Impact of Modifiable Risk Factors on Bone Loss During Periodontal Maintenance
The aim of this study was to analyze modifiable patient risk factors from dental chart histories and radiographs for progressive mild-moderate periodontitis during periodontal maintenance (PM). Bitewing radiographs of 442 elderly periodontal maintenance patients were taken before and after two years of periodontal maintenance. Each progressive periodontitis (PP) patient (with at least one site of posterior interproximal bone loss of ≥2 mm, n=71) was matched to a periodontitis stable (PS) patient (no sites with bone loss, n=71) of the same gender and age (±five years) to control for these variables and was compared for measurements of general patient (medical history, smoking, hygiene and compliance habits) and tooth-related (bone loss, overhangs, interproximal dimensions) factors at baseline. Fisher exact and t-tests were used to compare groups. While the elderly PM patients with mild-moderate periodontitis were generally stable, 71 of 442 were PP patients. No significant differences from PS patients were observed at baseline with regard to the systemic factors measured. However, the PP group had less cementoenamel junction to bone length (bone loss p<0.0001) and more interproximal width (2.3±1.0 mm) than did the PS group (1.7±0.6 mm, p=0.0016). This was reflected in more open sites without adjacent tooth contact in PP (42% vs 15%, p=0.0006). In the short term, systemic and behavior factors are of limited value in identifying mild-moderate periodontitis patients on PM at increased risk of bone loss. However, interproximal width and lack of adjacent tooth contacts are related to the likelihood of losing interproximal bone during periodontal maintenance, suggesting the need for restorative therapy.SUMMARY
Objectives:
Methods and Materials:
Results:
Conclusions:
INTRODUCTION
Periodontitis is the result of complex interrelationships between infectious agents in dental plaque and multiple host factors. Periodontal maintenance (PM) is an important part of periodontal treatment that includes procedures performed at different intervals to aid the periodontal patient in maintaining oral health.1-5 It has been shown6,7 that periodontal treatment followed by long-term maintenance is successful in the preservation of the majority of patients' teeth. Most patients with milder forms of periodontitis are managed in general practices on four to six-month intervals, with the expectation that all sites will remain periodontally stable (no bone loss).8 However, following the current population in a dental school setting for two years on PM revealed that 16% of patients had at least one site with ≥2 mm of interproximal bone loss.
The predictability of PM may be associated with diverse conditions, especially when a patient is exposed to one or more risk factors known to influence host response.7,9 There is evidence that age, gender, smoking, compliance with recalls, and systemic diseases such as diabetes mellitus and osteoporosis may affect the results achieved through periodontal therapy.2,4,9-13 Meanwhile, studies10,11,14,15 have also shown that different tooth-related factors are associated with the long-term stability of periodontal maintenance. Clinical parameters such as pocket depth, bleeding on probing, attachment loss, and tooth mobility are recorded during periodontal maintenance to measure the periodontal condition of patients.2,16 However, other tooth-related factors that might affect the long-term outcome of periodontal maintenance are not commonly recorded or corrected.17-19
Bitewing radiographs (BWs) are routinely obtained during PM, and radiographic bone loss is an objective measurement and an important indicator of progressive periodontitis. Maintaining stable bone levels is one of the major goals of periodontal maintenance.20,21 Other measurements that can be easily obtained from BWs also may be important prognostic indicators. However, to our knowledge, the relationship between different radiographic tooth-related factors and alveolar bone loss in PM patients has not been thoroughly studied. It is still controversial which tooth-related factors are predictive for bone loss during PM; specifically, whether the specific measurements of the anatomy of interproximal areas, such as interproximal width, restoration overhangs, baseline bone loss, and lack of contact, are associated with the increased likelihood of subsequent crestal bone loss during PM.
The aim of this research was to compare prominent modifiable systemic patient and tooth-related factors identifiable on chart histories and radiographs in groups of mild/moderate periodontitis patients who had either shown posterior interproximal periodontitis stability or progressive periodontal bone loss during PM. The results may help dentists develop more reliable prognoses and treatment options for PM patients.
METHODS AND MATERIALS
Four hundred forty-two patients over age 45 (to eliminate aggressive periodontitis) participating in the University of Nebraska Medical Center College of Dentistry periodontal maintenance program with at least two years of regular PM therapy were chosen as subjects under an institutional review board protocol (IRB 015-14). All patients received a standard protocol of BWs, periodontal probing, oral hygiene instructions, and scaling/root planing during PM. Since all providers were not calibrated for probing measurements, bone loss on radiographs was used to determine progressive periodontitis. Guidelines conformed to the Code of Ethics of the World Medical Association (Declaration of Helsinki). Patients were deidentified, and posterior digital BWs before (baseline) and after the two-year PM period (two-year follow-up) were measured at all posterior interproximal sites (premolar and molar) from the cementoenamel junction (CEJ) or restoration margin to the crestal bone where the periodontal ligament space became uniform. A ruler tool (MiPACS Dental Enterprice Solution, Medicor Imaging, Microtek, Hsinchu, Taiwan) was used to make the linear measurements separately by two examiners masked to patient identity. The progressive periodontitis (PP) patients were defined as having at least one site of posterior interproximal bone loss measuring ≥2 mm between baseline and two-year follow-up on BWs. The 2-mm threshold was chosen to reflect a clinically relevant change that could be detected on non-standardized radiographs taken in clinical practice.22 The periodontitis stable (PS) group was defined as having all sites with posterior interproximal bone change measuring <2 mm between baseline and two-year follow-up on BWs, and PS patients were paired to a PP by age (±five years) and gender to control for these variables. Ten percent of patients were remeasured at baseline and two-year follow-up by the same examiners in order to determine the reliability of measurements in this study.
Medical and dental history questionnaires at baseline were used to obtain general systemic and behavioral risk factors previously associated with periodontitis, as follows:
-
Systemic conditions from medical history: diabetes mellitus, osteoporosis, rheumatoid arthritis;
-
Smoking: Current smoker, former smoker, or never smoker;
-
Awareness of periodontal and oral disease: loose teeth, food or floss caught between teeth, diagnosed with gum disease, treated for gum disease, gums bleed when brushed, and dry mouth;
-
Oral hygiene habits: brushing frequency per week and flossing frequency per week; and
-
Compliance with periodontal recalls: numbers of maintenance appointments within two years and average visits per year for two years.
Tooth-related factors were measured at baseline in posterior sites with bone loss of ≥2 mm in the PP group and were matched to a similar interproximal location (eg, molar-molar, molar-premolar) in the paired PS patient. The tooth-related factors measured were as follows:
-
CEJ to alveolar crest length;
-
Presence or absence of adjacent tooth contact;
-
Overhanging restorations of >1 mm;
-
Interproximal contact to alveolar crest length;
-
Width of interproximal (ITP) embrasure: measured from CEJ to adjacent CEJ; and
-
CEJ to CEJ angle relative to long axis of the tooth (horizontal CEJ-CEJ=90° angle).
Baseline severity of periodontitis of study sites and of overall posterior sites were calculated according to bone loss of the site, where normal = 0 to 2 mm CEJ to alveolar crest on BW, mild = 2 to 4 mm, moderate = 4 to 6 mm, and severe = more than 6 mm.
Comparisons of categorical factors between PP and PS groups were conducted with Fisher exact tests. Comparisons of continuous factors between PP and PS groups were conducted with t-tests. p-Values of less than 0.05 were considered to be statistically significant. SAS software version 9.4 was used for analysis (SAS Institute Inc, Cary, NC, USA). Single-measures intraclass correlations (ICCs) for absolute agreement were calculated using a two-way mixed-effects model for each of the examiners, at each of the time points, using SPSS software, version 23 (IBM Corp, Armonk, NY, USA). ICCs ranged from 0.663 to 0.881. According to Cicchetti,23 the clinical significance values of ICCs between 0.60 and 0.74 and between 0.75 and 1.00 are “good” and “excellent,” respectively.
RESULTS
Each group had 71 subjects after identification of PP patients and matching to a PS patient and interproximal location. Demographic characteristics of the subjects are presented in Table 1. No significant differences were observed since patient and control groups were matched by gender and age. The mean age in the lower 70s with mild-moderate periodontitis indicates a patient population with a slow rate of bone loss in whom an episode of clinically significant bone loss might define high-impact risk factors.

