Impact of local and systemic factors on the incidence of late oral implant loss.

For figures, tables and references we refer the reader to the original paper.

When a properly documented implant system with a long-term success rate has been selected, long lasting prosthetic survival can be expected. Lindquist et al. (1996), evaluating symphyseal fixed prostheses supported by implants, reported implants cumulative success rate of 98.9% both after 10 and 15 years. Implant failure can compromise the prosthetic rehabilitation. Implant failures can be subdivided into early and late failures, defined as occurring before or at abutment connection (early) or after occlusal loading is established (late). The etiology of failures may be different in these two time periods.

An early failure of an implant results from ‘an inability to establish an intimate bone-to-implant contact’ (Esposito et al. 1998; Quirynen et al. 2002). This means that bone healing after implant insertion is impaired or even jeopardized. Both systemic and local factors can interfere with these primarily cellular events. The mechanisms that normally lead to wound healing by means of bone apposition do not take place, and rather a fibrous scar tissue is formed in between the implant surface and surrounding bone (Esposito et al. 1999). This can lead to epithelial downgrowth, a so-called saucerization or marsupialisiation of the implant, which often results in mobility or even implant loss. Thus the anchoring function of the endosseous implant cannot be properly performed. Late implant failures on the other hand are influenced by both the microbial environment and the prosthetic rehabilitation. These failures have been associated with both peri-implantitis resulting from plaque-induced gingivitis and peri-implantitis and/or occlusal overloading (van Steenberghe et al. 1990; Quirynen et al. 2002).

Long-term maintenance of a rigid implant to bone interface requires continuous bone remodeling (Roberts et al. 1992). This may be influenced by implant, patient, and surgery-related factors.

Systemic factors play a prominent role for early failures (van Steenberghe et al. 2002, 2003; MombelliGionca 2006).

For late failures, the exposure of the implants and superstructures to the microbial environment and occlusal forces are supplementary risk factors. It renders the detection of impact of systemic and local factors more difficult.

The aim of this large-scale retrospective study is to assess the influence of these systemic and local factors on the occurrence of late implant loss up to 2 years after abutment connection.

In order to achieve a good analysis of these factors the following two questions were set: (1) What is the effect of all the factors on the failure rate of the implants? Then the unit for the analysis is the implant and one only has to take into account the fact that implants within each patient are correlated. Or(2) What is the effect of all these factors on patient's ability to use the implants? Then the unit for the analysis is indeed the patient.

However, then one has to clearly define what failure means.

For example, from a prosthetic point of view, a patient who has received five or six implants (fully edentulous) loses one or even two – they will often not be replaced because the prosthetic treatment–(the one the patient really matters about) – can still be successfully performed. The answer to the first question is the goal of this retrospective study.

Material and methods

Materials

The files of 700 patients collected randomly from the total patient group treated by means of endosseous implants at the Department of Periodontology of the University Hospital of the Catholic University Leuven were evaluated.

It is a general policy of the department to accept treatment for all patients who can benefit from implants for their oral rehabilitation. Thus even if systemic or local factors are detected which can compromise the outcome of this treatment, modality is considered vs. classical prosthetic approaches. All patients were treated by means of Brånemark system® implants (Nobel Biocare, Gothenburg, Sweden). A minimal bone height of 7mm was the requirement for implant placement. Surgery in the department is performed under strict aseptic conditions (van Steenberghe et al. 1997). A thorough sterility policy allows limiting the use of antibiotics to well-defined indications such as endocarditis prophylaxis, a remaining infection at the site of surgery, coughing or sneezing by the patient during surgery. It involves the use of two suction devices, a nose cap, etc.

The end point observation was evaluating the failure rate of the implants 2 years after abutment installation. The study involved all implants that did not encounter loss before or at abutment surgery (early loss) and implants for which it was possible to evaluate its status 2 years after abutment surgery.

The following implants were not considered for the analysis:

  • • Implants which failed before or at abutment surgery.
  • • Implants that although did not fail but in patients who could not be followed for up to 2 years after abutment surgery.

The remaining data of 412 patients (240 females) provided with a total of 1514 implants could thus be analyzed.

The later data set implant loss were analyzed and related to health and behavioral factors, implant lengths and diameters, bone quality and quantity, insertion site, type of edentulism, prescription of antibiotics pre- or immediately after surgery, dehiscence or perforation of the jawbone during surgery, Periotest® (Siemens A G, Bensheim, Germany) values (PTV) at implant insertion (by using a temporary abutment) as well as at abutment connection. The PTV measures the stability of the implant–bone continuum by tapping with an electro-magnetically driven rod on the implant. The outcome is expressed in arbitrary units, reaching from −8 to +50 (Tricio et al. 1995). Implants should lead to values below +5; the more negative, the better the stability.

PTVs were performed only on a fraction of the patient material because of irregular availability of the machinery.

