Evaluation of clinical performance and survival rate of Straumann dental implants in Saudi Population based on cross-sectional study

Risk indicators of peri-implantitis is still contradictory and somehow unclear in present literature therefore efforts should be done for better understanding of the exact etiology of peri-implant disease progression. The present study aimed to assess risk indicators associated with peri-implantitis by observing the changes in several periodontal parameters after implant placement. This cross-sectional study included 213 female and 271 male patients aged 26–87 years, who received 484 titanium implants (Straumann, Switzerland) at King Saud University’s Dental College, Saudi Arabia. Patients were called for dental visits. During these visits; full clinical and radiographic assessment of implants were done. The periodontal pocket depth (PPD) was greater around implants placed at grafted sites than non-grafted sites and around bone-level implants than tissue-level implants. The plaque index (PI) was associated with poor oral hygiene. There was a strong association between graft (yes/no) and bleeding on probing (BOP). Patients with good oral hygiene showed high radiographic bone stability. Keratinized tissue width < 2 mm was associated with a higher PPD, higher PI, higher BOP, more edematous gingiva, and more exposed implant threads on radiography. In patients receiving implants, poor oral hygiene status and inadequate keratinized tissue level can be proposed as risk indicators for developing periimplantitis due to strong association found between them and developments of peri-implantitis.

As more dental implants were in place, more long-term complications were observed upon different implant placement scenarios. Several theories and thoughts were discussed through dental implant literature by several case reports, series.
Efforts have been made to understand the primary etiological causes of these diseases. Although speculations pointed that basic principles of biofilm's formation are similar to periodontal and implant disease due to their presence in similar oral environment 5,6 . Overall it is crucial to understand that pathogenic microbiota still remains the main etiological factor of developing periimplantitis. Furthermore, several studies have shown that microbiota may be different due to the presence of inert materials mainly titanium in the ecological setting 6,7 . Another factor which plays major role in microbial changes is the difference of blood supply as well as cytokines surrounding the dental implant comparable to natural tooth 8 .
Furthermore, it is essential to identify peri-implantits. Additional risk factors and indicators that can cause more destructions and failures of implants in order to understand the progressive pathway of peri-implant disease [9][10][11][12] . Several risk factors were proposed based on longitudinal studies and risk indicators based on other cross-sectional studies have been debated to be additional influencers on peri-implantitis. These include and not limited to; risk factors such as smoking, diabetes and risk indicators such as osteoporosis and local factors including restorative part mishaps and presence of excessive cement 13,14 . Furthermore, this cross-sectional study aimed to assess risk indicators associated with different stages of peri-implantitis at implant-based analysis by observing changes in several periodontal parameters over a period of three years post-implant placement in Saudi Arabia.

