Type 1 diabetes and periodontal disease: a literature review

Abstract

Objective:

This narrative review examines the literature on type 1 diabetes mellitus (T1DM) and periodontitis pathogenesis, seeking to determine the effectiveness of periodontal therapy in improving glycemic control in individuals with T1DM.

Methods:

A detailed search of the literature was conducted in the following electronic databases: PubMed, Google Scholar, Scopus, and Cochrane Library. Inclusion criteria were systematic reviews with meta-analyses published between 2015 and 2020, and human peer-reviewed clinical trials addressing the effectiveness of periodontal treatment on glycemic control in individuals with T1DM published between 1995 and 2020.

Results:

The search retrieved 3 systematic reviews and 9 original research papers that included 10 clinical studies.

Discussion:

Three systematic reviews on T1DM and periodontal disease suggested that individuals with T1DM have more features of periodontitis than healthy subjects, although long-term data are scarce. Nine of the ten clinical studies showed no impact on glycemic control in individuals with T1DM, while 1 study reported improvement.

Conclusion:

The selected literature lacked data on long term assessment and adequate randomization with controls. The data perused did not provide sufficient evidence to determine the effectiveness of periodontal therapy in improving glycemic control in type 1 diabetes or to suggest that T1DM is a risk factor for periodontal disease.

PRACTICAL IMPLICATIONS OF THIS RESEARCH.

• The prevalence of periodontal disease is higher in individuals with T1DM than in healthy individuals.

• The clinical features of periodontal disease in T1DM resemble those of T2DM.

• Non-surgical periodontal treatment improves the periodontal parameters in clients with T1DM but with little effect on glycemic control.

BACKGROUND

Type 1 diabetes mellitus (T1DM), previously referred to as “juvenile diabetes” and “insulin-dependent diabetes,” is a chronic autoimmune condition. Hyperglycemia is a consistent manifestation associated with insulin deficiency attributed to pancreatic β-cell destruction. ¹ The prevalence of T1DM in children and youth in Canada has increased from 1790 individuals in 2002-2003 to 2264 individuals in 2012-2013. ² The condition has been associated with a genetic predisposition of human leukocyte antigen (HLA) with class 2 genes and a deficiency of vitamin D. ³

It is of interest that periodontal disease has been considered a complication of diabetes mellitus since 1993. ⁴ Periodontal disease poses a threat to the tooth-supporting structures through a microbial and immune-mediated inflammatory challenge. Several mechanisms explain the association between diabetes and periodontal status, such as alterations in the host's vascular, cellular, and repair processes. ⁵ The duration of hyperglycemia and its severity are the prime risk factors for the development of diabetes complications. ⁶ Diabetes presents with common oral manifestations such as salivary gland enlargement, xerostomia, burning mouth syndrome due to oral candidiasis and lichen planus. Furthermore, an increase in the severity of gingivitis and tooth loss have been documented. ⁵

The evidence indicates that periodontitis adversely affects glycemic control and worsens complications of both T1DM and type 2 diabetes mellitus (T2DM). ⁷ Much of the literature explores the relationship between T2DM and periodontal disease, due to the greater prevalence of T2DM, ⁸ while evidence on T1DM is scarce.

The reports evaluating the relationship between T1DM and periodontal health have been inconsistent. The available data hint that treating periodontitis improves glycemic control in T2DM, while similar data on T1DM are lacking. Hence, the present review appraised the literature evaluating the effects of T1DM on periodontal disease and explored the effectiveness of periodontal therapy on glycemic control in individuals with T1DM.

METHODOLOGY

The focused questions for this review were “What are the effects of T1DM on periodontal disease?” and “Does periodontal therapy improve glycemic control in individuals with T1DM and periodontitis?”

Effect of type 1 diabetes on periodontal disease

A detailed search of the following electronic databases was conducted: PubMed, Google Scholar, Scopus, and Cochrane Library. The keywords used for this search were type 1 diabetes, periodontitis, periodontal therapy, insulin-dependent diabetes mellitus, and non-surgical periodontal therapy. The inclusion criteria were “systematic review and meta-analysis” published between January 2015 and December 2020. Only those systematic reviews and meta-analyses reporting the impact of T1DM on periodontal disease were included. Three systematic reviews met the inclusion criteria for the appraisal.

