Implant stability of narrow diameter implants in hyperglycemic patients—A 3‐month case–control study

Abstract Objectives The aim of this prospective case–control study was to compare the development of implant stability quotients of narrow diameter implants in patients with type 2 diabetes mellitus (T2DM) and healthy individuals within the first 3 months after implant insertion. Methods Sixteen patients with T2DM (HbA1C > 6.5%) as test group and 16 nondiabetic patients (HbA1C < 5.9%) as the control group were evaluated. All patients received narrow‐diameter tissue level implants in an edentulous area posterior to the canine. The implant stability was measured by means of resonance frequency analysis after 3 days, 7 days, 4 weeks, and 3 months postplacement. Statistical analysis of intergroup differences and correlation to HbA1c values and treated jaw was performed in PRISM 8. Results The means for implant stability quotients showed a significant increase between Day 3 and 3‐month assessment in both groups. No significant differences between study groups and no correlation of implant stability to HbA1c were found. Conclusion The present study shows encouraging clinical outcomes for narrow‐diameter implants inserted in the posterior zone in patients with uncontrolled T2DM.


| INTRODUCTION
Type 2 diabetes mellitus (T2DM) is a metabolic disorder with an increasing prevalence in both developing and developed countries. It is characterized by hyperglycemic blood serum as a result of either insufficient insulin production, defective insulin receptor function, or both (Zimmet et al., 2016). Subsequently, T2DM patients suffer from impaired wound healing due to defective tissue proliferation, remodeling, and exacerbated inflammation (Baltzis et al., 2014).
The number of patients undergoing restorative dental therapy using dental implants has grown significantly during the last decades (Armas et al., 2013). In some cases, bone resorption or periodontitis results in a diminished horizontal and vertical alveolar ridge dimension, making surgical augmentation procedures before implant insertion necessary (Chiapasco et al., 2009). However, extensive reconstructive surgery of the edentulous ridge is not always a viable treatment option. A recent systematic review identified T2DM-associated vascular and immunological pathologies as a major risk factor for bone augmentation success (Moy et al., 2000).
Narrow-diameter implants (NDI) were developed for sites with diminished ridge dimensions, which result from numerous clinical reasons and a plethora of studies indicate their clinical success (Klein et al., 2014).
By circumventing the need for invasive augmentation procedures and thus the wound healing burden, NDI present a suitable treatment option reducing the wound healing burden in T2DM patients with a diminished alveolar ridge dimension (Friedmann et al., 2021). Recent meta-analysis and literature reviews attest that NDI are a feasible hardware choice in the posterior region (Schiegnitz & Al-Nawas, 2018). Moreover, Ma et al. reported that the use of NDI instead of regular diameter implants with bone augmentation procedures did not exhibit differences in survival rates within the reported period .
Osseointegration, the direct anchorage of the dental implant to the bone, is the major biological prerequisite for implant success.
Clinically, successful osseointegration is measurable by implant stability (Albrektsson & Zarb, 1993;Meredith, 1998). In terms of NDI, a study conducted by Pommer et al. showed that a reduced implant diameter had no influence on primary stability as measured by resonance frequency analysis (RFA) (Pommer et al., 2014). However, the clinical literature suggests a significant correlation between reduced implant diameters, the site of implant placement, and declining primary implant stability (Quesada-García et al., 2012). To this day, studies on the topic of primary implant stability in T2DM patients are scarce. A prospective clinical study by Oates et al. reported a correlation between impaired implant stability and the amount of glycated hemoglobin (HbA1c); however, this study neither focused on the implant diameter nor on chemically modified implant surfaces (Oates et al., 2009)

| Sample size considerations
The sample size was calculated with G*Power (Faul et al., 2007). For effect size considerations, we referred to the mean maximum change of implant stability relative to baseline as published elsewhere (Oates et al., 2009). However, for our study, we anticipated less significant differences between study groups, due to the chemical modification of the implant surface and the relatively high HbA1C (<8.1%) reported in the previous study. Thus, the anticipated effect size was set at d = 1.148, implying a minimum sample size of n = 26 (α = .05, 1−β err prob = 0.8).

