Journal of Dental Implants

: 2022  |  Volume : 12  |  Issue : 2  |  Page : 95--105

Gender-based predilection for the microbial load of Aggregatibacter actinomycetemcomitans present in anterior versus posterior implant sites: A preliminary observational study

Soumee Sengupta1, S Ganesh1, S Meenakshi1, Raghavendra M Rao2, K N. Raghavendra Swamy1,  
1 Department of Prosthodontics and Crown and Bridge, JSS Medical College and Hospital, JSSAHER, Mysuru, Karnataka, India
2 Department of Microbiology, JSS Medical College and Hospital, JSSAHER, Mysuru, Karnataka, India

Correspondence Address:
Dr. S Ganesh
Department of Prosthodontics and Crown and Bridge, JSS Dental College and Hospital, JSSAHER, Mysuru, Karnataka


Purpose of Study: Bacterial biofilm-induced peri-implantitis has been one of the leading causes of implant failure. There are a plethora of local and systemic factors that have been studied at a depth and thereafter have been proven to have a contributory role in the overall disease progression. Epidemiological factors such as site specificity and gender stand to be two confounding factors that have insufficiency in the literature regarding their involvement in the same. Thus, the present article aims to address this gap in the literature and present conclusive evidence about the gender-based comparative evaluation of the microbial load of Aggregatibacter actinomycetemcomitans, one of the potential periodontopathogens for the disease progression, present in anterior versus posterior implant sites. Materials and Methods: Twelve patients (six males and six females) undergoing the implant prosthetic rehabilitation at two intraoral sites, one anterior and one posterior region, were selected as suitable subjects and the healing abutments as the clinical test samples. Culture-independent microbiological analysis was carried out for all the samples for quantification of A. actinomycetemcomitans. Results: The mean viable bacterial DNA count was 503076.49 copies/μL for the male subjects and 474587.85 copies/μL for the female subjects. Hence, there was no significant function correlating gender specificity and the viable bacterial DNA counts. The mean total of viable bacterial DNA counts for the anterior region (site 1) was 407087.17 copies/μL and for the posterior region (site 2) was 570577.17 copies/μL, irrespective of the gender. Thus, a highly significant difference was observed in the mean viable bacterial DNA counts between site 1 and site 2 (F = 20.214; P = 0.001) irrespective of the gender. Conclusion: There seems to be no gender-based predilection for the quantification of viable bacterial DNA counts for A. actinomycetemcomitans. However, a propensity for the presence of higher bacterial load of A. actinomycetemcomitans, one of the causative microorganisms of per-implant diseases, does exist for the implants placed in the posterior region as compared to those placed in the anterior region.

How to cite this article:
Sengupta S, Ganesh S, Meenakshi S, Rao RM, Swamy K N. Gender-based predilection for the microbial load of Aggregatibacter actinomycetemcomitans present in anterior versus posterior implant sites: A preliminary observational study.J Dent Implant 2022;12:95-105

How to cite this URL:
Sengupta S, Ganesh S, Meenakshi S, Rao RM, Swamy K N. Gender-based predilection for the microbial load of Aggregatibacter actinomycetemcomitans present in anterior versus posterior implant sites: A preliminary observational study. J Dent Implant [serial online] 2022 [cited 2023 Jan 29 ];12:95-105
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Full Text


Due to the predictability of a long-term successful outcome, the clinico-scientific discipline of oral implantology has seen a tremendous rise in demand among patients and clinicians alike, over the past decades. However, microbial challenge poses a serious threat over the longevity of the treatment survival and success rate, causing peri-implant diseases.