Periodontal treatment effects on glycemic control in individuals with type 1 diabetes

The electronic databases of PubMed, Google Scholar, Scopus, and the Cochrane Library were searched. The keywords used for the search were type 1 diabetes, periodontitis, periodontal therapy, insulin-dependent diabetes mellitus, and non-surgical periodontal therapy. The inclusion criterion was “human clinical studies” published between January 1995 and September 2020. Only clinical trials evaluating the effectiveness of periodontal therapy on glycemic control in individuals with T1DM were included. Case reports and case series were excluded from the review. From a total of 214 titles and abstracts, 20 potentially relevant articles were identified, from which 9 original articles (reporting 10 clinical studies) with 396 participants met the inclusion criteria and were reviewed.

RESULTS

Effect of type 1 diabetes on periodontal disease

Three systematic reviews on the subject, which suggested that T1DM was a risk factor for the onset of periodontal disease, were selected for analysis (Table 1).

In the systematic review by Ismail et al. ⁹ 26 case-control and 3 longitudinal studies evaluated periodontal health in children, ages 16 and younger, with T1DM. The authors observed heterogeneity in the study parameters. Most studies documented oral hygiene status; Siudikiene et al. ²⁰ found good oral hygiene in 61% of children with T1DM, while Alavi et al. ²¹ found that 38% of children had poor oral hygiene. Of the 2 studies using the,Simplified Oral Hygiene Index, Rai et al. ²² found higher scores in children with T1DM, indicating poor oral hygiene. Dental plaque was assessed as a parameter in only 8 of 21 studies, with higher plaque scores in children with T1DM than the control group, ^23-30 while one study showed more plaque in the non-diabetic group. ²⁰ Three of nine studies ^23,29,30 demonstrated higher gingival bleeding parameters in children with T1DM. Ten of sixteen studies reported significantly higher gingival index (GI) scores in subjects with T1DM when compared to the controls. However, long term assessment showed no differences in the plaque and gingival indices in a 3 year follow up by Sbordone et al. ³¹ and a 5-year follow-up by Firatli et al. ³² Four studies ^20,23,33,34 showed more significant deposits of calculus in children with T1DM, while one study ²⁶ reported no significant difference between the groups. Periodontal index scores were higher among children with T1DM in the study by Luczaj-Cepowicz et al. ³³ However, Siudikiene et al. ²⁰ found no such differences. Clinical attachment loss, reported in only one study, by Firatli et al. ³² was more significant in those with type 1 diabetes. Hence, the systematic review by Ismail et al. found that individuals with T1DM had poorer periodontal health with higher plaque accumulation compared to healthy individuals. Furthermore, those with uncontrolled diabetes had poorer periodontal health (Table 1).

A systematic review and meta-analysis by Jensen et al. ¹⁰ included 23 articles that assessed periodontal disease markers such as plaque index (PI) (20 articles), gingival index (GI) (18 articles), bleeding on probing (BOP) (12 articles), pocket depth (PD) (8 articles), and clinical attachment level (CAL) (7 articles). Most studies showed higher plaque scores in children with T1DM except those of Duque et al. ³⁵ and Rafatjou et al. ³⁶ Similarly, 16 of the reviewed studies found higher GI in T1DM children, but 2 studies by Duque et al. ³⁵ and Ismail et al. ³⁷ stated otherwise. Ten of the twelve studies showed significantly higher BOP in T1DM children. Of the 8 studies assessing pocket depths, 5 studies reported higher PD in T1DM subjects. Among the 7 studies that assessed CAL, 3 showed more significant CAL loss in subjects with diabetes than controls, while only one study reported a higher value for the control group. This systematic review surmised that, in subjects with T1DM, the risk markers for periodontal disease present greater severity ¹⁰ (Table 1). However, many of the studies were cross-sectional and did not consider confounders such as the duration of diabetes.

Table 1.

