Influence of Glycemic Control on the Survival of Implants Placed in the Zygomatic Bone of Edentulous Patients With and Without Type 2 Diabetes Mellitus: 10-Year Follow-Up Results

Alveolar bone resorption in conjunction with a compromised bone quality and increased pneumatization of maxillary antrum often challenge clinicians during conventional implant placement in the posterior maxilla.¹  Osseous augmentation protocols are often done before placement in load-bearing areas such as the atrophic posterior maxilla² ; however, a reliable alternate to bone grafting is placement of implants in the zygomatic area.¹  In a 1-year follow-up study, Hirsch et al³  assessed zygomatic implants in relation to their survival, prosthetic functioning, and patient satisfaction. In this study, outcome of 76 individuals treated with 145 implants placed in zygomatic bone (ZB) were appraised. At 12 months, the overall survival rate of implants placed in ZB was 97.9%, and 80% of the patients expressed their satisfaction with the prosthetic and esthetic outcomes of the zygomatic implants.³  Moreover, peri-implant mucosa was reported as “normal” in 60% of the sites.³  This short-term follow-up clinical study concluded that prosthesis supported implants placed in the ZB are successful in terms of esthetics and prosthetic functioning.³ 

Diabetes mellitus (DM) is an endocrine disorder associated with an absolute or partial insulin deficiency, with type 2 DM (T2DM) being its most common subtype.⁴  An impaired glycemic status risks the general health status of vulnerable patients by suppressing the immune response⁵ ; however, the risk of periodontal and peri-implant diseases (peri-implant mucositis and peri-implantitis) is also high in these individuals.^6–10  Despite the fact that poor control of DM increases the scores of peri-implant crestal bone loss (BL), probing depth (PD), and plaque and gingival indices (PI and GI, respectively), clinical evidence^11–14  has shown that such peri-implant parameters can remain within normal limits provided stringent measures are taken toward regular blood glucose maintenance. This suggests that dental implants can demonstrate high survival rates in medically compromised patients, such as individuals with T2DM as long as serum glycemic levels are controlled in these individuals. In a 24-month follow-up observational clinical study, Eskow and Oates¹⁵  showed that dental implants can demonstrate survival rates of nearly 99% in T2DM patients with impaired glycemic levels; however, there is a dearth of evidence in indexed literature that has demonstrated the survival of implants in these patients in the long term (at least 10 years of follow-up). Moreover, there are no studies that have assessed the influence of glycemic control (GC) on the survival of zygomatic implants placed in patients with varying glycemic levels.

The authors of this observational cohort study hypothesize that there is no difference in the survival of implants placed in the zygomatic bone of edentulous patient with and without T2DM. The aim was to assess the survival of implants placed in the zygomatic bone of edentulous patient with and without T2DM at 10-year follow-up.

The present clinical study was done according to the guidelines of the Declaration of Helsinki, which were revised in 2013 for experimentation involving human patients. All volunteering individuals were requested to read and sign a consent form written in simple English and Arabic. All participants were informed that they could withdraw their participation at any phase of the study without consequences. Ethical approval was obtained from ethics research committee of Centre for specialist dental practice and clinical research, Riyadh, Saudi Arabia. All volunteering patients were informed that they can withdraw from the present study at any time and withdrawal bears no penalty.

Based on hemoglobin A1c (HbA1c) levels, participants were classified into 3 groups: (1) patients with poorly controlled T2DM¹⁶  (HbA1c ≥ 6.5%)¹⁷; (2) patients with well-controlled T2DM (HbA1c < 5.7%)^16,18 ; and (3) self-reported systemically healthy individuals with normal glycemic levels (HbA1c < 5.7%).¹⁸ 

Using a structured questionnaire demographic information (age, sex, daily tooth brushing, and flossing habits; durations of T2DM and implants implant-supported prosthesis in function) was recorded. Participants were also inquired if they were visiting their oral and general health care providers at least bi-annually and annually, respectively. The questionnaire was managed by 1 experienced co-investigator (κ = 0.94). Medical archives of the consenting patients were also explored to verify the duration of T2DM.

The HbA1c levels were measured as described elsewhere.^14,19  In summary, HbA1c levels were recorded by a blinded investigator (κ = 0.9) using a calibrated commercially available kit (QuoTest, E-K-F Diagnostics, Magdeburg, Germany).

