Biological complications in patients with implant-supported dental restorations

SUMMARY Introduction Biological complications are the most common type of complications around dental implants. They appear in two forms, peri-mucositis and peri-implantitis. The aim of our research was to analyze the above-mentioned complications regarding the time elapsed from implantation and implant loading, as well as regarding the type of dental restoration. Material and methods 18 patients with self-reported complications were examined at the Department of Periodontology and Oral medicine, School of Dental medicine, University of Belgrade. Each patient filled an anamnestic questionnaire. Clinical examination, including photographic and radiographic documentation have been performed. Results Clinical examination included 18 patients and 97 implants in total (70% female patients and 30% male patients). The average time elapsed from implants placement was 7.5 years and the average from final dental restoration was 7 years. Periodontitis was diagnosed in 85% of the patients. Complications were more common among the patients with cement-retained restorations. Conclusions Due to the limitation of our study, we can assume that periodontal disease and cement-retained restorations are the risk factors for genesis and development of the complications around dental implants. The results of our study are in consent with data found in the literature, but in order to confirm these results it is necessary to perform analysis on a larger sample and with longer follow-up.


INTRODUCTION
Biological complications are the most common complications around dental implants. They present as peri-implant mucositis and peri-implantitis. New classification of periodontal and peri-implant diseases and conditions was the result of the meeting of The American Academy of Periodontology and The European Federation of Periodontology in 2017. Finally, new and uniform definitions of peri-implant health, peri-implant mucositis and peri-implantitis were adopted [1].
• The main criterion for distinction between healthy and inflammatory mucosa is bleeding on probing (BoP). • The main criterion for distinction between peri-mucositis and peri-implantitis is deterioration in the bone supporting the dental implant.
In the period of healing, after implant placement, soft tissues and hard tissues are forming. The formation of a new bone on the implant surface is the process called osseointegration. The development of masticatory mucosa and connective tissue around the new implant, and formation of peri-implant mucosa is the process known as mucointegration [2].
Peri-implant health is characterized by the absence of the clinical signs of the inflammation in the peri-implant complex. It is marked as absence of swelling, redness and bleeding on probation. Hence, there is no precisely defined range of probing depths that is compatible with peri-implant health, because peri-implant probing depth depends on thickness of the peri-implant tissues, type and position of the implant, as well as the type of dental replacement. In addition, peri-implant health can exist around implants with reduced bone support. It can be established after successful treatment of peri-implantitis.
The characteristics of the peri-implant tissues in health are: • The absence of clinical signs of inflammation • The absence of bleeding or suppuration on mild probation • The absence of increased probing depth • The absence of bone loss We can diagnose peri-mucositis with first discrete signs of soft tissue inflammation, but without peri-implant bone loss. The common cause is accumulated dental plaque around the neck of a dental implant. Dental plaque in peri-implant region is generally the most common cause of peri-mucositis.
The main clinical sign of peri-mucositis is bleeding on mild probation, but we can also notice redness and swelling. Sometimes, there can be increased probing depth due to swelling. It is important to point out that the main inflammatory process is located exclusively in epithelial tissue, while the junction between connective tissue and epithelium is not affected.
There is evidence that biofilm is the main etiological factor of peri-mucositis. It is proven that adequate plaque control therapy reduce inflammation. That means that in peri-mucositis changes are most probably reversible.
• Clinical signs of peri-mucositis: • Bleeding or suppuration on mild provocation • Absence of bone loss Inadequate peri-mucositis therapy leads to the spread of inflammation from soft to hard tissues. There is apical migration of pathologically changed masticatory epithelium and bone resorption. Defect in alveolar bone is developing, known as peri-implant pocket that can be diagnosed with probing or radiography. Afterword we can put diagnosis of peri-implantitis. The peri-implantitis is characterized by inflammation of peri-implant soft tissues and progressive bone loss. All clinical signs of infections are presented (redness, swelling) as well as bleeding and suppuration on probing.
The main etiological factor is the same as in peri-mucositis, bacterial infection and the influence of dental plaque microorganisms. The connection between peri-implantitis and accumulated dental plaque is confirmed by many studies that showed in patients with inadequate oral hygiene and rare control checkups lay higher risk for the development of the inflammation of soft tissue and bone around the implant. The frequency of this disease is about 20% in regard to the patients, and about 10% in regard to the implants [3].
Clinical signs of peri-implantitis: • Bleeding and/or suppuration on mild provocation • Increased probing depth on each control • Probing depth ≥ 6mm • Bone loss (bone level ≥ 3mm apically from the most coronal bone level) There is clear evidence that patients with positive medical history of the periodontal disease have increased risk for the development of peri-implantitis. Risk factors that are important are some systemic disorders like diabetes, osteoporosis, bad habits (inadequate oral hygiene and smoking), and iatrogenic factors (inadequately planned oral and prosthodontic procedures that lead to many mistakes that can result with occlusal overload, that latter accelerate marginal bone loss and lead to contact loss between bone and implant neck) [4].
It is important to pay attention to risk factors during preparation, planning, patient motivation, implantation and dental restoration, since consequences may be very delicate. Also it is very important to have frequent and regular oral hygiene checkups of patients with implants and also treatment evaluation [5].
The bone destruction has faster pattern around dental implant than around natural tooth, hence peri-implantitis progression can be very aggressive. It is of a great importance to mark probing depth values measured around newly placed implant, as well as to make control radiograms, since they will represent referent values for discovering pathological changes in early stadium [4].