Common systemic or behavioral risk factors for PP and PS groups at baseline are presented in Table 2. In general, no significant differences were observed with regard to systemic conditions, smoking, awareness of periodontal and oral disease, oral hygiene habits, and compliance with periodontal recalls. There was a trend toward more PP in diabetic patients (p=0.13).

The tooth-related factors of PP and PS groups at baseline are presented in Table 3, Figure 1. While local plaque control and instrumentation are the cornerstones of effective PM, several other local factors were significantly different between the two groups. At baseline, mean CEJ to alveolar crest length of the PP site was 1.9 ± 1.3 mm, while CEJ to alveolar crest length of the PS site was 3.0 ± 1.6 mm (p<0.0001). This indicated normal bone height (56% of cases) in PP and early bone loss in PS (54%, p=0.001). Therefore, past periodontitis was not a risk factor in future bone loss in these mild-moderate periodontitis patients on PM. As for baseline severity of periodontitis of overall posterior sites, the results did not show a statistically significant difference between the two groups. The baseline embrasure width from CEJ to adjacent CEJ of the PP group was wider (2.3±1.0 mm) than for the PS group (1.7±0.6 mm, p=0.0016). This was reflected in more sites without adjacent tooth contacts in PP (42% vs 15%, p=0.0006), but not in tipped teeth (CEJ-CEJ angle in PP sites=91.5°±34.5° compared to PS sites=97.9°±32.1°, p=0.31; Table 3). To further focus on tooth-related factors, major systemic risk factors were removed from the analysis, with results described in Table 4. Significant findings for baseline CEJ to bone, CEJ to CEJ width, and lack of contact remained after eliminating patients with diabetes, osteoporosis, rheumatoid arthritis, or current smoking habit.




