In the first part of this three-part series of essays, the prevalence of diabetes mellitus (DM) in the United States and across the globe was reviewed, as was the recent literature on the bidirectional relationship of DM and periodontal disease, and DM as a risk factor for endodontic complications. It is evident from recently released epidemiological data that DM remains an enormous global health problem. The prevalence in the United States is 10% of the population (13% of adults). Globally, the International Diabetes Federation has estimated that 463 million adults between the ages of 28 and 79 have DM. Further, recent studies have confirmed and deepened our understanding of DM is an important risk factor for periodontitis, that conservative periodontal therapy can improve glycemic control and local and systemic inflammation underlie this bidirectional relationship. Regarding endodontic complications, persons with DM are at increased risk for development of such complications, and periapical healing is delayed in persons with DM. These relationships, however, are complicated by other factors such as the caries burden and the potential influence of reduced salivary flow that can both accompany DM and are a side effect of certain medications.

This second part of this series of essays will review the next stages in the natural history of dental disease in the context of DM, specifically dental disease leading to tooth loss, and then replacement of teeth with dental implants.

DM and Tooth Loss

The complex relationship of DM and oral disease is emphasized by the many oral disorders and changes in the oral cavity that can be seen in persons with DM. Adult tooth loss is the culmination of a lifetime of dental disease. While there are several reasons for tooth loss, primary causes are dental caries and periodontitis. Risk factors for tooth loss have also been identified, including age and socioeconomic status). DM is also an epidemiological risk factor for tooth loss, and this relationship has been evaluated in a systematic review with a meta-analysis and documented in recent studies from many countries.

The recent systematic review with a meta-analysis examined the relationship of DM and tooth loss. Ten studies were included, and six studies found an association of increased tooth loss in persons with DM, with an overall risk ratio of 1.63 (p < 0.00001). A relationship between poor metabolic control and increased risk of tooth loss was seen. Interestingly, geographic differences were observed, as the risk of tooth loss in persons with DM was greater in Asia and South America as compared to Europe and North America.1Weijdijk LPM, Ziukaite L, Van der Weijden GAF, Bakker EWP, Slot DE. The risk of tooth loss in patients with diabetes: A systematic review and meta-analysis. Int J Dent Hyg. 2021;00:1-22

Recent studies examining the relationship of DM and tooth loss are notable in that reports have come from across the globe, and a number of these have analyzed large databases. Two studies from Japan have reported this association. Using the National Database of Health Insurance Claims and Specific Health Checkups collected in 2015-2016, there were more than 5.2 million people without DM, and more than 1.5 million people with DM.2Suzuki S, Noda T, Nishioka Y, et al. Evaluation of tooth loss among patients with diabetes mellitus using the National Database of Health Insurance Claims and Specific Health Checkups of Japan. Int Dent J. 2020;70(4):308-15 Regardless of sex, persons with DM displayed more tooth loss than persons without the disease. This increased loss was independent of periodontal treatment. Differences in tooth loss between the two groups were most notable for posterior teeth, which were lost at an earlier age in the DM group (see Table 1).

Another study from Japan (Japan Diabetes Complication and Prevention Study) followed patients prospectively, examining a total of 6099 adult patients, with an age range of 40 to 70 years.3Inagaki K, Kikuchi T, Noguchi T, et al. A large-scale observational study to investigate the current status of diabetic complications and their prevention in Japan (JDCP study 6): baseline dental and oral findings. Diabetol Int. 2021;12(1):52-61 The mean number of teeth present at the beginning of the study was 19.8. Women with type 2 DM had greater tooth loss than men with type 2 DM. Regression analysis revealed that a higher risk of having less than 20 teeth was associated with glycated hemoglobin (HbA1c) of greater than 7.0% for patients with type 1 DM (odds ratio = 2.38) and greater than 8.0% for patients with type 2 DM (odds ratio = 1.16).

Two studies from South Korea also examined the occurrence of tooth loss in relationship to DM. Using data from the Korean National Health Insurance Service – National Sample Cohort, 10,125 persons with DM were followed and compared to an equal number of persons without DM.4Yoo JJ, Kim DW, Kim MY, Kim YT, Yoon JH. The effect of diabetes on tooth loss caused by periodontal disease: A nationwide population-based cohort study in South Korea. J Periodontol. 2019;90(6):576-83 There was an increased risk of tooth loss associated with DM (hazard ratio = 1.3). As the severity of the DM worsened, tooth loss increased. There was a decreased risk of tooth loss as the number of dental visits increased.