Systematic reviews of comparisons of T1DM effects on periodontal disease

	Reference	Databases	Data search	Number of studies	Outcome measuresa	Conclusion
1	Ismail et al. 20159	PubMed/MEDLINE, Web of Knowledge, SCOPUS, and EMBASE.	Up to January 2014	37	PI, GI, BOP, CAL	Children with T1DM had poorer periodontal health, with higher plaque accumulation, when compared to healthy children
2	Jensen et al. 202110	PubMed and EMBASE	Up to February 2019	23	PI, GI, BOP, PD, CAL	T1DM children more likely to have higher PI, GI, BOP, PD, and CAL compared to healthy children
3	Dicembrini et al. 20208	MEDLINE, Cochrane Central Register of Trials and EMBASE	Up to October 31, 2019	11	Primary outcome: the prevalence of periodontal disease; Secondary outcome: CAL	High prevalence of periodontitis, deeper CAL; T1DM could be a risk factor for periodontitis

^aPI: Plaque Index; GI: Gingival Index; BOP: bleeding on probing; CAL: clinical attachment level; PD: pocket depth

Another systematic review by Dicembrini et al. ⁸ examined 19 articles that assessed the prevalence of periodontal disease and periodontal destruction in individuals with T1DM compared to the general population. Of these, 11 studies (8 were cross-sectional studies, 2 were cohort studies, and 1 was a retrospective study) with 5888 T1DM subjects revealed that the prevalence of periodontal disease was 18.5% among subjects with T1DM. The risk of periodontal disease in subjects with T1DM versus the general population was assessed in 5 studies (4 cross-sectional studies and 1 retrospective analysis) with 172 individuals, which revealed that the number of subjects with T1DM and periodontitis was more than twice the number of subjects without T1DM. The prevalence of more significant periodontitis in individuals with T1DM suggests that this group could be at a higher risk for the progression of periodontitis. A relatively severe form of periodontal disease is apparent in those with uncontrolled T1DM compared to those with controlled T1DM (Table 1). ⁸ The authors of this systematic review concluded, however, that there was insufficient evidence to illustrate a cause-effect relationship between T1DM and periodontitis.

Periodontal treatment effects on glycemic control in individuals with T1DM

Ten studies were selected for the review process (Table 2), with only 4 being randomized controlled clinical trials. ^11,15,16 Two studies ^13,14 included individuals with T1DM or T2DM, while another study compared T1DM and T2DM. One study used local drug delivery—Arestin^® (minocycline microspheres) ¹⁵ —while 2 studies administered systemic antibiotics after scaling and root planing. ^16,19 It may be noted that the test groups received non-surgical periodontal therapy in all the studies followed by supportive periodontal therapy.

Aldridge et al. ¹¹ conducted 2 single-blinded controlled trials, which reported the effect of periodontal therapy on metabolic control. In their first study on subjects with T1DM and shallow probing depths (<5 mm), similar mean scores were noted for the treatment and no-treatment groups. While the treatment group received dental hygiene therapy (brushing, scaling, and flossing) and oral hygiene reinforcement, the concurrent oral hygiene improvement in the non-treated controls was attributed to a “Hawthorne effect,” as the subjects were well aware of the need for regular self-care. The association between glycated hemoglobin (Hb) and periodontal parameters was collectively assessed for the 2 groups. There were no differences in the metabolic control between the groups at the different time intervals. Gingival bleeding seemed to be the only periodontal parameter correlating with change in metabolic control. Further correlation suggested that the change in glycated Hb was associated with the number of bleeding sites at follow up. ¹¹ It may be noted that the recruited subjects with T1DM were between the ages of 16 and 40 years, with no complications, and were followed up for 6 months.

Aldridge et al. ¹¹ conducted another study over 8 months in individuals with advanced periodontitis in fewer than 5 sites, with reasonable metabolic control, and in the broader age range of 20 years to 60 years, to remove the Hawthorne effect and examiner bias. In this second study, there was a marked improvement in all aspects of periodontal health in the treatment group compared to controls, but with no significant effects on metabolic control, assessed by glycated Hb. However, in this study, there was little correlation found between bleeding and glycated Hb. ¹¹

These studies indicate that reducing periodontal inflammation has no significant effect on metabolic control in individuals with T1DM and stable metabolic control. Therefore, adequate metabolic control is a significant factor influencing periodontal treatment effects.

