Unlike orthopedic implants placed in an aseptic environment, dental implants are placed in the jaw bone and exposed to the oral cavity, which is a complex biological environment. Therefore, the early failure of implants might be affected by multiple factors. Previous studies have detailed various patient-, surgeon-, and biomaterial-related factors that can play a role in early implant failure [7, 17]; however, the diversity of implant systems has made it is difficult to achieve a consensus about them. The diagnosis and implant removal indication also vary between clinicians. Esposito et al. [6] suggested that early failure is characterized by a lack of osseointegration and the main clinically relevant criterion for the indication of implant removal is the mobility level of an implant. Other subjective signs, such as the patient experiencing pain or sensitivity, signs of infection, and peri-fixture radiolucency, could be improved through time in the healing process and preserving treatment.
Implant placement with sinus lifting and bone grafting is currently a widely used treatment approach in patients with inadequate vertical bone height in the posterior maxillary region to improve the bone quantity and implant osseointegration. Sinus augmentation is highly predictable, with a reported success rate of more than 95% [18]. The survival rate of implants placed in sinuses augmented using the lateral window technique varies between 61.7 and 100%, with an average survival rate of 91.8% [19]. However, several complications may develop, mostly due to disruption of the sinus membrane and displacement of grafting material into the sinus cavity. The incidence of odontogenic maxillary sinusitis after maxillary sinus lifting ranges from 0 to 20%. In the current study, all three cases of implant failure were linked to the sinus-lifting and bone-grafting procedures. Even though the implant demonstrated initial stability after installation, mobility was found after sinus symptoms developed. In cases 1 and 2, resorption and displacement of grafting material were observed. In case 2, a complication was detected 2 weeks after installation, and a change in the air-fluid level in the sinus was observed. Case 1 experienced a longer period of inflammation (one month after installation); therefore, a clearer pseudocyst with a well-defined border was allowed to develop. In case 3, the patient was treated with implant apex-cutting and MESS surgery initially to resolve the sinus irritation and inflammation and to preserve the non-mobile implant. The sinus symptoms were resolved after surgery; however, the peri-implant alveolar bone was subsequently resorbed and the implant failed to osseointegrate. The process of these three cases suggested that patient-related and technique factors could both have played an important role in the initial onset of odontogenic maxillary sinusitis and implant failure. In addition, biomaterial-related factors might have led to implant failure.
According to a meta-analysis study by Kim et al. [11], the only factors that had a significant impact on the rate of postoperative sinusitis were preoperative sinusitis and Schneiderian membrane perforation. Meanwhile, the only factors that affected implant failure were smoking and residual alveolar bone height. The authors found that the implant failure rate was 5.19 times higher when the residual bone height was less than 5 mm [11]. In the current report, the displacement of bone graft material into the sinus cavity was observed in cases 1 and 2, which suggests the presence of sinus membrane perforation and may be the main cause of acute sinusitis. The inflammatory products from acute sinusitis could damage the osteoconduction and bone remodeling of bone graft material and affect the osseointegration of the dental implant, finally leading to implant failure. Moreover, the finding of immune cells under TEM analysis and excessive activity of osteoclasts surrounding the bone particles under the light microscope was evidence of the progressing host reaction response and osteolysis process. In one of our pilot studies that examined the removed peri-implantitis-related implant [20], the SEM and TEM images of the dendritic cells (DCs) were recorded on the implant surface and peri-implant inflamed tissue, respectively. In contrast, there was a dominance of macrophages and the absence of DCs in current cases. These observations gave a glimpse of the role of two antigen-presenting cell populations in the initiate and regulate immune responses. Nevertheless, some studies have reported that sinusitis without chronic change could be treated sufficiently using medication, and there is no certain evidence available proving the direct impact of sinusitis on implant survival [11, 21].
An ideal maxillary sinus bone grafting material should induce a high ratio of vital bone as well as prevent re-pneumonization following resorption of the graft material. Besides autogenous bone, which has been considered as the “golden standard” for bone augmentation, allogenic bone is also used widely in sinus-lifting and bone-augmentation procedures. Allogenic bone graft allows for rapid bone formation and remodeling; however, there are reports of unpredictable bone resorption, and the physical strength of the new bone tends to be weak [22, 23]. The bone-formation rate following allogenic bone grafting is low because the allograft has no osteogenesis and weak osteoinductivity, and the process of sterilization and storage influences both osteoconductivity and osteoinductivity. In the early stage postoperation, blood clotting allows the colonization of bone particles, and the anatomical structure of the sinus walls facilitates mechanical stability of the grafting mass. However, in cases when the rupture of the sinus membrane is available, an increase in the physiologic intra-sinus air pressure due to hemorrhagic reaction, nose-blowing, or sneezing can cause displacement of the bone graft material into the sinus cavity through membrane perforation [24].