Data collection and analysis

Only screw-shaped Brånemark system® implants (Nobel Biocare), were used either with a machined (n=1316) or a moderately rough very oxidized Ti-Unite™ surface (n=198). The general health and the behavioral history of the patient were carefully recorded on the patient's files. It was obtained after thoroughly questioning the patients preoperatively as a routine procedure. An implant was considered a failure if a peri-implant radiolucency could be detected on the intra-oral radiographs, if an individual's implants showed the slightest sign of mobility corresponding to a PTV of >5, or if the patient showed subjective signs of pain or infection, all these led to implant removal. Thus failed implant in our study is equal to lost implant.

Jawbone quality and the degree of jawbone resorption were evaluated by the periodontologist at implant placement. Tactile evaluation during drilling and assessment of the alveolar crest both radiographically and clinically allowed classification according to LekholmZarb index (1985).

The following health or behavioral factors were particularly questioned and assessed (often also by consulting the files from other medical departments): smoking habits, hypertension, ischemic cardiac problems, coagulation anomalies, gastric problems such as ulcers, osteoporosis, hypo- or hyperthyroidism, hypercholesterolemia, asthma, diabetes types I or II, Crohn's disease, rheumatoid arthritis, chemotherapy, intake of medication (antidepressants, steroids).

Smoking patients were allocated to one of the following three categories (<10 cigarettes/day, 10–20 cigarettes/day or >20 cigarettes/day). Local bone factors, such as radiotherapy of the maxillofacial region involved, were also recorded. Finally, a special note was made for patients with claustrophobia. These patients were treated with reduced coverage of the face, often without a nose cap and as such with a serious breach of asepsia (van Steenberghe et al. 1997).

The type of edentulism was classified according the presence and location of natural teeth in the oral cavity related to implant location: full edentulism, teeth present only in the antagonistic jaw, teeth present in the same jaw as the implants either in the vicinity or not from the implant.

Statistical analysis

Logistic regression models were used to evaluate the effect of explanatory variables on the late loss of the implant. Generalized estimating equation (GEE) method (Liang & Zeger 1986; Zeger & Liang 1986) was used to account for the fact that several implants were available for a single patient (repeated observations). The question of the study was: what is the effect of all the factors on the failure rate of the implants? Thus the unit which was considered for the analysis is the implant, and the fact that implants within each patient are correlated was taken into account in the analysis.

Firstly, a univariate effect of each implant-related, behavioral, and local bone factor on the late loss was evaluated by fitting univariate GEE logistic regression model. Odds ratios and their 95% confidence intervals based on the robust standard errors from the GEE logistic regression model were computed. The Wald test based on robust standard errors was used to assess the significance of each factor. Additionally, we adjusted obtained P-values for multiple testing using the method of Holm (1979). For categorical factors with more than two levels, differences in the loss proportions between these levels were evaluated by multiple comparison provided by the robust Wald's P-values adjusted using the method of Holm (1979).

Secondly, a multivariable was used to evaluate the effect of the health factors when controlled for the behavioral, implant related and local bone factors that were univariately (at 5%) significant. Namely, the following factors were controlled for: location (mandible, anterior/mandible, posterior/maxilla, anterior/maxilla, posterior), diameter. Although univariately significant, jaw (mandible/maxilla), and site (anterior/posterior) was not controlled for since these together determine location. Further, although univariately significant, bone quality, PTV at implant insertion, aPTV at abutment connection were not controlled for because the data were available for only a limited subgroup of patients. Due to the fact that no implant loss has been observed in the group of patients having a given disease, the effect of chemotherapy, diabetes types I, II, rheumatoid arthritis, claustrophobia, steroid medication, could not be assessed statistically.

A statistical analysis was performed using the r 2.4.0 software (r Development Core Team) and the r package gee (version 4.13-10).

Results

A total of 101 implants of different lengths and diameters, out of the 1514 implants installed, appear to have failed between abutment connection and the 2 years follow-up.

Table 1 describes the distribution of numbers of implant placed per patient and provides a summary statistics of the number of implants failed.

Table1.Distribution of number of implants placed per patient, and number of patients who experienced one or more implant failures

When implant characteristics were related to implant late loss, implant diameter and location in the jaw were relevant, while implant length were not (P-value=0.01, <0.001, 0.34, respectively).

Smoking habits could not be related to implant loss (P-value=0.28). The same was applied for the type of edentulism (P-value=0.85). The presence of dehiscence or fenestration of the bone tissue at implant insertion did not affect the late outcome (P-value=0.58, 0.31, respectively). The same holds true for bone volume (P-value=0.34), while bone quality affected significantly late implant loss (P-value=0.03).

A summary of the univariate GEE logistic regression for all the above mentioned factors can be found in Table 2a and b.

Table2a.Univariate GEE logistic regression: implant related, behavioral and local bone factors, the total number of patients whose factors were evaluated, and the distribution of the failed and success implants

Table2b.Univariate GEE logistic regression: implant related, behavioral and local bone factors, the total number of patients whose factors were evaluated, and the distribution of the failed and success implants

Significantly more late loss occurred with higher PTV values either at implant insertion or at abutment connection, which reflects a lower rigidity (P-value/adjusted P-value<0.001) (Fig. 1).