MATERIAL AND METHODS
In the period of October 2019 to March 2020 at the Department of Periodontology and Oral medicine at the Faculty of Dental medicine at the University of Belgrade, 18 patients with dental implant difficulties were examined.
In each patient, anamnestic questionnaire was filled, clinical examination was performed, and clinical photos and control radiograms were taken, in order to set up adequate diagnosis and treatment.
Anamnestic data: Clinical examination included the following parameters: • Probing depth (PD), the measured distance from the free end of the gingival margin to the bottom of the peri-implant space. • Attached gingiva level (AGL), the measured distance from the top of the implant to the bottom of peri-implant space • Bleeding on probing (BoP), bleeding 30s after probing, with score 1 if the bleeding is present and score 0 if there is no bleeding at all • Silness-Loe plaque index, defined by scores from 0 to 3 based on recording dental plaque around dental implant • Modified gingival index (GI), score 0 -no signs of inflammation, 1-mild inflammation, minimal color change, minimal swelling, absence of BoP, 2-mild inflammation, redness, swelling, BoP, 3-modern inflammation, modern redness, severe swelling, ulceration, spontaneous bleeding • Gingival recession (GR) on the buccal side -the measured connection implant-abutment distance • Width of the keratinized gingiva (WKG), the measured distance from the free gingival margin to the mucogingival junction The measuring was performed with periodontal probe in 4 points around each implant.

RESULTS
Our research included 18 patients, 13 females and 5 males. Clinical examination was performed around 97 implants and data were collected.
One third of patients (33%) were cigarettes consumers, defined as heavy smokers (10 cigarettes or more per day). 85% of all patients affirm having history of periodontal disease, while 15% clinically have not presented any problem with periodontal health (Figure 1).
Findings from anamnestic questionnaires revealed that more than half of the patients had some systemic disease: 56% of the patients stated systemic disease (40% hypertension, 30% asthma, 10% rheumatic disease, 10% migraine, 10% other disease). While discussing their habits associated with mechanical plaque control, all patients confirmed brushing at least 2 per day, while only 50% of them were using additional tools for interdental hygiene. 20% of the patients used Waterpik device. None of the patients have experienced any changes of the general health condition after implant placement.
While summarizing data about surgical and prosthodontics rehabilitation of the patients, we found out that average time elapsed from implants placement was 7.5 years, while average time elapsed from completion of dental restoration was 7 years. Out of 18 examined patients 15 had cement retained implant restoration, 2 screw retained and only one patient had attachment retained restoration ( Figure 2). Data acquired by clinical examination around implants are summed in Table 1.
The diagnoses were based on anamnesis, clinical examination and additional diagnostic procedures. Data are presented in Figure 3.
According to diagnosis, specific treatment plan was prepared: ◆ In patients with peri-mucositis: -In 88% causal therapy was indicated -In 12% beside causal therapy, additional therapy was necessary ◆ In patients with peri-implantitis: -In 40% explantation and another implant placement -In 30% surgical therapy -In 20% causal therapy with antibiotics -In 10% causal therapy without antibiotics