Smith et al. ¹² measured HbAlc values before and after 2 months of periodontal treatment, evaluating clinical, biochemical, and microbiological profiles of subjects with diabetes. While the periodontal status and biochemical marker, aspartate aminotransferase (AST), improved modestly, there was no difference in glycated Hb levels before and after treatment. The microbial profile did not reflect changes in improved periodontal health. Elevated antibody titres indicated the persistence of infection, which suggested susceptibility to future periodontal breakdown despite the clinical improvement. Hence, the authors opined that the obtained improvement following periodontal treatment might be short lived and adjunctive therapy was warranted in individuals with diabetes. The subjects in the study had long-standing diabetes for an average of 17 years. The authors found no correlation between duration of diabetes and HbA1c, gingival index, probing depth or attachment levels or the inflammatory marker, AST. AST was in the higher range post-treatment in a few subjects, suggesting increased risk for periodontal disease activity. The data on subjects without diabetes from previous publications were used as controls. In addition, smokers were also part of the experimental group. ¹²

Westfelt et al. ¹³ compared the frequency of recurrence of periodontal disease in individuals with T1DM and T2DM, to the frequency among individuals without diabetes, following non-surgical and surgical therapy, as needed,, along with maintenance recall every 3 months, for 5 years. HbA1c did not show much improvement in the diabetes group when observed either between baseline and 24 months or between 24 and 60 months. At the end of the study period, the 2 groups showed similar improvements in periodontal parameters and recurrence of disease. The authors observed no correlation between glycated Hb and changes in periodontal parameters. However, smokers were not excluded from this study. Therefore, in this longitudinal study, effective maintenance therapy was a significant factor in response to treatment despite the presence of underlying systemic disease or habits. The authors suggest that individuals with diabetes may be comparable in treatment response to those without diabetes if they are on a regular plaque-control program. ¹³

Christgau et al. ¹⁴ compared subjects with diabetes (both T1DM and T2DM) and healthy subjects over 4 months. There were no specific periodontal pathogens dominant in the subjects with diabetes before non-surgical therapy. The changes observed post scaling and subgingival debridement in terms of plaque and gingival bleeding indices, reduction in pocket depth and probing attachment levels, and subgingival bacterial load were not significantly different for either healthy subjects or those with diabetes. The oxidative burst function of those with diabetes and those without diabetes was also similar. Periodontal treatment showed little effect on glycated hemoglobin, the acute phase proteins, fibrinogen, and leukocyte numbers in the subjects with diabetes. The subjects in this study had reasonable long-term metabolic control, which explained the comparable healing to healthy subjects without diabetes. ¹⁴ However, the study did not attempt to differentiate between T1DM and T2DM.

Skaleric et al. ¹⁵ was the first study to locally administer Arestin^® as an adjunct to scaling and root planing. The drug was placed into pockets ≥5 mm. Local delivery proved effective in reducing probing depths and providing a gain in CAL compared to scaling and root planing alone in individuals with T1DM. HbA1c was also reduced in all subjects, though the difference between the test and control groups was not significant and most likely attributable to the small sample size (20) or complete dependence of T1DM subjects on insulin. ¹⁵ It may be noted that the participants in the Skaleric study were exclusively those with poorly controlled type 1 diabetes (HbA1c ≥ 9%), with almost one-fourth having diabetes for more than 5 years.,Periodontal treatment of subjects with T1DM, with or without concomitant systemic administration of doxycycline (100 mg/day for 15 days) showed minimal effects on glycated Hb levels in a study by Llambés et al. ¹⁶ Although there was a good response to the periodontal treatment at 3 months, the effects on glycemic control were not apparent. Furthermore, HbA1c did not show any changes in individuals with the best periodontal response or the worst metabolic control. Insulin dose, diet, and exercise were suggested to be influential in the responses of these study subjects. ¹⁶