| Statistical analysis
For all data obtained, mean and standard deviation were calculated. were calculated by Pearson's correlation coefficient. The level of significance was set at p = .05.

| RESULTS
Thirty-two patients with a mean age of 67 years were eligible for further analysis. The mean HbA1c value for the hyperglycemic test   and 3). Furthermore, no significant difference in stability was found between implants in the maxilla or the mandible (Figure 3). The

Pearson coefficient revealed no significant correlation between
HbA1c and ISQ. In the maxilla, however, the implant position was positively correlated with the HbA1c at visit 5 ( Figure 4).

| DISCUSSION
The objective of this prospective case-control study was to evaluate the osseointegration process of NDI into the native posterior alveolar bone in T2DM and normoglycemic patients. The implant stability quotients were compared between groups based on mean values over a 3-month observation period and correlated to the underlying HbA1c and the implant-receiving jaw. The data suggest that NDI display no significant limitations regarding osseointegration quality in T2DM patients. Correspondingly, the data analysis demonstrates that the implant stability quotient is not correlated to the HbA1c amount.
The presented data are not in line with previously published results from a prospective pilot study (Oates et al., 2009 Gu et al., 2013). Moreover, various preclinical studies affirm the superior properties of the SLActive over the SLA surface in terms of implant integration (Alayan et al., 2017;Schlegel et al., 2013). In light of these findings, the idea that chemically modified surfaces may have ameliorated hyperglycemia-induced deceleration of periimplant bone healing around NDI appears rational. Nevertheless, sufficient randomized controlled clinical trials are lacking to verify this theory indefinitely (Stafford, 2014).
In our study, the mean ISQ value increased constantly in both groups, from 55.87 (±5.992) initially to 63.84 (±6.052) before loading in the T2DM group and 51.41 ± (9.618) to 63.84 ± (6.175) in the control group, respectively (Table 2). In comparison to the values assessed at integrated implants with a greater diameter but similar design, the preload ISQ values in our study were diminished, which may serve as a sign of reduced implant stability (Baldi et al., 2018;Bornstein et al., 2009;Scarano et al., 2006). Nonetheless, the thresholds for appropriate ISQ values obviously differ between various implant systems, and an ISQ range from 55 to 65 is considered safe for Straumann implants according to the published data reviews (Sennerby & Meredith, 2008;Sennerby, 2013). In addition, the implant diameter and insertion torque may also exert a significant influence on the ISQ value (Huang et al., 2020). A recent prospective clinical trial concluded that higher implant diameters are correlated with higher ISQ values (Kim et al., 2017). Therefore, the anticipation of diminished ISQ at NDI appears rational.
Surprisingly, we discovered a significant positive correlation between HbA1c and the ISQ at visit 5 for implants inserted into the maxilla (Figure 4 and Table 3). A previous randomized controlled trial reported a similar observation, disclosing a tendency for higher ISQ values in patients with HbA1c levels exceeding 9.6% compared to patients with HbA1c levels below 9.6% (Khandelwal et al., 2013). However, the authors concluded that varying baseline implant stability quotients may have been the rationale for this finding. In our study, only seven patients received implants in the maxillary area, while neither the patient's age nor the bone quality was taken into account for the calculation.
Therefore, the chance that this correlation was detected accidentally is highly probable. Moreover, our finding contradicts the current knowledge and understanding of bone metabolism and biology under diabetic conditions (Hu et al., 2019;Marin et al., 2018). In any case, further research in a larger study population is necessary to substantiate this discovery.
In this study, all implants were osseointegrated after the 3-month observation period. In conjunction with the outcome of our analysis,

ACKNOWLEDGMENTS
The authors declare that they do not have any commercial, proprietary, or financial interest in the products or companies described in this article. The study was supported by a restricted grant including the donation of the NDI's by the Institut Straumann AG.

CONFLICTS OF INTEREST
The authors declare no conflicts of interest.

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.

ETHICS STATEMENT
This study was performed in line with the Declaration of Helsinki. Abbreviations: CI, confidence interval; T2DM, type 2 diabetes mellitus.