Peri-implant diseases are inflammatory conditions affecting the soft and hard tissues surrounding dental implants, and can be grouped into two categories, namely peri-implant mucositis and peri-implantitis. According to the American Academy of Periodontology, peri-implant mucositis refers to the inflammation of the associated soft tissues around an endosseous implant, sans the loss of surrounding bone support or any continuous additional marginal bone loss.[1] On the other hand, peri-implantitis has been defined as an inflammatory reaction associated with the loss of supporting bone beyond initial biologic bone remodeling around an implant in function.[2]

There can be various etiological risk factors influencing the disease initiation and progression, both host related and implant related. The former includes a diverse circle of factors that may include systemic factors (uncontrolled diabetes mellitus, autoimmune disorders, patients undergoing radio/chemotherapy for head-and-neck cancers or bisphosphonate therapy, genetic makeup of the patients, etc.) or local factors (bone quantity and/or quality, soft tissue characteristics, bacterial biofilm, patients with a history of periodontitis, poor oral hygiene, overcontoured or overhanging restorations, etc.) or environmental factors (deleterious habit history of tobacco or alcohol consumption).[3] Implant-related factors include material, shape, topography, surface chemistry, mechanical loading, implant-abutment connection, number of implant-abutment connections/disconnections, the presence of excess amount of residual cement, and surgical technique.[4],[5]

Of all the factors that have been studied rigorously, the authors claim that bacterial-induced insult is the most instrumental in causing implant failure. An implant seems to undergo the formation and attachment of a supramucosal implant biofilm within 30 min of its installation intraorally.[6] This biofilm generally comprises a rich commensal micro-population that exists in harmony and helps in maintaining homeostasis within the host. However, under any delicate change of the optimum oral conditions (pH, temperature, humidity, etc.), this microflora may undergo a dysbiotic shift toward a more patho-odontogenic, virulent, fusiform population of more Gram-negative bacteria.[7],[8] There has been enough corroborative evidence to state that out of all the dysbiotic polymicrobial species, A. actinomycetemcomitans, initially present as a commensal in the intracoronal compartment and healthy peri-implant sulcus,[9] is a definitive causal agent for intraoral peri-implant diseases,[10],[11] though not a keystone pathogen, this pathobiont exhibits a latent virulence that initially, may escape the normal immune function of an individual, but can cause an acceleration in the biofilm expansion, which may get detected too late.[12] Furthermore, in rare severe cases, a microbial overload of this species can impact the systemic health of the patient, cross the blood–brain barrier, and cause bacterial endocarditis and brain abscess.[13]

A thorough literature search yields the ambiguity of the results in the effect of epidemiological factors such as age and sex of the patient and site of the implant placement on the prevalence of peri-implant diseases.[5],[14],[15],[16]

Thus, the purpose of the current study was to correlate the epidemiological factors of sex of the patient and the site of implant placement with the local precipitant factor of bacterial accumulation of A. actinomycetemcomitans in healthy individuals, so as to provide a statistical model to predict the outcome of a planned implant prosthetic rehabilitation of an edentulous span. The implications of this study could help the clinicians in a better case selection, diagnosis, treatment planning, and execution of a planned restoration.

 Materials and Methods

The current study was carried out in the Department of Prosthodontics and Crown and Bridge, JSS Dental College and Hospital, in active collaboration with the Department of Microbiology, JSS Hospital, Mysuru. Ethical clearance was obtained from the Institutional Ethical Committee of JSSDCH. Purposive sampling technique was followed to obtain a sample size of 12 patients, 6 males and 6 females undergoing the prosthetic phase of implant rehabilitation at two sites, one in the anterior (in place of any of the two central incisors, two lateral incisors, and two canines) and one in the posterior area (in place of any of the two premolars or molars).

Selection criteria were set up in a stringent manner to adjust for the multiple risk variables of peri-implantitis, and thus, the risk of selection bias was avoided. Patients falling in the age group of ≤49 years of age, reporting to the Outpatient Department, were included. Patients with any known relevant systemic history; pregnant and lactating mothers; those under any antibiotics, analgesics, and nonsteroidal anti-inflammatory drugs; those undergoing periodontal treatment at the time of recruitment; and those presenting with any other suspicious lesion of hard or soft tissue were excluded. To the authors' best knowledge, none of the patients had a deleterious habit history. It was carried out as a single-center study, with all the implants belonging to one particular system.

