between the combined and basic groups was not statistically different ( P >0.05). However, there was a significant difference in the severity of periodontitis between the combined and basic groups ( P <0.05).
| Characteristic | Combined group (n = 59) | Basic group (n = 58) | Normal group (n = 52) | t/F / χ 2 | P |
|---|---|---|---|---|---|
| Age (y) | 36.5 ± 5.8 | 34.8 ± 6.1 | 33.9 ± 5.7 | 2.902 | 0.058 |
| Sex | 3.865 | 0.145 | |||
| Male | 38 | 30 | 36 | ||
| Female | 21 | 28 | 16 | ||
| Disease duration (mo) | 11.9 ± 3.6 | 13.1 ± 3.3 | – | 1.879 | 0.063 |
| Education | 9.173 | 0.164 | |||
| Primary school | 9 | 12 | 13 | ||
| Middle school | 15 | 21 | 18 | ||
| High school | 12 | 13 | 12 | ||
| University and above | 23 | 11 | 9 | ||
| Smoking history | 1.481 | 0.477 | |||
| Yes | 34 | 27 | 28 | ||
| No | 25 | 31 | 24 | ||
| Drinking history | 1.470 | 0.480 | |||
| Yes | 18 | 15 | 19 | ||
| No | 41 | 43 | 33 | ||
| Tea/coffee drinking habit | 2.191 | 0.334 | |||
| Yes | 27 | 19 | 22 | ||
| No | 32 | 39 | 39 | ||
| Betel nut chewing habit | 0.989 | 0.610 | |||
| Yes | 31 | 26 | 23 | ||
| No | 28 | 32 | 29 | ||
| Teeth cleaning frequency | 3.025 | 0.220 | |||
| <2 times/day | 8 | 14 | 7 | ||
| ≥2 times/day | 51 | 44 | 45 | ||
| Severity of disease | 6.342 | 0.042 | |||
| Mild | 18 | 31 | – | ||
| Modest | 25 | 16 | – | ||
| Severe | 16 | 11 | – |
After the 2-year follow-up of all patients, 50 were relapse-free (84.75%), and 9 had relapsed (15.25%) in the combined group. In the basic group, 39 were relapse-free (67.24%), and 19 had relapsed (32.76%). Compared with the basic group, the postoperative efficacy in the combined group was better, and a significant difference was found between the 2 groups ( P <0.05) ( Fig 1 ).
The periodontal parameters (probing depth, tooth mobility, plaque index, clinical attachment level, and sulcus bleeding index) of patients in the combined and basic groups were not significantly different before treatment (all, P >0.05) but were both higher than those in the normal group (all, P <0.05). Compared with the periodontal parameters before treatment, the indexes in the combined and basic groups were both significantly lower after 6 and 18 months of treatment (all, P <0.05). After 6 months of treatment, the periodontal parameters were significantly lower in the combined group than in the basic group (all, P <0.05), but the combined and basic groups were still higher than the normal group (all, P <0.05). After 18 months of treatment, the periodontal parameters in the combined group were all lower than those in the basic group (all, P <0.05) but were not significantly different from those in the normal group ( P >0.05) ( Table II ; Supplementary Fig 1 ).
| Parameter | Combined group | Basic group | Normal group | ||||
|---|---|---|---|---|---|---|---|
| Before | After 6 months | After 18 months | Before | After 6 months | After 18 months | ||
| Probing depth | 3.76 ± 0.56 ‡ | 2.58 ± 0.51 ∗ † ‡ | 1.72 ± 0.45 ∗ † | 3.55 ± 0.64 ‡ | 2.79 ± 0.57 † ‡ | 1.94 ± 0.53 † ‡ | 1.57 ± 0.41 |
| Tooth mobility | 0.57 ± 0.23 | 0.33 ± 0.12 ∗ † ‡ | 0.21 ± 0.09 ∗ † | 0.56 ± 0.19 ‡ | 0.40 ± 0.12 † ‡ | 0.29 ± 0.11 † ‡ | 0.18 ± 0.08 |
| Plaque index | 2.32 ± 0.63 ‡ | 0.64 ± 0.17 ∗ † ‡ | 0.26 ± 0.11 ∗ † | 2.45 ± 0.68 ‡ | 0.72 ± 0.19 † ‡ | 0.47 ± 0.14 † ‡ | 0.22 ± 0.11 |
| Clinical attachment level | 3.59 ± 0.94 ‡ | 1.93 ± 0.78 ∗ † ‡ | 0.45 ± 0.14 ∗ † | 3.47 ± 0.88 ‡ | 2.24 ± 0.82 † ‡ | 1.53 ± 0.35 † ‡ | 0.41 ± 0.10 |
| Sulcus bleeding index | 3.32 ± 0.51 ‡ | 2.24 ± 0.43 ∗ † ‡ | 1.06 ± 0.45 ∗ † | 3.26 ± 0.57 ‡ | 2.42 ± 0.50 † ‡ | 1.38 ± 0.46 † ‡ | 0.92 ± 0.35 |
∗ P <0.05 compared with the basic group.