Dental implants of lengths and diameters ranging between 6 and 8 and 4 and 4.8 mm from a standardized implant system were assessed in the present study (soft tissue level implants, Straumann, SLA Active implant system, Basel, Switzerland). All implants assessed were placed under local anesthesia by an oral surgeon in the tuberosity region (zygomatic bone) posterior to the sinus. In summary, in all groups, full-thickness mucoperiosteal flaps were raised, and an osteotomy was performed at a drilling speed of 2000 revolutions per minute under copious irrigation. In all groups, the implants were placed using an insertion torque of 30–35 Ncm. In all cases, soft-tissue closure was performed using nonresorbable sutures (UNIFY 3/0 e-PTFE surgical sutures, Sunnyvale, California). Prosthetic loading (using screw-retained restorations) was done 3–3.5 months after implant insertion. All implants placed in the tuberosity were used as part of a full mouth prosthesis connected to implants placed in the maxilla (teeth #18, #14, #13, #11, #21, #23, #24, and #28). All implants were placed and restored by a trained prosthodontist.

In all patients, peri-implant GI,²⁰  PD,²¹  and PI²⁰  were measured by a skilled and standardized examiner (κ = 0.89). These measurements were performed on 6 surfaces per tuberosity implant (midlingual/palatal, distolingual/palatal, mesiolingual/palatal, distobuccal, midbuccal, and mesiobuccal). In this study, crestal BL was calculated as the perpendicular distance from 2 mm under the abutment-implant junction to the alveolar crestal height. This calculation was done on digital radiographs, which were taken using the long cone paralleling technique.²²  A positioner (X-ray Holders, KerrHawe.SA, Bioggio, Switzerland) was positioned on 30.5- × 40.5-mm size film (Kodak-Ultraspeed size-II Dental-Film, Kodak, Rochester, New York) parallel to the long axis of the implant and right angled to the X-ray cone.²² 

The methodology and results were reviewed by an independent statistician. Statistical analysis was done using computer software (SPSS, Version 20, Chicago, Illinois). Group comparisons were done using the Student t test. Sample-size estimation was done from the data obtained through a pilot study. Sample-size estimation was done based on the results obtained from a pilot investigation using software (nQuery Advisor 5.0, Statistical Solutions, Saugus, Massachusetts). The estimation was based on the supposition that a mean difference of 0.5 and 1 mm in marginal bone loss and PD, respectively, should be detected at a significance level of 0.05. It was estimated that inclusion of at least 10 patients per group would provide an estimated 95% to the study with a 5% error.

In total, 20 male patients with medically diagnosed T2DM and 12 male patients without T2DM were included. Among patients with T2DM, 10 and 10 individuals had poorly and well-controlled T2DM, respectively. There was no statistically significant difference in the mean age of individuals in all groups. The mean HbA1c levels were significantly higher in patients with poorly controlled T2DM (9.2 ± 0.7%) compared with well-controlled T2DM (4.8 ± 0.3%; P < .01) and nondiabetic individuals (4.6 ± 0.3%; P < .01; Table 1).

The crestal BL on the mesial (P < .01) and distal (P < .01) surfaces, PD (P < .01), PI (P < .01), and GI (P < .01) were significantly higher around implants placed in the anterior and premolar/molar region of the edentulous maxilla among patients with poorly controlled T2DM compared with patients with well-controlled T2DM and patients without T2DM (Table 2). There was no significant difference in peri-implant PI, GI, PD, and crestal BL on the mesial and distal surfaces around implants placed in the anterior and premolar/molar region of the edentulous maxilla of patients with well-controlled T2DM and individuals without T2DM (Table 2).

Among implants placed in the tuberosity, crestal BL on the mesial (P < .01) and distal (P < .01) surfaces, PI (P < .01), PD (P < .01), and GI (P < .01) were significantly higher among patients with poorly controlled T2DM compared with patients with well-controlled T2DM and patients without T2DM (Table 3). There was no significant difference in peri-implant PI, GI, PD, and CRESTAL BL on the mesial and distal surfaces of all implants placed in the maxillary arch of patients with well-controlled T2DM and individuals without T2DM (Table 2). Group-wise, there was no statistically significant difference in peri-implant distal and mesial crestal BL, PD, and GI among implants placed in the zygomatic region compared with implants placed in the anterior and posterior maxilla of patients with poorly and well-controlled T2DM and patients without T2DM (Tables 4 to 6).