A retrospective study from South Korea analyzed data from more than 230,000 individuals, and assessed the relationship of tooth loss to health status variables. Data was available for participants from 2002 to 2015.5Kim YT, Choi JK, Kim DH, Jeong SN, Lee JH. Association between health status and tooth loss in Korean adults: longitudinal results from the National Health Insurance Service-Health Examinee Cohort, 2002-2015. J Periodontal Implant Sci. 2019;49(3):158-70 The analysis considered epidemiological and personal habit data. The risk of 4 or more teeth being lost was associated with increasing age [50-59 years, hazard ratio (HR) = 1.98. 60-69 years, HR = 2.93, 70-79 years, HR = 2.93], smoking (HR = 1.69) and DM (HR = 1.43). The authors concluded that tooth loss was due to multiple factors, and increasing age, smoking and DM were important variables.

There were also two studies from Mexico. One study reported on a cohort of 3,406 patients that were treated between 2013 and 2017.6Lopez-Gomez SA, Gonzalez-Lopez BS, Scougall-Vilchis RJ, et al. Tooth loss in patients with and without diabetes: A large-scale, cross-sectional study of Mexican adults. J Am Dent Assoc. 2020;151(4):276-86 Mean age was 42.5 years, and 64% were women. Of the total cohort, 12.1% had a diagnosis of DM. Patients with DM had on average 10.1 missing teeth, versus 7.1 missing teeth for persons without DM. Using regression analysis, the authors calculated that if a person had a diagnosis of DM, they had 11.4% more missing teeth than those without the disease. Other variables that were identified as related to the number of missing teeth were the type of occupation, insurance availability, and marital status.

Another report from Mexico evaluated patients seen at a community clinic. Information obtained included epidemiological variables (i.e., age, sex, education), as well information about perceived oral health, oral hygiene practices, visits to a dentist, smoking habits, and a diagnosis of DM.7Fatima Del Carmen AD, Aida BS, Javier FH. Risk indicators of tooth loss among Mexican adult population: A cross-sectional study. Int Dent J. 2021 The average age of this population was 41.6 years, two-thirds were female, and slightly more than half of the population had at least one missing tooth. Increased tooth loss was associated with being female [relative risk (RR) = 1.4], smoking (RR = 1.56) and patients who had DM and smoked (RR = 3.62). Fewer missing teeth was associated with more education, tooth brushing at least once per day, and brushing and flossing at least once per day. This study emphasizes that tooth loss has a multi-factorial etiology, but again emphasized the importance of DM as a risk factor.

Further, a study of a large cohort from Germany confirmed the relationship of DM and tooth loss.8Raedel M, Noack B, Priess HW, Bohm S, Walter MH. Massive data analyses show negative impact of type 1 and 2 diabetes on the outcome of periodontal treatment. Clin Oral Investig. 2021;25(4):2037-43 This study included 4,139 persons with type 1 DM, 22,430 persons with type 2 DM taking oral hypoglycemic mediation, and 23,576 persons with type 2 DM not taking oral hypoglycemic medication. A normoglycemic control group was also included. All individuals had received periodontal treatment. They calculated a ‘survival rate’ (no extractions over 4 years) to express the risk of tooth loss. These rates were 65.9% for the control group, and 51.7%, 54.0% and 57.7% for the three DM groups, respectively. This study adds the dimension of periodontal treatment to our understanding of DM as a risk factor for tooth loss.

