The Effect of Age of Titanium Dental Implants on Implant Survival and Marginal Bone Resorption: A 5-Year Retrospective Follow-Up Study

Dental implants are widely used in the rehabilitation of missing teeth, and the 10-year survival rate of SLA implants is 98.8%.¹  Implants are chemically attached to the bone by osteointegration, which is affected by many factors. Implant-related factors include width, length, shape, and surface structure, patient-associated factors include systemic diseases and smoking, and surgical factors include technique and the surgeon's experience.^2–4  In recent years, studies have focused on implant surface properties, which can be changed and improved.^5,6  Technology advances make it possible to change implant designs and improve the chemical, physical, and biological properties of the implant material by using different implant surface modification techniques.^7,8 

Titanium, one of the most preferred dental implant materials., has advantages such as high corrosion resistance, low module of elasticity, high fracture strength, and tolerance to surface modifications.⁹  Alloys and surface roughening methods are used to further improve the physical, chemical, and biological properties of titanium.¹⁰  The ratio of bone implant contact is known to be higher on roughened implant surfaces than flat implant surface.^11,12 

The literature provides no precise information about the parameters for providing optimal osseointegration and which minimum osseointegration parameter is sufficient for the implants to function under chewing forces. It is important to understand the biology of osseointegration and the relationship between the implant surface and the bone. In histomorphometric studies, the rate of bone implant contact was found to be at the maximum of 65%.^11,13  This rate is up to 90% in newly produced implants.¹⁴  Although an adequate bone-healing period is maintained before loading, it is not clear why the ratio of bone implant contact does not reach 100%.¹⁵  Recent cell culture studies have demonstrated that the osteoconductivity, hydrophilicity, and biological capacity of titanium decreased over time; this phenomenon was described as the biological aging of titanium.^14–17  In the literature, no study was found to evaluate the effects of implant age and biological aging on clinical status. The aim of this study was to evaluate the effects of implant age (time from date of production to date of operation) on bone resorption and survival rate of SLA titanium dental implants.

This nonrandom, convenience sample, retrospective pilot study was conducted using records of patients' admitted to the Oral and Maxillofacial Surgery Clinic between May 2010 and January 2014 to receive dental implant therapy in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Two hundred implants of 64 patients were included in the study. The study was approved by the Non-Interventional Clinical Research Ethics Committee (2019/02-03).

The inclusion criteria were no systemic disease; age 18 years or older; completion of all dental treatments before the procedure; no previous restorations in the edentulous area; positive oral hygiene; use of antibiotic, nonsteroidal anti-inflammatory drug, and chlorhexidine-containing antibacterial mouthwash in the first week after the operation; recorded date of implant production and/or expiration and operation; use of the same implant system (SLA Surface Standart Plus, Roxolid Implant, Institute StraumannAG, Basel, Switzerland); rehabilitation with flat abutment and cemented fixed prosthetic restoration (crown or bridge); implants with primary stability between 35 and 50 Nm; and implants placed at bone level (the rough-polished surface border/line placed at the bone level). Exclusion criteria were smoking, missing or inaccessible radiographic records, undocumented date of production and/or expiration date of implant brand, bone augmentation procedures, medication and/or interventional procedures for peri-implant mucositis and/or peri-implantitis during 5 years of follow-up.

Patients were followed up once every 6 months for 5 years. Pain, mobility, bleeding and/or suppuration on gentle probing, swelling and/or discoloration of the marginal soft tissue and probing depth, and patients' oral hygiene level were evaluated in clinical examination for peri-implant mucositis and/or peri-implantitis. Radiographic examinations were done using intraoral parallel periapical and panoramic radiographs. After clinical and radiographic evaluations, patients diagnosed with peri-implant mucositis and/or peri-implantitis were advised to increase their oral care. Initially, no interventional procedures were performed; however, patients who continued to have symptoms (bleeding on probing, pain, pus drainage) were managed surgically.

