NIH Public Access Author Manuscript Forum Implantol. Author manuscript; available in PMC 2014 October 17.
NIH-PA Author Manuscript
Published in final edited form as: Forum Implantol. 2012 February ; 8(2): 7–14.
Diabetes Effects on Dental Implant Survival Thomas W. Oates, DMD, PhD and Guy Huynh-Ba, DDS, Dr. med. dent., MS
SUMMARY The goal of this review is to critically appraise the clinical evidence guiding our application of dental implant therapy relative to glycemic control for patients with diabetes.
NIH-PA Author Manuscript
Our initial searches of the literature identified 129 publications relevant to both dental implants and diabetes. These were reduced to 17 clinical studies for inclusion. Reported implant failure rates in these 17 reports ranged from 0 to 14.3% for patients with diabetes. Unfortunately, the majority of these reports lacked sufficient information relative to glycemic control to allow the application of the findings toward clinical care. However, clinical evidence is emerging from several investigations that diabetes and glycemic control are important considerations that may require modifications to therapeutic protocols, but may not be contraindications to implant therapy in diabetes patients. Also, a potentially important role for implant therapy to support oral function in diabetes dietary management remains to be determined.
INTRODUCTION Diabetes mellitus is a chronic metabolic disorder that is reaching epidemic proportions, recently projected as affecting over 350 million individuals worldwide. The number of affected individuals underlines the urgent need to understand the effects of diabetes and improve the care for patients with diabetes (Danaei et al. 2011).
NIH-PA Author Manuscript
Diabetes mellitus has long been considered a relative contraindication to dental implant therapy. Our understanding of diabetes mellitus as a relative contraindication, based on the patient’s level of glycemic control, has changed little since the 1988 NIH Consensus Conference on Dental Implants (National Institutes of Health Consensus Development Conference 1988, World Workshop in Periodontics 1996, Javed & Romanos 2009). As a result, well-controlled diabetic patients may be considered appropriate for implant therapy while diabetic patients lacking good glycemic control may be denied the benefits of implant therapy. Given the importance of an evidence basis for care, this review is designed to critically examine the evidence available for the use of implant therapy for patients with diabetes based on glycemic control. Importantly, clinical studies directly examining the relationship between diabetes and implant survival, and the potential for glycemic control to serve as an appropriate discriminator for the application of care, are considered.
GLYCEMIC CONTROL Glycemic control has long been the primary consideration for implant patients with diabetes. This appears appropriate given the correlations between glycemic control and microvascular
Oates and Huynh-Ba
Page 2
NIH-PA Author Manuscript
and macrovascular complications (Cohen & Horton 2007). While there are multiple methods to assess glycemic levels, glycated hemoglobin A1c (HbA1c) is becoming the most frequently used and valuable diagnostic and therapeutic measure of blood glucose control. The HgA1c value represents the percentage of non-enzymatically glycated A1c hemoglobin in red blood cells. This value is based on the average circulating time of a red blood cell – 60 - 90 days – and reflects the average blood glucose exposure over two to three months. Elevated HbA1c levels correlate directly with morbidity and mortality in diabetes (Boltri et al. 2005). Therefore, achieving low HbA1c levels serves as an important therapeutic target in the management of diabetes (Wysham 2010). Recent recommendations for strict glycemic control for persons with diabetes have targeted maximal HbA1c levels ranging from 6.5% up to 7.0% (Rodbard et al. 2009, Standards of Medical Care in Diabetes, 2010).