Currently, there are many types of allograft materials with different bone origins and chemical compositions. The Oragraft® bone material, which was used in cases 1 and 2, is a particulate bone graft option combining 70% mineralized ground cortical bone with 30% demineralized ground cortical bone. Khanijou et al. [25] studied the physicochemical and osteogenic properties of different types of bone graft materials, including allograft, xenograft, alloplastic, autogenous bone, and human tooth options. EDS analysis revealed that all grafting materials contain O, C, Ca, P, Na, and magnesium, albeit varying percentages of such. As an example, Oragraft® contains C and O at proportions of 34.02% and 34.39%, respectively, while the Ca and P levels of this material are 21.28% and 9.79%, respectively; notably, the Ca/P ratio of Oragraft® is the highest among different types of bone graft material at 2.17. Khanijou et al. [25] also reported that the Oragraft® bone material has an extensive Ca dissolution at the early stage, with a decreasing trend, while the dissolution of P was consistent over 14 days. In the current study, in case 1, even though the Ca level at the integrated bone graft material on the implant surface was at a normal level (23.03%), the P level was undetectable. Furthermore, there was no detection of P on the surface of the implant in cases 2 and 3, with a low level of Ca. We suggest that the consistent dissolution of Ca and P into the peri-implant environment, combined with the coverage of organic matter on the implant surface—which prevented the contact and deposition of Ca and P from the body fluid to the implant surface—may impact and interrupt the initial osseointegration process.
In a previous study of chronic sinusitis-related implant failure in the late phase, we observed that contamination of potentially toxic elements, microorganism infection, and long perforation of the implant apex into the sinus might play a central role in dental implant failure associated with maxillary sinusitis [26]. In the current cases, on the SEM images, there was no detection of bacteria or other infectious organisms on the surface of all three implants, which suggested a low possibility of a bacterial infection etiology. The contamination of the implant and bone tissue with aluminum (Al), iron (Fe), and mercury (Hg) potentially had an influence on the integration of bone tissue and the health of peri-implant tissue. The exposure of the facial prosthesis and its implant to the external environment may have caused the contamination [27]. Noticeably, the significantly high level of gold (Au) on the implant surface and the trace amounts of Au and titanium (Ti) in the bone tissue were recorded, which might have resulted from instability and micro-movement of the implant-abutment connection over an extended period of time [28].
The implant surface morphologic analysis revealed heterogeneous surfaces and a low rate of osseointegration. “Distant” osseointegration was observed and might have arisen during the implant removal or, more likely, due to the inability of the implant fixture to osseointegrate along with the failure of the alveolar as well as grafted bone. Notably, the sandblasted and acid-etched surface might be modified due to oxidization or mechanical abrasion during insertion. However, given the concern that the implants were inserted into the posterior maxillary bone, mechanical abrasion might not be the main factor. Further investigation of this phenomenon using a larger sample size may be warranted.
Commercially pure Ti (cpTi) of grade 4, which is popularly used for implant fixture fabrication, consists of greater than 99% Ti and has an O content of 0.4%. Contamination of other elements is controlled to a maximum of 0.3% iron, 0.05% N, 0.15% hydrogen, and 0.1% C [29]. EDS surface analysis of the three implants in this study showed the incorporation of some contaminants in both the upper and apical regions. C, N, Na, Si, and Cl were detected on the surfaces of the failed implants. According to Kasemo and Lausmaa [30], there is usually a significantly large C signal and a smaller N signal present in dental implants. In the oxide layer of the implant, the intensity of the O signal might not be representative of the true composition of the TiO2 layer. The detection of this unrelated element is not related to impurities in cpTi but instead attributed to the C-, N-, Na-, and Cl-containing molecules that progress to adsorption during preparation procedures. The presence of Si is possibly due to the implant surface treatment process [31]. Olefjord and Hansson [32] suggested that inorganic contaminants might block the sites for the O cathodic reaction and therefore result in the dissolution of Ti.
Noticeably, S was only detected in case 1 among the three cases and only in the bone/organic matter region. This raised the question of possible contamination of the graft material in a way that typically causes inflammation and implant failure. Tl, Au, and Zr were uncommon contaminations of the implant surface. Tl amalgam has been used in low-temperature thermometers, and Tl is thought to make its way into dental amalgam due to the recycling of mercury thermometers. Au can be recovered as a dissolved product from other Au intraoral restorations. However, in the implants of cases 2 and 3, Au was detected at a high level in the apical region of the implant. This phenomenon might require further study to reveal the origin of those Au ions. Zr was only detected in case 2 and was hypothesized to have originated from the intraoral breakdown of restoration components. The influence of metallic contaminants on the dissolution rate of Ti in body fluids has not been evaluated to date. It is suggested that foreign ions on the TiO2 surface may catalyze the O reaction and thereby promote the dissolution of Ti [33].
As it is written previously, there are three basic causes of implant failure: the surgeon’s ability, the patient’s unique immunity, and the implant material itself. Of course, the comprehensive ability to integrate these three categories as deciding the whole treatment plan could be considered as the most important factor of implant success. Before discussing the cause of the used implant fixture, it is essential to recall and give feedback on whether there were any mistakes of the operator himself that the operator was not aware of, and whether there was any peculiar characteristic of the patient.