Similarly, Tervonen et al. ¹⁷ noted improvement in the number of bleeding sites and probing depths in a study on 65 individuals with T1DM, who were administered systemic antibiotics in conjunction with periodontal treatment (non-surgical and/or surgical). The 8 month-long duration of the study allowed effective resolution of periodontal infection but with no significant effects on glycemic control. The mean HbA1c of 8.6% before treatment reduced to 8.5% post-treatment. Individual response to periodontal treatment varied, with glycemic control improving in some and worsening in others. The clinical improvement is significant considering that the study participants had a mean duration of diabetes of 20.1 years. ¹⁷

Buzinin et al. ¹⁸ observed no improvement in periodontal parameters and HbA1c levels in their study during a 3 -month follow-up of non-surgical periodontal treatment in 20 individuals with T1DM compared with 20 individuals with chronic periodontitis. Specific microorganisms were reduced post-treatment in subjects with and without diabetes. They noticed no differences in the glycemic control of the included ethnic groups of Malay, Chinese and Indians following periodontal treatment. They attributed the inability to detect HbA1c changes to the small sample size of the study. ¹⁸

In contrast to the previous studies, Lopes et al. ¹⁹ noted better glycemic control in individuals with T1DM than those with T2DM 6 months after primary periodontal treatment. This correlated with the more significant reduction of plaque levels and expression of Prostaglandin E2 (PGE2). They opined that treatment of T2DM depends mainly on each person's efforts, such as lifestyle changes, and therefore may account for the difference in treatment response in the 2 forms of diabetes. There were fewer subjects with T1DM (n = 14) in this study compared to T2DM (n = 27) and healthy (n = 11) controls. ¹⁹

DISCUSSION

Effect of type 1 diabetes mellitus on periodontal disease

Research has focused mainly on T2DM and its effects on periodontal disease. It is, therefore, important to assess the effects of T1DM and recognize any differences in clinical presentation from those of T2DM.

Ismail et al. ⁹ in their systematic review of 37 studies that included individuals between the ages of 3 and 18 years, noted that the indices most used were the periodontal index and the gingival index. However, given that there are a variety of indices available in both categories, there were considerable differences among the chosen indices, making comparisons among studies difficult. With heterogeneity present in most observational studies, and inclusion of only 3 longitudinal studies, the results were questionable. Nevertheless, children with T1DM tended to have more significant plaque accumulation with higher gingival indices, although longitudinal studies did not show such differences. Longitudinal assessments showed oral hygiene scores worsened to a similar extent in children with diabetes and healthy controls. In the diabetes group, the poorer scores were attributed to impairment of saliva secretion, which prolongs the oral clearance. However, another longitudinal study included in this systematic review indicated significant attachment loss, which was related to the duration of diabetes. ⁹ Despite the mixed results, this systematic review included studies from different geographic locations, potentially supporting the generalizability of the results.

The systematic review by Jensen et al. ¹⁰ addressed differences in risk markers of periodontal tissue inflammation and periodontal disease such as plaque, gingivitis, BOP, PD, and CAL among children and adolescents with T1DM compared to healthy controls. The review reported that subjects with T1DM had greater severity of the periodontal risk markers than healthy individuals. ¹⁰ However, the review considered only studies in English, which were primarily cross-sectional in design, with considerable heterogeneity among studies. Hence, the temporal relationship between the duration of T1DM or glycemic control and periodontal risk markers could not be established.

Dicembrini et al. ⁸ in their systematic review, observed twice the number of subjects with T1DM affected by periodontitis compared to those without diabetes, providing more evidence that T1DM could be a likely risk factor for developing periodontal disease. They found a higher prevalence of periodontitis (18%) and greater CAL in T1DM subjects with poor glycemic control (HbA1c > 7%). ⁸ However, most of the studies were cross-sectional with only 3 cohort studies and one case-control study. Additionally, heterogeneity among the reported studies was attributed mainly to differences in diagnostic criteria and procedures.