MASTICATORY FUNCTION AND DIABETES
NIH-PA Author Manuscript
Periodontal disease frequently results in tooth loss, with the cumulative effects most significant in older patients (Albandar et al. 1999). It is these older patients who are also particularly susceptible to type 2 diabetes and its comorbidities. Thus, one of the more subtle complications of diabetes may be a decrease in a patient’s health and quality of life due to tooth loss and compromised function (McGrath & Bedi 2001). Importantly, compromises in masticatory function that lead to alterations in dietary behaviors for diabetic patients may be an essential consideration in the overall disease management for these patients, directly impacting glycemic control (Kawamura et al. 2001, Nuttall et al. 2003, Roumanas et al. 2003, Savoca et al. 2010). Therefore, oral health and functional tooth replacement must be considered in the overall dietary and nutritional management of patients with diabetes (Quandt et al. 2009). It may be those individuals with significant oral debilitation and difficulties managing glycemic levels who have the most to gain from improvements in oral function associated with implant therapy.
BONE METABOLISM AND DIABETES MELLITUS
NIH-PA Author Manuscript
Dental implant survival is initially dependent upon successful osseointegration following placement. Subsequently, as an implant is restored and placed into function, bone remodeling becomes critical to long-term implant survival in responding to the functional demands placed on the implant restoration and supporting bone. The critical dependence on bone metabolism for implant survival may be a vulnerability for patients with diabetes. Both type 1 and type 2 diabetes have been associated with osteopathic outcomes. Several recent meta-analyses of clinical studies have identified direct associations between type 2 diabetes and increased risk of fracture, however, they failed to find an association between HbA1c levels and fracture risk (Janghorbani et al. 2006, Vestergaard 2007, Asano et al. 2008). These results are also consistent with their finding no association between bone density and HbA1c (Janghorbani et al. 2006, Asano et al. 2008). Therefore, the importance of glycemic control as a factor for compromised bone metabolism has yet to be realized at a systemic level.
Forum Implantol. Author manuscript; available in PMC 2014 October 17.
Oates and Huynh-Ba
Page 3
DIABETES AND IMPLANT INTEGRATION NIH-PA Author Manuscript
As questions remain as to the effects of diabetes and glycemic control on bone metabolism, it is important for us to consider these effects for implant therapy as well. A thorough review of the literature for clinical investigations examining diabetes and dental implant survival identified 17 primary studies, many of which are frequently cited in support of diabetes as a relative contraindication to implant therapy. The majority of the studies identified in this review, 13 of 17 reports, were undertaken with the prevailing view that good glycemic control is critical to the successful use of implant therapy for patients with diabetes (Table 1). All 13 of these studies looked to include only patients considered as having acceptable glycemic control in order to receive implant therapy. Nine of the 13 studies did not quantify glycemic levels, and the four investigations that did document glycemic levels suggested that not all enrolled patients were well-controlled. However, for these four studies, there was considerable variability in the evaluation or documentation of the patients’ glycemic levels, leaving the findings not clearly interpretable toward clinical care (Kapur et al. 1998; Olson et al. 2000; Abdulwassie & Dhanrajani 2002; Peled et al. 2003).
NIH-PA Author Manuscript
Evaluation of implant failure rates for these 13 studies demonstrated considerable variability in the rate of implant failure in patients with diabetes (0 to 14.3%; Fig. 1). Additionally, the rate at which diabetic patients receiving one or more implants experienced at least one failed implant was also highly variable (0 to 31.3%, Fig. 2). A search of the literature also identified four of the 17 studies in which patients lacking acceptable glycemic control were included and reported specifically defined assessments of glycemic control (Table 2). In contrast to the studies lacking this methodological detail, these four studies had implant failure rates ranging from 0 to 3.9%, and the rate of patients experiencing implant failure from 0 to 4.1% (Table 2). These four reports extend our understanding of the effects of diabetes by including patients with only moderate or poor glycemic control and warrant specific consideration (Dowell et al. 2007, Tawil et al. 2008, Turkyilmaz 2010, Khandelwal 2011).