Radiographic measurements were performed on periapical radiographs with the parallel technique. Periapical radiographs taken immediately after the operation were used to check whether the implants were at the bone level. The amounts of mesial and distal marginal bone resorption around the dental implants were measured. Periapical radiograph measurements were carried out on the same computer (Intel Core I5-6200U CPU @ 2.4 GHz, Windows 10 Pro, 64 bit operating system, 1920 × 1080 resolution, HP Desktop-76JJRSC, Hewlett-Packard Development Co, LP, Houston, Tex) with ImageJ software (version 1.52, LOCI, University of Wisconsin). Each patient's periapical radiograph(s) were calibrated using the distance between the 2 grooves of the implant (1 mm for 3.3-mm-diameter implants and 1.25 mm for other diameters) as a reference. Mesial and distal marginal bone resorption was determined by measuring the distance from the rough-polished surface border of the implant to the mesial or distal marginal bone (Figure 1). For each implant, the production date was extracted from the date of surgery, and implant age was calculated (in months). Implants were divided into 2 groups according to the age of implant: group 1 = 0–3 months; group 2 = 36–41 months.

The NCSS (Number Cruncher Statistical System) 2007 (Kaysville, Utah) software was used for statistical analysis. Descriptive statistical methods (mean, standard deviation, median, frequency, percentage, minimum, maximum) were used to express the data. The normal distribution of quantitative data was tested with the Shapiro-Wilk test and graphical investigations. The Student t test was used to compare the normal distribution of quantitative variables between 2 groups, while Mann-Whitney U test was used to compare the difference between 2 independent groups of nonnormally distributed quantitative variables. The Pearson χ² test was used to compare the qualitative data. Spearman correlation analysis was used to evaluate the relationships between quantitative variables. Statistical significance was set as P < .05. The methodology was reviewed by an independent statistician.

The 64 participants ranged in age from 22 to 70 years, with a mean age of 51.91 ± 10.78 years. By sex, 40.6% (n = 26) of the patients were men and 59.4% (n = 38) were women (Table 1).

Implant ages were between 0 and 41 months. We observed 41% (n = 82) of the implants were between 0 and 3 months old, and 59% (n = 118) were between 36 and 41 months old. Furthermore, 100% (n = 200) of the implants survived and maintained their function. The mean mesial marginal resorption measurements were 0.60 ± 0.65 mm, and the mean distal marginal resorption was 0.77 ± 1.07 mm. In terms of location, 8% (n = 16) of the implants were in the maxillary anterior region, 46% (n = 92) were in the maxillary posterior region, 11% (n = 22) in the mandibular anterior region, and 35% (n = 70) in the mandibular posterior region (Table 2).

There was no statistically significant difference between the study groups in terms of age and sex (P > .05; Table 3). No statistically significant relationship was found between patient ages and the amounts of mesial and distal marginal bone resorption around implants (P > .05). No statistically significant difference was found between mesial and distal marginal bone resorption measurements around SLA implants according to sex (P > .05). Finally, there was no statistically significant difference between the mesial and distal marginal resorption measurements around implants according to implant age (P > .05; Table 4).

This pilot study evaluated the effect of implant age on implant survival and marginal bone resorption. Dental implants are usually stored in sterile boxes for 5 years and are used at any time during this period.¹⁷  The time-related deterioration of the osteoconductivity of titanium dental implants over the date of manufacture is called “biological aging,” and it has been shown that the implant shape, surface roughening, and surface cleaning affect implant aging.^14–17  Accumulation of hydrocarbons on the surface of titanium under ambient conditions reduces the adhesion ability of blood proteins and osteogenic cells. As the ratio of hydrocarbons on the surface of titanium increases, the surface zeta potential changes from electropositive to electronegative. The initial hydrophilic structure of the surface turns to hydrophobic. This prevents negatively charged blood proteins and the extracellular matrix of the osteoblast cells from attaching to the implant surface.^18,19  The effects of biological aging of titanium have been demonstrated in implants up to 6 months old in cell culture studies. The present study included implants between 36 and 41 months old in the aged implant group, and it has been observed that biological aging of titanium does not affect the clinical success of dental implants.