As shown in Table III , GCF levels of inflammatory cytokines in the combined and basic groups were not significantly different before treatment (all, P >0.05) but higher than those in the normal group ( P <0.05). After 6 months of treatment, GCF levels of high-sensitivity C-reactive protein, interleukin-1β, interleukin-5, interleukin-6, interleukin-8, tumor necrosis factor-α, and prostaglandin E2 in the combined and basic groups decreased (all, P <0.05) but were still higher than those in the normal group, whereas GCF levels of these inflammatory cytokines in the combined group were lower than those in the basic group (all, P <0.05). After 18 months of treatment, GCF levels of those inflammatory cytokines in the combined group were significantly lower than those in the basic group (all, P <0.05) but not different from those in the normal group (all, P >0.05). GCF levels of inflammatory cytokines in the basic group decreased after 18 months of treatment but were still higher than those in the normal group ( P <0.05).
| Parameter | Combined group | Basic group | Normal group | ||||
|---|---|---|---|---|---|---|---|
| Before | After 6 months | After 18 months | Before | After 6 months | After 18 months | ||
| hs-CRP (mg/L) | 1.29 ± 0.74 ‡ | 0.48 ± 0.22 ∗ † ‡ | 0.35 ± 0.13 ∗ † | 1.26 ± 0.81 ‡ | 0.57 ± 0.26 † ‡ | 0.46 ± 0.13 † ‡ | 0.31 ± 0.12 |
| IL-1β (ng/L) | 57.27 ± 10.84 ‡ | 25.14 ± 6.73 ∗ † ‡ | 7.90 ± 1.15 ∗ † | 60.18 ± 11.36 ‡ | 31.25 ± 7.01 † ‡ | 9.37 ± 1.42 † ‡ | 7.50 ± 1.12 |
| IL-5 (ng/L) | 34.49 ± 6.92 ‡ | 21.35 ± 5.77 ∗ † ‡ | 16.49 ± 5.16 ∗ † | 34.72 ± 7.14 ‡ | 25.47 ± 5.52 † ‡ | 18.68 ± 5.29 † ‡ | 15.23 ± 4.51 |
| IL-6 (ng/L) | 4.19 ± 1.25 ‡ | 2.06 ± 0.95 ∗ † ‡ | 0.96 ± 0.36 ∗ † | 4.23 ± 1.33 ‡ | 2.44 ± 1.08 † ‡ | 1.09 ± 0.34 † ‡ | 0.84 ± 0.29 |
| IL-8 (ng/L) | 97.30 ± 21.76 ‡ | 72.49 ± 14.53 ∗ † ‡ | 50.13 ± 8.94 ∗ † | 105.48 ± 23.10 ‡ | 84.49 ± 16.25 † ‡ | 78.56 ± 11.45 † ‡ | 47.21 ± 7.64 |
| TNF-α (ng/L) | 5.45 ± 1.93 ‡ | 3.12 ± 1.43 ∗ † ‡ | 1.27 ± 0.55 ∗ † | 5.38 ± 1.97 ‡ | 3.76 ± 1.52 † ‡ | 1.53 ± 0.59 † ‡ | 1.08 ± 0.45 |
| PGE2 (ng/L) | 124.68 ± 25.43 ‡ | 85.61 ± 11.39 ∗ † ‡ | 71.10 ± 6.52 ∗ † | 115.77 ± 26.38 ‡ | 89.96 ± 12.15 † ‡ | 76.81 ± 7.69 † ‡ | 68.75 ± 6.14 |
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