NIH-PA Author Manuscript
The first of these studies evaluated implant healing over a four-month evaluation period prior to implant restoration. Importantly, this landmark study did so for diabetic patients having an HbA1c of up to 12% at the time of surgery and with HbA1c levels extending as high as 13.8% over a four-month evaluation period (Dowell et al. 2007, Oates et al. 2009). The 25 diabetes patients ultimately enrolled in this study included 12 patients (17 implants) who would not be considered as well-controlled, having HbA1c levels between 8.1 to 10.0%, and three patients (four implants) with HbA1c levels over 10.0%. Also, as diabetes may affect bone metabolism differently following implant placement from that associated with long-term functional restoration, this study focused on understanding the effects of glycemic levels on the early healing events following implant placement prior to restoration. This study failed to identify any implant failures over the four-month healing period. Interestingly, consistent with animal studies on the effects of hyperglycemia on bone metabolism, this study did identify significant compromises in implant integration in direct Forum Implantol. Author manuscript; available in PMC 2014 October 17.
Oates and Huynh-Ba
Page 4
NIH-PA Author Manuscript
relation to HbA1c levels (Oates et al. 2009). Specifically, delays in implant integration were identified for patients with HbA1c levels over 8.0%, but not for patients below this level of glycemic control, consistent with increased risks for many diabetes comorbidities (Cohen & Horton 2007). This study’s findings show that the effects of hyperglycemia on implant integration, if clinically significant, were successfully accommodated with an extended healing period from two months to four months prior to functional loading as utilized in this study. It must be emphasized that this study did not evaluate implant failure over a longer time period following restoration.
NIH-PA Author Manuscript
In a second study, 45 diabetes patients having an initial HbA1c below 7.2% received 255 implants. They were followed over a period ranging from one to 12 years (Tawil et al. 2008). The HbA1c levels for these patients varied over the follow-up period, with frequency of HbA1c assessments not reported. HbA1c levels below 9% were identified for 44 patients, while one patient recorded an HbA1c level over 9%. This latter patient received 11 implants and had one failure, giving the study a seemingly high failure rate (9.1% implant failure rate) for this one patient. However, when this patient’s results are combined with the other 22 patients having only moderate glycemic control over the course of their evaluation period, the cumulative implant failure rate is 3.9%. As all these patients initiated implant therapy with an HbA1c 10.0
Poor
ModeratePoor
8.1-10.0
6.0-8.0
Well Moderate
NIH-PA Author Manuscript
Published in final edited form as: Forum Implantol. 2012 February ; 8(2): 7–14.
Diabetes Effects on Dental Implant Survival Thomas W. Oates, DMD, PhD and Guy Huynh-Ba, DDS, Dr. med. dent., MS
SUMMARY The goal of this review is to critically appraise the clinical evidence guiding our application of dental implant therapy relative to glycemic control for patients with diabetes.
NIH-PA Author Manuscript
Our initial searches of the literature identified 129 publications relevant to both dental implants and diabetes. These were reduced to 17 clinical studies for inclusion. Reported implant failure rates in these 17 reports ranged from 0 to 14.3% for patients with diabetes. Unfortunately, the majority of these reports lacked sufficient information relative to glycemic control to allow the application of the findings toward clinical care. However, clinical evidence is emerging from several investigations that diabetes and glycemic control are important considerations that may require modifications to therapeutic protocols, but may not be contraindications to implant therapy in diabetes patients. Also, a potentially important role for implant therapy to support oral function in diabetes dietary management remains to be determined.
INTRODUCTION Diabetes mellitus is a chronic metabolic disorder that is reaching epidemic proportions, recently projected as affecting over 350 million individuals worldwide. The number of affected individuals underlines the urgent need to understand the effects of diabetes and improve the care for patients with diabetes (Danaei et al. 2011).
NIH-PA Author Manuscript
Diabetes mellitus has long been considered a relative contraindication to dental implant therapy. Our understanding of diabetes mellitus as a relative contraindication, based on the patient’s level of glycemic control, has changed little since the 1988 NIH Consensus Conference on Dental Implants (National Institutes of Health Consensus Development Conference 1988, World Workshop in Periodontics 1996, Javed & Romanos 2009). As a result, well-controlled diabetic patients may be considered appropriate for implant therapy while diabetic patients lacking good glycemic control may be denied the benefits of implant therapy. Given the importance of an evidence basis for care, this review is designed to critically examine the evidence available for the use of implant therapy for patients with diabetes based on glycemic control. Importantly, clinical studies directly examining the relationship between diabetes and implant survival, and the potential for glycemic control to serve as an appropriate discriminator for the application of care, are considered.