The present study was based on the hypothesis that, under optimal GC, there is no difference in the survival of implants placed in the zygomatic bone of edentulous patient with and without T2DM. To the authors' knowledge, the present study is the first long-term follow-up investigation to assess the impact of glycemic maintenance on the peri-implant clinic-radiographic inflammatory parameters. The results reported in this study are in support of the hypothesis as there was no statistically significant difference in the crestal BL, GI, PD, and PI around all implants placed in the edentulous maxilla. Various elucidations may be postured in this context. Studies^23,24  have shown that proinflammatory cytokines such as interleukin (IL)1-β and tumor necrosis factor-α are more often expressed in the peri-implant sulcular fluid of patients with hyperglycemia compared with diabetic patients with a satisfactory glycemic status and individuals without DM. Similarly, in a recent study, Akram et al¹⁹  compared the levels of advanced-glycation end-products (AGEPs) in the gingival crevicular fluid (GCF) samples collected from patients with and without periodontitis. The results showed that AGEPs were more often expressed in the GCF of patients with than without periodontitis. Interestingly, in a recent study, Al-Rabiah et al²⁵  proposed that expression of AGEP levels in the peri-implant crevicular fluid (PCF) is directly associated with glycemic status in patients with T2DM. The authors of the present study support the results reported in the study by Akram et al¹⁹  and Al-Rabiah et al²⁵  and simultaneously hypothesize that impairment in glycemic status (as evident in patients with poorly controlled T2DM) enhances the expression of AGEP in the peri-implant sulcular fluid of all implants including those placed in the zygomatic area, thereby augmenting soft tissue inflammation and accelerating crestal BL in patients with poorly controlled T2DM than patients with well-controlled T2DM and medically healthy individuals. The authors therefore perceive that under optimal glycemic control the load of clinical (Bleeding on probing, PD, and crestal BL) and immunologic (destructive cytokines such as IL-6) inflammatory markers is markedly reduced, which in turn contributes toward implant soft tissue and BL stability.

It has been reported that deprived living conditions and underprivileged education standards are often manifested in patients with DM compared with individuals without T2DM.⁹  Such factors may compel individuals to neglect their oral health maintenance and focus on attaining the basic necessities of survival. Moreover, it has also been reported that the education status of the patient plays an important role toward achieving glycemic control in patients with DM.²⁶  It is worth stating that, in the present study, 80% of patients with poorly controlled T2DM were not undergoing yearly medical evaluations for their overall health, and only 20% individuals reported that they were visiting their oral health care providers biannually. In contrast, majority of the systemically healthy individuals and patients with well-controlled T2DM were undergoing routine yearly medical check-ups and were also visiting their oral health care providers biannually. These factors may have also contributed toward maintenance of glycemic levels in patients with well-controlled T2DM and status of dental implants. Because a bidirectional relationship exists between oral and systemic health,^27,28  it is important to educate patients with DM about the detrimental effects of hyperglycemia on oral and systemic health and at the same time illuminate the importance of oral health. Community-based efforts in this regard may help improve the overall quality of life of these patients.

One limitation of the present study is that peri-implant clinic-radiologic investigations were limited to the edentulous maxilla. This was primarily done because the focus of the present investigation was on implants placed in the zygomatic bone, and they were compared with similar implants inserted in anterior and posterior locations of the same jaw. Another limitation is that the radiographic investigations were based on 2-dimensional radiographs. However, cone-beam computerized tomographic analysis would yield more information in terms of bone density around implants inserted in T2DM patients with varying glycemic statuses. This warrants additional well-designed and power-adjusted studies. Further studies focusing on the use of 3-dimensional computerized tomographic imaging are needed to assess bone levels and related bone loss around implants placed in different jaw locations.

Optimal GC is essential for the long-term stability of zygomatic plants in patients with T2DM.

The authors are grateful to the Research Supporting Project at King Saud University for funding through Research Supporting Project No. (RSP-2021-44).

The authors thank the statistician, Tasleem Sheikh, for statistically evaluating the raw data.

The authors declare no conflicts of interest.