DISCUSSION
Peri-implant disease develops gradually. It starts with peri-mucositis, when inflammation appears in peri-implant soft tissues, but without changes on supporting alveolar bone. It is assumed that with progression of untreated peri-mucositis, the inflammation spreads from mucosa to connective tissue and bone, leading to peri-implantitis [4].
The main etiological factor is bacterial infection i.e. bad oral hygiene that causes plaque accumulation around the implant. Peri-implant diseases were more common among patients without adequate oral hygiene, or usage   of indicated hygiene tools for elimination of dental plaque around implants. It is necessary to support interdental hygiene in the implant retained dental restorations with interdental toothbrushes like 'Superfloss' etc. Inadequate oral hygiene maintenance is in correlation with infrequent professional plaque control (at least 2 per year). It is noticed that patients with implant retained dental restorations that don't come to regular checkups, are more prone to develop any kind of complications [5].
Many studies showed correlation of peri-implantitis with history or presence of periodontal disease. The frequency of peri-implantitis (PD ≥ 5mm, with BP, and bone loss >2mm annual) was higher in patients with anamnestic data of positive periodontal disease history. One study showed that the therapy of peri-implantitis required longer time in patients with positive periodontal disease history than in healthy patients. Also, complications of peri-mucositis into peri-implantitis were more common in patients with present periodontal disease than in those without positive periodontal disease history [6]. One of the important periodontal measures that were in relation with peri-implant complications was the width of keratinized gingiva, i.e. existence of functional attached gingiva.
Iatrogenic factors, as inadequate dental restoration, can also influence the development of peri-implantitis. Inadequately planned dental restorations (usually full arch bridge or cantilever bridge) with unstable position or inadequate number of placed implants cannot enable good stabilization, and usually lead to occlusal overload and inadequate pressure transmission from implants to supporting bone. That causes loss of connection between implant and marginal bone and development of peri-implantitis. Poorly manufactured restoration (enlarged, inadequately planned) can make difficult to maintain oral hygiene and indirectly influence development of peri-implant disease. The choice of retention of the restoration is also very important since it is known that biological complications are more often around restoration retained with cements. The reason for that is probably accidentally extruded cement in subgingival region. Considering that our research was conducted on a limited sample, the presence of complications was more common in patients with cement-retained restorations and with extended restorations.
Many studies were focused on research of incidence and prevalence of the peri-implant disease. Hence, they showed different results. The reason for that is the lack of consensus about definition of peri-implant disorder, which significantly complicates the comparison of different studies. With publication of a new classification, this deficiency was solved [1,3].

CONCLUSION
Within this study, on a limited sample, we analyzed patients with implant retained dental restoration completed mostly 7 years ago. In that period we can expect the development of complications. The existence of periodontal diseases was significant risk factor for the development of peri-implant complications. This statement is in consent with data found in literature. Besides, low levels of WAG potential can influence development and progression of complications. Also, many restorations were retained with cement so it was reasonable to expect complication if cement is accidentally extruded apically.
In prevention of peri-implant complication, it is important to have adequate treatment plan, previous treatment of periodontal diseases, adequate restoration, and maintain the results with frequent control checkups. In order to confirm results from our research, it is necessary to have larger sample.