GLYCEMIC CONTROL Glycemic control has long been the primary consideration for implant patients with diabetes. This appears appropriate given the correlations between glycemic control and microvascular
Oates and Huynh-Ba
Page 2
NIH-PA Author Manuscript
and macrovascular complications (Cohen & Horton 2007). While there are multiple methods to assess glycemic levels, glycated hemoglobin A1c (HbA1c) is becoming the most frequently used and valuable diagnostic and therapeutic measure of blood glucose control. The HgA1c value represents the percentage of non-enzymatically glycated A1c hemoglobin in red blood cells. This value is based on the average circulating time of a red blood cell – 60 - 90 days – and reflects the average blood glucose exposure over two to three months. Elevated HbA1c levels correlate directly with morbidity and mortality in diabetes (Boltri et al. 2005). Therefore, achieving low HbA1c levels serves as an important therapeutic target in the management of diabetes (Wysham 2010). Recent recommendations for strict glycemic control for persons with diabetes have targeted maximal HbA1c levels ranging from 6.5% up to 7.0% (Rodbard et al. 2009, Standards of Medical Care in Diabetes, 2010).
MASTICATORY FUNCTION AND DIABETES
NIH-PA Author Manuscript
Periodontal disease frequently results in tooth loss, with the cumulative effects most significant in older patients (Albandar et al. 1999). It is these older patients who are also particularly susceptible to type 2 diabetes and its comorbidities. Thus, one of the more subtle complications of diabetes may be a decrease in a patient’s health and quality of life due to tooth loss and compromised function (McGrath & Bedi 2001). Importantly, compromises in masticatory function that lead to alterations in dietary behaviors for diabetic patients may be an essential consideration in the overall disease management for these patients, directly impacting glycemic control (Kawamura et al. 2001, Nuttall et al. 2003, Roumanas et al. 2003, Savoca et al. 2010). Therefore, oral health and functional tooth replacement must be considered in the overall dietary and nutritional management of patients with diabetes (Quandt et al. 2009). It may be those individuals with significant oral debilitation and difficulties managing glycemic levels who have the most to gain from improvements in oral function associated with implant therapy.
BONE METABOLISM AND DIABETES MELLITUS
NIH-PA Author Manuscript
Dental implant survival is initially dependent upon successful osseointegration following placement. Subsequently, as an implant is restored and placed into function, bone remodeling becomes critical to long-term implant survival in responding to the functional demands placed on the implant restoration and supporting bone. The critical dependence on bone metabolism for implant survival may be a vulnerability for patients with diabetes. Both type 1 and type 2 diabetes have been associated with osteopathic outcomes. Several recent meta-analyses of clinical studies have identified direct associations between type 2 diabetes and increased risk of fracture, however, they failed to find an association between HbA1c levels and fracture risk (Janghorbani et al. 2006, Vestergaard 2007, Asano et al. 2008). These results are also consistent with their finding no association between bone density and HbA1c (Janghorbani et al. 2006, Asano et al. 2008). Therefore, the importance of glycemic control as a factor for compromised bone metabolism has yet to be realized at a systemic level.
Forum Implantol. Author manuscript; available in PMC 2014 October 17.