Citation: Operative Dentistry 44, 3; 10.2341/18-041-C

The interproximal anatomy in progressive periodontitis sites was additionally characterized in Table 5, Figure 2. Amount of open contact was evenly distributed between those with <2 mm (food impaction) and those with >4 mm (self-cleansing). The most common restoration was cast crown, similar in incidence to no restoration. The incidences of opposing plunger cusps and overhanging restorations were rare. There were slightly more PP sites in the maxilla.




Citation: Operative Dentistry 44, 3; 10.2341/18-041-C
DISCUSSION
At baseline, the majority of patients in each group had mild chronic periodontitis, according to the diagnostic standard used in this study. All of the subjects had finished initial periodontal therapy and had gone into PM. While these patients with mild-moderate periodontitis on PM were generally stable, 16% of the patients followed in this study showed at least one site with ≥2 mm of interproximal bone loss. Periodontal maintenance has been proven24 effective in minimizing long-term tooth loss and controlling disease progression and relapse in patients with chronic periodontitis. However, even within compliant periodontal maintenance patients, disease progression still cannot be completely stopped.25 While results indicated that regular PM allowed for stable and relatively normal interproximal bone levels, even mild-moderate periodontitis patients on PM should be followed closely for evidence of bone loss, and risk factors associated with this event should be considered.
Common systemic and behavioral risk factors among PM patients that have been reported26-31 to be associated with progression of periodontal diseases appeared to show less impact on PP and PS groups than did local factors in the two-year follow-up period. However, there was a trend toward more PP in diabetic patients (p=0.13). Previous studies28,32 have supported that poorly controlled diabetes acts as a risk factor in development of periodontitis and that long-term periodontal care provided in a clinical setting improves long-term glycemic control among individuals with type 2 diabetes. Working with the patient's physician may also modify glycemic control to reduce this risk factor. Unfortunately, most health questionnaires usually contain no information of hemoglobin A1C levels. This study reinforces that large populations with hemoglobin A1C information are needed to fully assess the impact of diabetes on mild-moderate periodontitis patients on PM.
It was interesting to notice that in our study more than 40% of patients at baseline did not realize that they had gum disease. This may reflect insufficient previous patient education. With a better understanding about their periodontal diseases, they may have better home care and compliance.
Currently, there are several risk factor assessment tools for the prevention of periodontitis progression based on long-term analysis. The majority of the tools are variations of a few basic approaches, in particular of the Periodontal Risk Calculator, PRC,33 and of the Periodontal Risk Assessment, PRA,34 using bone loss as one major parameter. The previous studies mainly focused on moderate to severe periodontitis patients. Our findings indicated that for mild chronic periodontitis patients, bone loss and initial periodontitis severity may not be able to predict future bone loss and short-term progression of disease. Previous tools also used systemic risk factors and local soft-tissue measurements, but interproximal anatomy, as in Tables 3 through 5, was not analyzed.
Width of interproximal embrasure was wider in PP at baseline than in PS. Wider ITP may be caused by tipped teeth or open spaces between the studied tooth and adjacent tooth. Our results indicated that lack of interproximal contacts (open contact or missing tooth) played a larger role than did tipped teeth. This was true when patients with other major systemic risk factors (diabetes, osteoporosis, rheumatoid arthritis, and smoking) were removed from the analyses (Table 4). Further characterization of the interproximal anatomy of progressive periodontitis sites (Table 5) indicated that open contact that could promote food impactions (<2 mm) and those which were likely self-cleansing (>4 mm) were evenly distributed, suggesting that even wide-open interproximal areas would benefit from tooth replacement to help prevent interproximal periodontal bone loss.
Two-thirds of teeth in PP sites had restorations, most commonly cast crowns. However, horizontal overhangs were rare, especially large ones, which have been shown35 to contribute to periodontal bone loss. Likewise, the low incidence of plunger cusps did not seem to contribute to interproximal bone loss.
The relatively short period of follow up and the small sample size were limitations of our study, particularly in terms of analysis of systemic risk factors. However, interproximal periodontal anatomy easily measured on BWs showed highly significant difference in PP sites and suggests some restorative treatments to change the risk profile.
CONCLUSIONS
While PM patients with mild-moderate periodontitis are generally stable, they still should be followed closely for evidence of bone loss. Lack of interproximal contacts is related to the likelihood of losing interproximal bone during periodontal maintenance, suggesting the need for restorative therapy.

Measurements for tooth-related factors. (A) CEJ to alveolar crest length; (B) Presence or absence of adjacent tooth contact; (C) Horizontal overhanging restorations of >0.25 mm; (D) Interproximal contact to alveolar crest length; (E) Width of CEJ to CEJ; and (F) CEJ to CEJ angle relative to long axis of the tooth.

Interproximal radiographic anatomy. Top panel shows molar-molar open interproximal contact and bone loss on #30 distal between baseline (A) and two years of periodontal maintenance (B). Bottom panel shows molar-molar contact and minimal molar interproximal bone change between baseline (C) and two years of periodontal maintenance (D).
Contributor Notes