Materials and methods
Study design and participants. The study was conducted on patients receiving conventional length (> 6 mm), non-turned, 2-and 3-piece titanium implants* (Straumann, Switzerland) in King Saud University's Dental College, Riyadh, Saudi Arabia during the period 2015 to 2018. The patients were randomly included and scheduled for dental appointments; all clinical parameters were collected from June 2018 to September 2019 during regular implant maintenance visits. Furthermore, all clinical measurements were taken by a single blinded trained and calibrated investigator to exclude possible operator-dependent bias.
Inclusion criteria. In accordance with Konstantinidis et al. 15 and Schwarz et al. 16 for patient selection, sample of the study consisted of systemically healthy partially edentulous patients with one or more missing teeth being replaced by single crown implant-supported restoration with a minimum period of 6 months of functional occlusal loading during the appointment for evaluation. Implant surgical operations and prosthetic restorations were all performed in the same institute.
Exclusion criteria. The following exclusion criteria were defined: (1) any uncontrolled systemic diseases that could influence the implant therapy outcome (e.g., diabetes [HbA1c > 7], osteoporosis); (2) Smoking; (3) pregnancy or breastfeeding in women; (4) intake of medications having an effect on bone turnover and mucosal healing (i.e., steroids, antiresorptive therapy); (5) antibiotic use for a medical or dental reason within the 2 months prior to the examination; (6) any restorations that did not allow for the calculation of periodontal pocket depths(PPD); (7) inability or refusal to sign the informed consent form and (8) the absence of baseline radiographs taken at the time of placement of the implant or final crown 15,16 . Anamnestic data and implant site characteristics. The following study variables were assessed at the time of final examination: (1) age (2) gender. The following implant site characteristics were considered: (1), implant type (bone level vs. tissue level), (2) implant size, (3) implant location (maxillary vs. mandibular arch, (4) grafting the area (yes/no), (5) graft type (Autograft vs. Allograft vs. xenograft) and (6)  Clinical measurements. The clinical parameters were assessed for each implant. Periodontal probing depth (PPD) was measured using plastic probe (11 Colorvue Probe, Hu-Friedy) by inserting the probe within sulcus area with gentle pressure (less than 0.25Ncm) around the neck of an implant at three points buccal and three points lingual to the implant having the probe placed parallel to the crown of the implant at mid buccal and mid lingual points and 10 degree tilted inward at the proximal points to the nearest mm 17 . Bleeding on probing (BOP) was assessed by either the presence (+) or absence (−) of bleeding at the site of probing immediately after periodontal pocket depth measurement 2 . Plaque index (PI) was assessed by either the presence (+) or absence (−) of Plaque on four surfaces (mesial, distal, palatal and buccal) of crown after placing disclosing agent* (Hu-Friedy Mfg. Co., Chicago, IL, USA). The measurements of PPD, BOP, and PI were performed at six aspects per implant: mesio-buccal, mid-buccal, disto-buccal, and respective lingual/palatal sites 3 . Gingival color and consistency were evaluated via direct visual assessment, i.e., visibility of the periodontal probe , Gingival changes were determined by assessing redness area visible between the level of the inter-proximal papillae and the gingival margin.as redness is an indication for inflammation color pink is indication or gingival health 4 .
Keratinized tissue width (KTW) of presence or absence of (≥ 2 mm) was assessed from the peri-implant marginal mucosa to the muco-gingival junction (MGJ) at the buccal and lingual side of each implant. KTW was measured round the implant and calculated by the mean of four margins (buccal, lingual, mesial, and distal) by the aid of the periodontal probe. The former was measured from the peri-implant marginal mucosa to the mucogingival junction (MGJ) at the buccal and lingual marginal portion of the implant's mucosa 6 . Finally, standardized periapical radiographs were taken at the time of the clinical examination with the long cone paralleling technique and film holders (Rinn XCP, Dentsply Corporate, PA, USA) and compared with a baseline radiograph taken at the time of prosthesis installation for bone level confirmation at the same facility 14  www.nature.com/scientificreports/ were scanned to obtain standardized digital images with a resolution of 1200 dpi. These images were imported and analyzed using specialized computer software (Image J v 1.49, Research Services Branch, National Institute of Health, Bethesda, MD, USA). The calibration of the pixel/mm ratio was performed using the length of the implant as a fixed reference point to compensate for potential radiographic distortion. For the assessment of bone loss, the radiographic distance between the implant shoulder level and the most coronal bone-to-implant contact level was measured mesially and distally, parallel with the long axis of the implant. The same-blinded examiner performed all radiographic measurements 18 .
Data analysis. Data  www.nature.com/scientificreports/ was used to assess the association between the categorical study and outcome variables. Karl Pearson's correlation coefficient was used to quantify the relationship between attached gingiva values and PPD scores. A p-value of < 0.05 was used to report the statistical significance of results.
Ethical approval. The present cross-sectional study was carried out in accordance with the Helsinki Declaration of 1975, as revised in 2013. The protocol used in this study was approved by the Institutional Committee of Research Ethics at King Saud University, Riyadh, Saudi Arabia (87,563). Each patient was given a detailed description of the procedure, and informed consent was obtained prior to participation in the study.

Results
From 2045 screened patients' records, 213(48.1%) female patients and 271 (51.2%) male patients aged 26-87 years (mean, 60 ± 8.6 years) were selected due to sufficient clinical data. Among these selected patients, a total of 484 dental implants were inserted, 251 (56%) into female patients and 233 (49%) into male patients. According to definition given, out of 484 implants, 201 (42%) presented with BOP on more than one surface area around the implant and were therefore diagnosed with peri-implant mucositis. Further analysis using means of periapical X-rays, 115 (23.76%) revealed peri-implant marginal bone loss, and therefore, out of all implants included in present study, 42% sites showed peri-implant-mucositis while 23.76% showed peri-implantitis.
Periodontal pocket depth (PPD). The mean PPD was deeper around implants placed in grafted sites versus non-grafted sites (6.82 ± 2.27 mm) versus (4.60 ± 2.0 mm), this difference was statistically significant p < 0.001. Additionally, It showed that PPD was statistically significantly deeper around bone level implants in comparison to tissue level (6.70 ± 2.1 mm) versus (4.61 ± 2.0 mm), p < 0.001). Furthermore, PPD was also shown to be statistically significant in patients exhibiting poor oral hygiene in comparison to individuals either with fair or good oral hygiene ( Bleeding on probing (BOP). The distribution of BOP across the study variables showed a highly statistically significant association between graft (yes/no) and BOP (83 ± 45.6%) versus (5 ± 55.6%), p < 0.001).