Oates and Huynh-Ba
Page 3
DIABETES AND IMPLANT INTEGRATION NIH-PA Author Manuscript
As questions remain as to the effects of diabetes and glycemic control on bone metabolism, it is important for us to consider these effects for implant therapy as well. A thorough review of the literature for clinical investigations examining diabetes and dental implant survival identified 17 primary studies, many of which are frequently cited in support of diabetes as a relative contraindication to implant therapy. The majority of the studies identified in this review, 13 of 17 reports, were undertaken with the prevailing view that good glycemic control is critical to the successful use of implant therapy for patients with diabetes (Table 1). All 13 of these studies looked to include only patients considered as having acceptable glycemic control in order to receive implant therapy. Nine of the 13 studies did not quantify glycemic levels, and the four investigations that did document glycemic levels suggested that not all enrolled patients were well-controlled. However, for these four studies, there was considerable variability in the evaluation or documentation of the patients’ glycemic levels, leaving the findings not clearly interpretable toward clinical care (Kapur et al. 1998; Olson et al. 2000; Abdulwassie & Dhanrajani 2002; Peled et al. 2003).
NIH-PA Author Manuscript
Evaluation of implant failure rates for these 13 studies demonstrated considerable variability in the rate of implant failure in patients with diabetes (0 to 14.3%; Fig. 1). Additionally, the rate at which diabetic patients receiving one or more implants experienced at least one failed implant was also highly variable (0 to 31.3%, Fig. 2). A search of the literature also identified four of the 17 studies in which patients lacking acceptable glycemic control were included and reported specifically defined assessments of glycemic control (Table 2). In contrast to the studies lacking this methodological detail, these four studies had implant failure rates ranging from 0 to 3.9%, and the rate of patients experiencing implant failure from 0 to 4.1% (Table 2). These four reports extend our understanding of the effects of diabetes by including patients with only moderate or poor glycemic control and warrant specific consideration (Dowell et al. 2007, Tawil et al. 2008, Turkyilmaz 2010, Khandelwal 2011).
NIH-PA Author Manuscript
The first of these studies evaluated implant healing over a four-month evaluation period prior to implant restoration. Importantly, this landmark study did so for diabetic patients having an HbA1c of up to 12% at the time of surgery and with HbA1c levels extending as high as 13.8% over a four-month evaluation period (Dowell et al. 2007, Oates et al. 2009). The 25 diabetes patients ultimately enrolled in this study included 12 patients (17 implants) who would not be considered as well-controlled, having HbA1c levels between 8.1 to 10.0%, and three patients (four implants) with HbA1c levels over 10.0%. Also, as diabetes may affect bone metabolism differently following implant placement from that associated with long-term functional restoration, this study focused on understanding the effects of glycemic levels on the early healing events following implant placement prior to restoration. This study failed to identify any implant failures over the four-month healing period. Interestingly, consistent with animal studies on the effects of hyperglycemia on bone metabolism, this study did identify significant compromises in implant integration in direct Forum Implantol. Author manuscript; available in PMC 2014 October 17.
Oates and Huynh-Ba
Page 4
NIH-PA Author Manuscript
relation to HbA1c levels (Oates et al. 2009). Specifically, delays in implant integration were identified for patients with HbA1c levels over 8.0%, but not for patients below this level of glycemic control, consistent with increased risks for many diabetes comorbidities (Cohen & Horton 2007). This study’s findings show that the effects of hyperglycemia on implant integration, if clinically significant, were successfully accommodated with an extended healing period from two months to four months prior to functional loading as utilized in this study. It must be emphasized that this study did not evaluate implant failure over a longer time period following restoration.
NIH-PA Author Manuscript
In a second study, 45 diabetes patients having an initial HbA1c below 7.2% received 255 implants. They were followed over a period ranging from one to 12 years (Tawil et al. 2008). The HbA1c levels for these patients varied over the follow-up period, with frequency of HbA1c assessments not reported. HbA1c levels below 9% were identified for 44 patients, while one patient recorded an HbA1c level over 9%. This latter patient received 11 implants and had one failure, giving the study a seemingly high failure rate (9.1% implant failure rate) for this one patient. However, when this patient’s results are combined with the other 22 patients having only moderate glycemic control over the course of their evaluation period, the cumulative implant failure rate is 3.9%. As all these patients initiated implant therapy with an HbA1c 10.0
Poor
ModeratePoor
8.1-10.0
6.0-8.0
Well Moderate