Several recently published smaller studies also provide valuable information about the DM-tooth loss relationship. A short-term study of healing after an extraction observed that initial healing of an extraction site in patients with DM is associated with more complications as compared to persons without DM. During the first week following the extraction, the size of the socket was larger, and a greater amount of swelling (suggestive of infection) were observed in the DM group. However, the authors concluded that these complications were minor.9Gadicherla S, Smriti K, Roy S, et al. Comparison of extraction socket healing in non-diabetic, prediabetic, and type 2 diabetic patients. Clin Cosmet Investig Dent. 2020;12:291-6

A study of hospitalized patients included those with and without DM. Both groups showed extensive tooth loss. Risk factors for having fewer ‘healthy’ teeth included older age, smoking, DM, and infrequent tooth brushing. Interestingly, for both groups having fewer teeth was associated with cardiovascular disease.10Izuora K, Yousif A, Allenback G, Gewelber C, Neubauer M. Relationship between dental loss and health outcomes among hospitalized patients with and without diabetes. J Investig Med. 2019;67(3):669-73 Cardiovascular disease is a recognized clinical complication of DM.

A small study reported the reasons for tooth extraction in older adults (mean age of 63 years). The most common reasons for tooth loss were caries (52%) and periodontal disease (36%). Persons with DM had a greater number of missing teeth, and these individuals also had a higher percentage of teeth extracted due to periodontal disease than persons without DM.11Passarelli PC, Pagnoni S, Piccirillo GB, et al. Reasons for tooth extractions and related risk factors in adult patients: A cohort study. Int J Environ Res Public Health. 2020;17(7)

These recent studies on the relationship of DM to tooth loss certainly confirm that DM is a risk factor for loss of teeth, and that tooth loss is a result of many factors, including but not limited to a history of caries and periodontitis, health status, age and various personal characteristics.

DM and Implant Complications

One of the most discussed aspects of the DM – oral disease relationship is how implant outcomes are affected by dysglycemia. The importance of this topic evidenced by the large number of recently published systematic reviews on this subject. It is important to differentiate systematic reviews which include a meta-analysis to estimate the actual effect of the modifying variable (here DM), from systematic reviews which do not include a meta-analysis. Both types of reviews differ in the number of studies included, due to different criteria used to evaluate the studies included in the review. The more stringent the criteria, the fewer original studies will be included.

Three recent systematic reviews without a meta-analysis examined this question. One of these12Souto-Maior JR, Pellizzer EP, de Luna Gomes JM, et al. Influence of diabetes on the survival rate and marginal bone loss of dental implants: An overview of systematic reviews. J Oral Implantol. 2019;45(4):334-40 was a systemic review of previous published systematic reviews. The other two13Chambrone L, Palma LF. Current status of dental implants survival and peri-implant bone loss in patients with uncontrolled type-2 diabetes mellitus. Curr Opin Endocrinol Diabetes Obes. 2019;26(4):219-22,14Meza Mauricio J, Miranda TS, Almeida ML, et al. An umbrella review on the effects of diabetes on implant failure and peri-implant diseases. Braz Oral Res. 2019;33(suppl 1):e070 included original research. These reviews examined both peri-implant bone loss (peri-implantitis) and implant survival. Conclusions drawn from these three reviews are:

  1. If patients with DM have good metabolic control, and demonstrate excellent oral hygiene, implant success rates are equivalent to what is observed for patients without DM. In other words, implant therapy is generally a very successful clinical approach to replace missing teeth in persons with well-controlled DM who also demonstrate excellent self-care.
  2. The occurrence of peri-implantitis is greater in patients with DM. This is often observed as marginal bone loss.
  3. When metabolic control in persons with DM is poor, implant complications increase above what is seen in patients without DM.

A consistent comment in all three reviews was that the quality of the original reports is generally only fair. This can lead to confusion when trying to interpret the findings.

Systematic reviews with a meta-analysis allow the reader to determine the actual effect, the magnitude of change, associated with the variable under study. Four systematic reviews with a meta-analysis are worth mentioning.

A study of the nature of implant complications (peri-implant mucositis, peri-implantitis) in metabolically well-controlled patients with DM included 7 studies, which the authors evaluated as being of “moderate quality”.15Lagunov VL, Sun J, George R. Evaluation of biologic implant success parameters in type 2 diabetic glycemic control patients versus health patients: A meta-analysis. J Investig Clin Dent. 2019;10(4):e12478 As compared to patients with implants but without DM, the patients with DM displayed greater bleeding following probing (p < .04), probing depth (p < .001) and marginal bone loss (p < .001). These changes occurred even when DM was well-controlled. This systematic review focused attention on changes in implant complications, not implant survival.