Figure1.

Box plots of Periotest® value (PTV) at implant insertion, and at abutment connection (aPTV) for the successful and failed implants.

When a multiple comparison (among the levels of categorical factors) was done, significantly more loss could be detected with implants of wide platform (5mm) when compared with implants of regular platform, diameter (4mm) or (≤3.75mm) (P-value=0.04, 0.009, respectively) [P-value=0.004, 0.02, odds ratio (95% CI)=2.7 (1.53–4.79), 2.73 (1.37–5.44), respectively]. There was significantly more loss in bone quality grade 4 (soft bone with little cortical bone) when compared to grade 2 [P-value=0.03, odds ratio (95% CI): 3.92 (1.51–10.21)].

The mandibular anterior region experienced significantly less loss than the posterior region [P-value=0.04, odds ratio (95% CI): 3.42 (1.91–9.06)], the maxillary posterior region [P-value=<0.001, odds ratio (95% CI): 76.83 (2.65–17.57)], and the anterior region [P-value=0.02, odds ratio (95% CI): 3.99 (1.58–10.07)]. Within the upper jaw, significantly more implant loss occurred in the posterior regions when compared to the anterior ones [P-value=0.04, odds ratio (95% CI): 1.71 (1.13–2.58)].

The frequency distribution of successful and failed implants within the patient suffering from a known systemic disease is described in Table 3.

Table3.The frequency distribution of successful and failed implants of patients with and without known healthy conditions

This was certified through a multivariate analysis controlled for the other diseases and other factors, which are related to late loss such as implant location and diameter.

Certain systemic factors, such as cardiac and gastric diseases, controlled diabetes type II, coagulation problems, hypertension, hypo- or hyperthyroidism, hypercholesterolemia, asthma, osteoporosis, Crohn's disease, claustrophobia, antidepressant medication did not lead to an increased incidence in the late loss (P-value 0.05). Radiotherapy significantly increased the number of implant loss (P-value=0.003) (Table 4).

Table4.Multivariable GEE logistic regression: implant related, behavioral and local bone factors and health factors

Discussion

Renouard and Nisand (2006) reported in a review paper that there is a trend for machined-surface implants – a trend that does not apply to rougher surfaces such as TiUnite™– for an increased loss rate with short- and wide-diameter implants. Although in the present study the statistical analysis revealed no significant difference in late failure rate between the machined surface and TiUnite™ surface implants, yet there is a trend for more implant loss with machined surface.

Such increased implant loss of wide-diameter implants was mainly associated with a learning curve, poor bone density, implant design and site preparation, and the fact that it is usually used as ‘rescue’ implants.

The present study, confirmed the trend for more loss occurring with wide-diameter implants. Here too, these implants were mostly installed in sites with poor bone quality and quantity. These confounding factors offer a possible explanation.

Low bone density – as assessed clinically or radiologically – has also been pointed as a possible reason for non-integration (Engquist et al. 1988; Friberg et al. 1991; Jaffin & Berman 1991). In our present findings, bone quality type 4 is indeed associated with slightly higher implant loss.

The effect of smoking on the late failure rate is not evidenced in the present study. It is well known to have an impact on early failures rate (Bain 1996, Bain & Moy 1993). This may be explained by the effect of smoking on the wound healing process, in early stage of osseointegration (Alsaadi et al. 2008) while other factors are more predominant for the late failures.

The PTV does not have a direct relation to the aim of the study, because it is not a systemic or a local factor but a method to measure the stability of the implant and therefore only an indirect measure for the bone quality. Higher PTVs at abutment are associated with more late loss. The only possible explanation is the less rigid bone to implant interface, which under loading may lead to a reversal of the osseointegration process: a differentiation to fibrous scar tissue. Lack of intimate bone apposition results in implant marsupialisation (Ivanoff et al. 1996; Szmukler-Moncler et al. 2000)

The higher implant loss in the upper jaw vs. the lower, and in the posterior vs. the anterior region reflect the thin cortical bone combined with less dense trabecular bone often observed in the upper jaw (Jacobs 2003). The poor degree of bone mineralization will reveal itself on the radiographs (Friberg et al. 1995, 1999). Distal regions also have higher chewing forces when compared to the anterior. On an average clenching forces are three times higher in the molar vs. the incisor regions (Helkimo et al. 1977).

The long-term effects of radiotherapy on bone quality are poor (Keller 1997). The dramatic effect of radiotherapy on late failures should lead to a cautious application of osseointegration in such patients (Jisander et al. 1997). But even with a higher failure rate the implant-retained prosthesis is often the only option because of xerostomia. The decreased bone blood supply can lead to osteoradionecrosis (Marx & Johnson 1987; el Askary et al. 1999).