The reviews by Jensen et al. ¹⁰ and by Dicembrini et al. ⁸ were further subjected to a meta-analysis, while Ismail et al. ⁹ conducted a systematic review only. The focus of research, in general, has been on comparing periodontitis in individuals with T1DM and healthy individuals, with scarce reporting of differences in periodontal disease presentation between individuals with T1DM or T2DM. Greater plaque, gingivitis, PD, and CAL was noted in most studies on T1DM. However, longitudinal studies were few and did not always corroborate these findings. The evidence, therefore, to suggest T1DM as a risk factor for periodontitis is weak. The periodontal disease manifestation in T1DM appears to be similar to that in individuals with T2DM but of greater severity. ³⁸ Although these 2 types of diabetes differ in their pathogenesis, the presence of high blood glucose levels in the 2 conditions will determine the clinical effects on local tissues. ³⁹

Periodontal treatment effects on glycemic control in individuals with type 1 diabetes mellitus

Diabetes and periodontitis appear to have a bidirectional relationship. Periodontitis connects with T1DM through the shared mechanism of inflammation, periodontal bacteremia, and the systemic response to distant low-grade infection. ⁴⁰

Improved metabolic control may lead to improved periodontal health, but it is still unclear whether diabetic control improves following periodontal treatment. A meta-analysis on 10 studies by Janket et al. ⁴¹ suggested that periodontal treatment has a greater effect on HbA1c in individuals with T2DM than in those with T1DM. Very few studies report treatments in individuals with T1DM, perhaps due to the higher incidence of T2DM in the population, which would make recruitment of subjects with T1DM difficult. ¹⁷ The present review focuses on the impact of periodontal treatment on glycemic control of individuals with T1DM as determined by glycated hemoglobin levels.

In the first study by Aldridge et al. ¹¹ , the test and control groups had similar baseline mean scores for all metabolic and periodontal parameters. During the follow-up, improvement of periodontal parameters was evident in both groups (p < 0.05), with no change in metabolic control. The second study by Aldridge et al. ¹¹ was consistent, showing improvements in periodontal parameters only, but not glycated Hb. The longitudinal study by Westfelt et al. ¹³ reported that mean values of glycated Hb between baseline and 24 months did not differ significantly from those between 24 and 60 months (Table 2).

Some authors have also noted poor metabolic control despite periodontal therapy. For example, Smith et al. ¹² observed a slight increase in the mean standardized glycated Hb from 8.18% before therapy to 8.28% after therapy, which is neither statistically nor clinically significant. In 11 of 18 study subjects, the HbA1c remained the same or increased 2 months after therapy. The short duration of 2 months resulted in clinical improvement, but biochemical parameters such as aspartate aminotransferase (AST)suggested the persistence of disease activity. ¹² Similarly, Christgau et al. ¹⁴ reported a slight increase in glycated Hb levels from 6.5% to 6.7% from baseline to 4 months following periodontal therapy, which was not statistically significant (Table 2).

Reports by the other authors have suggested a marginal beneficial impact on glycated Hb. Tervonen et al. ¹⁷ reported a reduction in mean glycated hemoglobin from 8.6% at baseline to 8.5% 2 months after periodontal therapy, but this change was not statistically significant. ¹⁷ Similarly, Buzinin et al. ¹⁸ showed lower glycated Hb values after periodontal therapy in the test group, from 9.24 ±2.34% at baseline to 8.93 ±2.35% at 3-month follow-up, but again, this reduction was insignificant. ¹⁸ In contrast, Lopes et al. ¹⁹ reported better glycemic control in subjects with T1DM after 6 months, with a reduction of 10.76% in glycated hemoglobin values from baseline (Δ = 0.07 ±0.03) when compared to T2DM (Δ = 0.02 ±0.02).