Another systematic review with a meta-analysis included 10 studies and observed similar findings regarding marginal bone loss, probing depth and bleeding following probing; all three parameters were greater for implants in patients with DM. They also observed that implants that were immediately loaded (a temporary restoration was placed on the implant at the time of implant insertion) demonstrated a greater increase in probing depth about the implants. An association of increased HbA1c and increased bleeding following probing was seen.16Jiang X, Zhu Y, Liu Z, Tian Z, Zhu S. Association between diabetes and dental implant complications: a systematic review and meta-analysis. Acta Odontol Scand. 2021;79(1):9-18

A third systematic review with a meta-analysis sought to answer the question: does an increase in HbA1c (decreasing metabolic control) correlate with increased implant complications?17Tan SJ, Baharin B, Nabil S, Mohd N, Zhu Y. Does glycemic control have a dose-response relationship with implant outcomes? A comprehensive systematic review and meta-analysis. J Evid Based Dent Pract. 2021;21(2):101543 They observed significant adverse changes when the HbA1c was above 8%, for both clinical parameters and implant survival. A dose-response relationship between increasing HbA1c and bleeding following probing and marginal bone loss was seen (see Table 2). Osseointegration was also adversely affected when HbA1c was above 8%.

The fourth systematic review with a meta-analysis reported both specific clinical parameters and the ultimate implant outcome, that is implant survival, in patients with type 2 DM. They did not report an increase in implant failure in patients with type 2 DM compared to healthy control patients but did report greater bleeding following probing and marginal bone loss in these patients.18Shang R, Gao L. Impact of hyperglycemia on the rate of implant failure and peri-implant parameters in patients with type 2 diabetes mellitus: Systematic review and meta-analysis. J Am Dent Assoc. 2021;152(3):189-201 e1

Two additional recent studies are worth noting. A scoping review of the relationship of the metabolic syndrome (often associated with obesity and considered an important risk factor for the development of DM) and DM to implant complications concluded that both conditions are to be considered risk factors for these complications, and the underlying mechanisms include hyperglycemia-associated impaired osseous healing, microvascular impairment, altered wound healing (after implant insertion), and an increased inflammatory response characterized by oxidative stress.19de Oliveira P, Bonfante EA, Bergamo ETP, et al. Obesity/metabolic dyndrome and diabetes mellitus on peri-implantitis. Trends Endocrinol Metab. 2020;31(8):596-610 Further, a systematic review and meta-analysis examined the more general effect of different systematic conditions associated with aging on survival of dental implants. Examining patients 75 years of age and older, data was included from 60 studies.20Schimmel M, Srinivasan M, McKenna G, Muller F. Effect of advanced age and/or systemic medical conditions on dental implant survival: A systematic review and meta-analysis. Clin Oral Implants Res. 2018;29 Suppl 16:311-30 Implant survival of 97% at 1 year and 96% at 5 years was reported, which indicates a remarkable degree of success. They did not observe any adverse effect of cardiovascular disease, Parkinson’s disease, type 2 DM, osteoarthritis, respiratory disease, and cognitive impairment on implant survival. For patients with cancer, treatment with radiation therapy did adversely affect implant survival. The impact of antiresorptive medicine varied by dose. With high doses (usually associated with bone metastases), survival was reduced. There was no adverse effect with low dose antiresorptive medications (used in the treatment of osteoporosis). The conclusion was that the use of implants in older adults was not contraindicated. While this review is subject to criticism given the wide range of disorders included and the variable design of the studies, it appears that the benefits of re-establishing a functional and esthetic dentition clearly were greater than the risks of implant complications for older adult patients with chronic diseases.

In summary, these recent reviews suggest that implant therapy is not contraindicated in persons with DM, but that an increase in implant complications can be expected in such individuals. This will mean a greater focus on personal care by patients, and the need for routine professional care which should include close monitoring of implant status.

Several recent individual studies are worth reviewing, as they help guide clinical decisions and follow-up care regarding the placement and maintenance of dental implants in patients with DM. The previous reviews emphasized that if a dental patient has DM, the likelihood is that they will experience more complications, and perhaps a lower survival rate of osseointegrated implants. What does the recent literature tell us about how these complications can be minimized?