Discussion
Due to the advancements made in the field of Dentistry, replacement of teeth by means of dental implants has become a common treatment modality in recent years. Success of implant depends on various systemic and local factors near the implant. Due to these factors, implant failures may take place either as early failure which can be observed immediately postsurgical implant placement and its main reason is failure to establish proper osteointegration initially during wound healing period, while late failure can occur after occlusal loading. This was suggested due to breakdown of osteointegration occurred preloading. To avoid such unwanted outcomes a carful assessment of various factors that might contribute to the implant failure is crucial.
The present study is aimed to assess the factors influencing the survival of Straumann dental implants in Saudi population over a 3 three years period. A total of 484 dental implants were evaluated for identifying risk indicators by assessing several periodontal parameters.
In the present study PPD was significantly associated with presence of keratinized tissue width, and oral hygiene status. In relation to grafting and implant type, grafted sites showed significantly deeper PPD than non-grafted sites and bone level implants showed deeper PPD compared to tissue level implants. These results were in accordance with French et al. who found greater probing depths at grafted sites when compared with non-grafted areas 19 .
BOP was measured as to whether bleeding is present or absent to recognize presence of inflammation, dental implants however, tend to bleed more upon probing with less probing force when compared to natural tooth 20 . Positive BOP was observed in 42% of implants that were examined, which is in accordance with other previously published studies. French et al. used modified Sulcular bleeding index and found BOP is associated with mucositis 19 . In a similar study by Buser et al. 21 using Mombelli's bleeding index which reported that on mere punctuating, bleeding spots merely suggests injury to the perimplant supporting tissues and mombelli's class 2 indicates mucositis, further they concluded that mucositis does not necessarily progress to peri-implantitis overtime 22 . Van velzan et al. using the same index as Buser et al. in the above-mentioned study, has found 20% of the implant sites showed BOP 23 .
Recently in a study carried by Stoker et al. BOP was reported in 14% of the sites examined 24 .    www.nature.com/scientificreports/ Costa FO et al. reported bleeding on peri-implant probing, periodontal probing depth, and the presence of periodontitis were associated with a higher risk of developing peri-implantitis 25 .
The BOP positive sites reported in this study are relatively higher when compared BOP reported in the previously published studies and this could be due to the difference in the index used to record the BOP. In the current study BOP was assessed as present or absent, whereas other published studies used more specific bleeding on probing indices.
One of the very interesting findings in this study was the impact the amount of keratinized tissue width around the dental implants, which was highlighted in many systematic reviews [26][27][28][29] . In the present study, sites with < 2 mm width of keratinized tissue showed significantly more edematous soft tissue when compared to those with > 2 mm KTW. These results are in accordance with Souza et al. who found implant sites with < 2 mm KTW showed more inflammation. There are several controversies regarding KTW around the implant and its importance, Wennstrom 2012 30 and Esper 2012 31 showed in their study that there was no major difference in the clinical parameters like plaque control, gingivitis, BOP and PPD as was seen in areas in with and without sufficient KTW.
Gunpinar et al. reported that when risk factors for periimplant disease were analyzed, in addition to PI and periodontitis, BOP, higher PPD and KTW width less than 2 mm were associated with occurrence of peri-implant mucositis and peri-implantitis 32 .
In the present study radiographic changes were assessed as having no change in bone level and threads exposed. Patients' poor oral hygiene was found to be significantly associated with radiographic thread exposure. This might suggest that failure to control patient oral hygiene could be a risk factor contributing to future inflammation development around the implant and consequently implant failure.
Furthermore, the present study findings revealed that lack of a minimum of 2 mm of KTW was associated with radiographic implant thread exposure. Gunpinar et al. presumed that less KTW is linked to the plaque accumulation than the bone loss which is noticed around implants as the higher PI were scored in implants with KTW less than 2 mm 32 . Bengazi et al. 33 in their study reported higher crestal resorption and apical soft tissue positioning of implants placed in areas with insufficient KTW. In a recent study Van Ekeren et al. 34 reported significantly lower crestal bone change in bone-level implants placed in an initial keratinized tissue thicknesses of 2 mm or less. There is enough evidence to highlight the importance of placing dental implants with enough keratinized tissue to avoid future complications such as bone loss around the implant [30][31][32][33][34][35][36] .
When planning implant placement various factors such as oral hygiene, keratinized tissues, bone must be considered, overlooking these factors can have a negative effect on the long-term success of the implant as reported here.
Several limitations had been observed in present study which include mainly inherent limitations of retrospective studies and inconsistent results from using different indices and tools in the methodology. In addition, the lack of follow up due to the retrospective design can affect the observation of a true association between different studied variables and outcomes measured. Additional limitation can be explained by collecting the present sample from one institute which cannot be highly efficient to translate the present findings to whole society of patients with Straumann implants and also having a considerably overall moderate sample size. Furthermore, the exclusion of classical and well-known risk factors related to implant diseases.

Conclusion
Within the limitation of this study, the data presented supports the previously published data that bone loss with exposing the implants threads was significantly associated with poor oral hygiene and it highlighted about the importance of controlling variables like oral hygiene status and keratinized tissue level which would help to have a good radiographic stability of the implants. Well controlled long-term prospective cohort studies are required to further assess factors affecting survival of Straumann implants.

Availability of data and materials
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Study variables
Radiographic findings Χ 2 -value p-value No change 1 thread exposed 2 threads exposed 3 threads exposed 5 threads exposed or more