Att et al¹⁴  cultured osteoblasts from rat bone marrow in novel, 3-day, 2-week, and 4-week implant discs. Osteoblast migration, binding and proliferation to titanium, alkaline phosphatase positive regions, and mineralized nodule regions were found to be significantly lower in aged titanium discs. In the cell culture environment, the number of osteogenic cells that bind to the aged implant surfaces after 3 hours of incubation was lower. Cell density and alkaline phosphate activity observed on the fifth day were lower on the older implant surfaces.¹⁵  However, it is unclear whether the number of attached cells increase over time, and the direction in which these parameters change over time is not known. Furthermore, the low number of osteogenic cells at the beginning may not be important for long-term osseointegration, and osteointegration may start with a small number of osteogenic cells and continue progressively in the 3-month healing period. In the present study, clinical success of older implants with 35–50 Nm primary stability was similar to that of newer implants. In clinical conditions, high primary stability and 3a -month healing period may change the deterioration of surface properties due to biological aging in the direction of osteointegration.

The effect of biological aging on osseointegration of implants cannot be solely be determined under cell culture conditions because it is not possible to imitate one-to-one clinical conditions in cell culture studies. Osseointegration is a multifactorial concept that includes local and systemic factors of the patient along with the implant's surface properties.^2–4  In animal studies, when push-in values were measured after a 2-week healing period of roughened implants with acid etch, the values for the new implant, 3-day implant, 2-week implant, and 4-week implant were 37 N , 36 N, 24 N, and 16 N, respectively. After a 4-week recovery, the push-in value of the new implant had increased to 49 N, and the value of the 4-week implant had increased to 29 N. The authors reported that the age of titanium negatively affected the success rate of osseointegration and the formation rate.¹⁴  In the in vivo studies of Suzuki et al,²⁰  the push-in value of sand-blasted implants was higher in new implants than in the 4-week-old implants, and the researchers confirmed the phenomenon of biological aging in vitro. When a new implant and a 4-week-old implant were compared, most of the new implants were covered with new bone, while the 4-week-old implants showed a limited amount of new bone. In addition, soft tissue was observed around 4-week-old implants between the new bone and titanium. After a 4-week recovery, the bone-implant contact rate reached 90% in the new implants, while this value was 58% in 4-week-old implants.¹²  The common result of these studies indicates that the biological aging of titanium reduces the stability of the implant with the rate of osteointegration. These data may be of particular importance in cases where immediate or early implant loading is performed. However, there is a routine waiting period of 3–6 months after implant placement. The success rate of 5–10 years in sand-blasted and acid-etched implants is high, ranging between 95.1% and 98.8%. In these studies, the recovery period was examined up to 4 weeks ,and the stability of the aged implants increased as the recovery period increased. Perhaps after longer recovery times, bone contact rates and push-in values of the implants will be similar to that of new implants, and the initial adverse effects associated with implant aging will not make a difference. Furthermore, although the studies were performed on animals, the primary stability of the implants was not addressed or ignored. The importance of the primary stability of implants in osseointegration cannot be excluded. In the present clinical study, the 5-years survival rates of new (0–3 months) and aged implants (36–41 months) were 100%, and there were no significant difference between the study groups in terms of marginal bone resorption. We think that a 3-monthshealing period for osteointegration tolerates biological aging of SLA titanium implants. In addition, it is possible that this biological aging phenomenon is limited to implants with adequate surface cleanliness (low hydrocarbon content on surface) at the time of production.

The fact that the study was composed of individuals with different personal characteristics may have affected the amount of marginal bone resorption. Although this study was a retrospective study, variables other than individuals were kept the same, such as implant surface properties or over-implant prosthesis type. This resulted in a low population number. These are the limitations of this study.

The present study revealed that the biological aging of titanium had no significant effect on 5-year survival rates and marginal bone resorption of SLA surface dental implants. After a 3-month recovery period, older implants had no adverse effect on implant survival and marginal bone resorption. Clinical success of older implants requires further investigation in future clinical trials. Therefore, the effect of biological aging of dental implants on implant success and osseointegration needs to be evaluated in further prospective, randomized, split-mouth clinical trials in larger populations.

Abbreviation

SLA:

sand-blasted and acid-etched

The authors thank Emire Bor (Expert Statistician, EMPIAR Statistical Consulting, İstanbul, Turkey) for her assistance in the statistical evaluation of the data and review of methodology.

The authors declare that they have no conflicts of interest.