A two-year study of implant complications followed patients with well-controlled type 1 DM and an age-matched control group. After 2 years, there were no differences in the rate of complications or implant failure between the two groups. Implant survival in the DM group was 95.2%, vs. 97.0% in the control group.21Sannino G, Montemezzi P, Pantaleo G, Agliardi E. Dental implants survival rate in controlled type I diabetic patients: A prospective longitudinal study with a 2-year follow-up. J Biol Regul Homeost Agents. 2020;34(6 Suppl. 3):37-45 This finding suggests the importance of communication with dental patients’ medical providers both before and after implant placement regarding the level of metabolic control. Another recent small study compared implant complications (plaque index, gingival index, probing depth and crestal bone loss) in patients without DM, with prediabetes, and type 2 DM who received dental implants.22Alshahrani A, Al Deeb M, Alresayes S, et al. Comparison of peri-implant soft tissue and crestal bone status of dental implants placed in prediabetic, type 2 diabetic, and non-diabetic individuals: A retrospective cohort study. Int J Implant Dent. 2020;6(1):56 The findings indicated that complications were significantly greater in patients with poorly controlled DM and prediabetes, as compared to those who were normoglycemic.

Another recent report examined implant survival in patients with well-controlled DM and individuals without DM. Over a 3-year period, implant failure was 9.8% in the patients with DM, versus 9.0%, in the healthy group. This difference was not significant.23Sghaireen MG, Alduraywish AA, Srivastava KC, et al. Comparative evaluation of dental implant failure among healthy and well-controlled diabetic patients-a 3-year retrospective study. Int J Environ Res Public Health. 2020;17(14) Examining the other side of this question, a study of crestal bone loss indicated that patients with HbA1c ranging from 8.1% to 10.0% demonstrated greater margin bone loss than the healthy controls24Lorean A, Ziv-On H, Perlis V, Ormianer Z. Marginal bone loss of dental implants in patients with type 2 diabetes mellitus with poorly controlled HbA1c values: A long-term retrospective study. Int J Oral Maxillofac Implants. 2021;36(2):355-60 The authors went so far as to conclude that patients with poorly controlled DM should be treated with removable dentures and not implants.

In sum, these reviews and individual studies indicate that dentists who are considering implant treatment for patients with DM must be familiar with the patient’s level of metabolic control both before and after implant placement to minimize adverse outcomes.

Prior to implant placement, every effort should be made to achieve the best possible metabolic control, which requires close collaboration with the patient’s medical providers. From a clinical perspective, adequate metabolic control as measured by HbA1c is generally considered to be 7% or less. The recent studies suggest that an HbA1c above 8% appears to be a critical value when greater complications and reduced implant survival can be expected. The importance of excellent personal oral hygiene, and regular professional dental care, should be discussed with all candidates for dental implants, especially those reporting a history of DM. In all cases the perceived risks of implant complications should be considered along with the important benefits of establishing a functional and esthetic dentition.

In closing, it is important to emphasize that in addition to DM, there are other risk factors for implant complications, including poor oral hygiene, a history of periodontitis and smoking. Consequently, preparation for implant therapy requires a very detailed level of planning and follow-up.25Rosing CK, Fiorini T, Haas AN, et al. The impact of maintenance on peri-implant health. Braz Oral Res. 2019;33(suppl 1):e074

Table 1: Mean yearly tooth loss in DM and control (C) patients. Stratified by age, sex and periodontal treatment.

Periodontal Treatment
    No Yes
  Age C DM C DM
Male 50-54 0.122 0.187 0.139 0.223
  55-59 0.153 0.215 0.168 0.247
  60-64 0.181 0.224 0.189 0.255
  65-69 0.197 0.226 0.205 0.262
  70-74 0.210 0.227 0.218 0.264
Female 50-54 0.100 0.174 0.105 0.204
  55-59 0.123 0.194 0.126 0.218
  60-64 0.145 0.199 0.141 0.225
  65-69 0.162 0.208 0.156 0.227
  70-74 0.176 0.210 0.172 0.233

Adapted from Suzuki et al (2020)

Table 2. Weighted mean bone loss in mm (per year).

Follow-up <6% 6.1-8.0% 8.1-10%
12 months 0.47 0.69 0.70
24 months 0.61 0.69 0.70
36 months 0.49 0.59 0.80

Adapted from Tan et al (2021)


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