Observations from studies that included local drug delivery as a form of treatment have also been inconsistent. Skaleric et al. ¹⁵ used minocycline microspheres in the control group of their study. They reported a minimal reduction of glycated Hb from 9.11% to 8.5% from baseline to 24 months, which was not statistically significant. The randomized controlled trial by Llambés et al. ¹⁶ showed a different outcome, however. The test group was prescribed systemic doxycycline 100 mg, bid for the first day, followed by one capsule per day for 15 days, followed by periodontal therapy. They noted a baseline mean HbA1c of 7.64 ±1.81%, increasing 3 months after treatment to 7.71 ±1.74%, which was not statistically significant (Table 2). ¹⁶

From the present review of these studies, it can be inferred that the institution of periodontal treatment brings about the resolution of periodontal infection with long-term supervision and adequate maintenance care but has insignificant effects on glycemic control. Alternatively, adequate metabolic control may be responsible for an individual's response to periodontal treatment. In those individuals with poor diabetes control and extended duration of diabetes, adjunctive therapies such as systemic and local antimicrobial therapies benefit the clinical healing of periodontal tissues. However, more studies are needed to substantiate the use of local antimicrobial strategies in individuals with T1DM.

Some studies have evaluated inflammatory markers in the gingival fluid of individuals with T1DM. ^42,43 However, a meta-analysis by Rapone et al. ⁴⁰ found no such correlation between circulating inflammatory markers and T1DM. Therefore, the impact of periodontal inflammation on metabolic control in T1DM cannot be substantiated.,An umbrella review on T2DM and periodontitis by Lavigne and Forrest ⁴⁴ found some short-term benefits of periodontal treatment in terms of glycemic control compared to 6-month studies. They suggested this was an indicator of the need for more frequent periodontal assessment at 3-month intervals. Their conclusions support those of Botero et al. ⁴⁵ who published a systematic review on T2DM and glycemic control. Their observations may also be relevant for individuals with T1DM. Furthermore, Lavigne and Forrest state that the emphasis of periodontal treatment should be on improving periodontal health and not primarily on influencing glycemic control. From the clinical perspective, for individuals with T1DM, this should be the dictum as well since long-term stability of periodontal health augurs well for the body as a whole.

Limitations

The literature evaluated in the present review varied in many respects. The observations, provided in this article, are limited to the data obtained through the search strategy and use of specific keywords, which may have restricted the number of generated studies. Stringent quality assessment of this review was not possible because of the limited literature on T1DM. No distinction was made between studies in children and adults or cases of more aggressive forms of periodontitis. Most studies and review articles published on diabetes include a mix of subjects with type 1 or type 2 diabetes or do not mention the diabetes type. Very few studies specifically look at levels of glycated Hb as an outcome following periodontal treatment. Including studies that utilized fasting blood glucose could have strengthened the observations made. For assessing the effect of T1DM on periodontal disease, data were restricted to systematic reviews from January 2015 to December 2020. Hence, it is not easy to make conclusive inferences. There is a need for more evidence with long-term evaluation and studies using randomization with controlled conditions.

CONCLUSION

The two focused questions of this narrative review may be answered in the following ways. First, the literature selected for review suggests that more features of periodontal disease are prevalent in individuals with T1DM than in healthy individuals. The observations of poor oral hygiene status, higher gingiva,l inflammation, and periodontal attachment loss in T1DM concur with those observed in T2DM, although the evidence from longitudinal investigations is weak. Second, non-surgical periodontal treatment of individuals with T1DM has been shown to improve periodontal parameters. However, its effect on glycemic control is not consistent. There appears to be no direct benefit of non-surgical periodontal therapy in terms of improvement of metabolic control. It has been implied that, to achieve optimal metabolic control, one must consider the duration of T1DM, the baseline levels of HbA1c, lifestyle modifications, and a supervised plaque control program.

Table 2.

Comparison of periodontal treatment effects on glycemic control in patients with type 1 diabetes

	Reference	Study design	Follow-up	Periodontal therapy	Metabolic control outcome measure	Periodontal parameters assesseda	Effects on metabolic control
1a	Aldridge et al. (study 1) 199511	RCT	2 months	41 T1DM subjects with gingivitis and early periodontitis Treatment group: oral hygiene instructions, scaling, correction of restoration margins, reinforcement at one month Control group: no treatment	Glycated hemoglobin, fructosamine	PI, BOP, PD	Periodontal treatment showed no effect on glycated hemoglobin levels
1b	Aldridge et al. (study 2) 199511	RCT	2 months	23 subjects were recruited and divided into 2 groups Treatment group: oral hygiene instructions, scaling/root planing, extractions, root canal therapy Control group: no treatment	Glycated hemoglobin	PI, BOP, PD	Periodontal treatment showed no effect on glycated hemoglobin levels
2	Smith et al. 199612	Treatment study Non-RCT	2 months	Scaling and root planing using an ultrasonic scaler, curettes, oral hygiene instructions	Glycated hemoglobin	PD, CAL, GI Gingival fluid AST levels	No significant change in glycated hemoglobin
3	Westfelt et al. 199613	Treatment study Non-RCT	5 years	20 patients with diabetes, T1DM or T2DM, were recruited Patients received oral hygiene instruction, scaling and root planing, subgingival scaling and surgery at sites with BOP and PD >5 mm	Glycated hemoglobin	PI, GI	The mean value of HbA1c between baseline and 24 months was not significantly different from 24 to 60 months
4	Christgau et al. 199814	Treatment study, Non-RCT	2 months	20 T1DM (n = 7) or T2DM (n = 13) with periodontal disease Scaling and root planing, irrigation with chlorhexidine, oral hygiene instructions, extractions	Glycated hemoglobin	PI, Papilla bleeding index, BOP, PD, Probing attachment level (PAL)	No changes in glycated hemoglobin
5	Skaleric et al. 200415	RCT	6 months	20 patients with poorly controlled diabetes (HbA1c 7.5%) and periodontitis Presence of 4 teeth with 5 mm periodontal pockets and BOP The test group received scaling and root planing with minocycline microspheres (Arestin®) The control group received only scaling and root planing	Glycated hemoglobin	PI, GI, PD, CAL	Demonstrated reduction in HbA1c levels in both groups, but the intergroup difference was not statistically significant
6	Llambés et al. 200816	RCT	3 months	60 T1DM subjects with moderate to severe periodontitis Test group received scaling and root planing, chlorhexidine mouthwash, and doxycycline 100 mg for 15 days Control group: same treatment as test group but doxycycline was not given	Glycated hemoglobin	PI, BOP, PD, CAL	No changes in glycosylated hemoglobin
7	Tervonen et al. 200917	Non-RCT	2 months	Oral hygiene education, scaling, root planing, with or without periodontal surgery	Glycated hemoglobin		No improvement in glycemic control was reported by many subjects
8	Buzinin et al. 201418	Non-RCT		41 Malaysian subjects: 20 subjects were T1DM with chronic periodontal disease (test group) and 21 only chronic periodontal diseases Both groups received oral hygiene instructions and one session of full-mouth debridement	Glycated hemoglobin	PI, GI, PD, PAL	No changes in HbA1c level in the test group
9	Lopes et al. 201719	Non-RCT	6 months	70 patients with periodontitis; 3 groups Control group (n = 11): systemically healthy subjects Test-group 1 (n = 14): subjects with T1DM Test-group 2 (n = 27): subjects with T2DM Basic periodontal treatment, oral hygiene instructions, scaling and root planing, supportive therapy; additional 2 g amoxicillin as antibiotic prophylaxis 1 h before—for subjects with diabetes	Glycated hemoglobin	PI, BOP, PD, CAL	Periodontal treatment was more effective for glycemic control in T1DM patients than in T2DM

^aPI: Plaque Index; GI: Gingival Index; BOP: bleeding on probing; PD: pocket depth; CAL: clinical attachment level

Early diagnosis and institution of treatment may help reduce the considerable loss of periodontal support, which may be even more relevant in those developing the disease at a very young age. Reduction in the bacterial levels reduces inflammation in individuals with T1DM. Hence, effective treatment and maintaining adequate oral hygiene appear crucial in managing periodontal disease in individuals with T1DM. Since this disease develops earlier in life, it is imperative to consider preventive management strategies to halt a more extensive and severe course of disease. Dental hygienists have an active role to play in the management of periodontitis by providing personalized client education, motivation for home oral care, treatment, and regular recall to obtain optimal oral health benefits in clients with T1DM.

CONFLICTS OF INTEREST

The authors have declared no conflicts of interest.