Patients were recruited as the subjects on the day of their second-stage surgery after ensuring voluntary participation. Implant healing abutments (Dentium Superline, Cypress, California, USA) were chosen to be collected as clinical samples from the two test sites (anterior and posterior). Since this particular component has a subgingival portion which would be in direct contact with the implant fixture, the subgingival peri-implant sulcus, and the gingival collar, it was expected to have the subgingival biofilm adhered to it with the rich micro-population of the target bacteria, A. actinomycetemcomitans. Hence, two healing abutments were placed at the implant sites, as per the treatment plan derived by the clinician. After 14 days from hereon, both the healing abutments were collected and placed into two sterile microcentrifuge tubes (Tarsons, Kolkata, India) for transport to the Department of Microbiology for carrying out quantitative real-time viability polymerase chain reaction (PCR) [Figure 1].{Figure 1}

Each of the two microcentrifuge tubes was pipetted (Tarsons Accupipet, Tarsons, Kolkata, India) with 200 μL of 0.9% normal saline solution (Vea Impex, Mumbai, India) followed by mechanical vortexing (Spinix, Tarsons, Kolkata, India), to ensure uniform dispersion of the bacterial biofilm adhered to the surface of the healing abutment into the entire sample solution [Figure 2]. This was followed by division of each 200 μL into two further parts, each of 100 μL. At this stage, each patient gave four microcentrifuge tubes, each containing 100 μL of the sample solution [Figure 3]. The following treatments were carried out for pre-PCR processing of the sample solutions:{Figure 2}{Figure 3}

Test site 1: Healing abutment collected from anterior region (initial total volume of 200 μL):

100 μL fraction, for quantification of total bacterial count present in that sample, ADX100 μL fraction, for quantification of viable bacterial count present in that sample, AD√

Test site 2: Healing abutment collected from posterior region (initial total volume of 200 μL):100 μL fraction, for quantification of total bacterial count present in that sample, PDX100 μL fraction, for quantification of viable bacterial count present in that sample, PD√

Now, a photosensitive viability dye, PMAxx dye concentrate, 20 mM, in H2O (Biotium, Fremont, California, United States of America), was prepared as a stock solution of 5 mM in H2O [Figure 4].{Figure 4}

For each patient, the two microcentrifuge tubes intended for the quantification of the viable bacterial count were then mixed with 1 μL of 25 μM of the stock dye solution followed by covering them completely with an opaque aluminum foil. Both the microcentrifuge tubes were then vigorously shaken for intermixing the contents, before incubation in the dark for 10 min. Then, they were exposed to blue LED light of λ=466 nm (spectral property of dye, λabs = 464 nm) for 15 min.

These steps were expected to make the dye cross-link with and cause selective alteration of the dead target bacterial DNA permanently. Thus it would aid in recognizing viable bacterial DNA via quantitative real-time viability PCR (qRT-PCR) for all the test sample solutions collected from all test sites in all patients.

HumqPCR real-time Aggregatibacter actinomycetemcomitans testing kit (Lote RTq-H710-100D111220, BioIngentech Corporation, Concepcion, Chile) was obtained for the extraction of genomic bacterial DNA and carrying out qRT-viability PCR (qRT-vPCR) in the Rotor-Gene Q PCR instrument [Figure 5].{Figure 5}

The entirety of the four aliquots previously prepared was then used individually for the bacterial DNA extraction prior to carrying out qRT-vPCR. 5' nuclease probe-based real-time PCR assay (hydrolysis probe-based detection method of quantification real-time PCR) was employed. Primers and probes, both contained within the kit, had the following sequence: forward primer sequence: 5'-GAA CCT TAC CTA CTC TTG ACA TCC GAA-3'; reverse primer sequence: 5'-TGC AGC ACC TGT CTC AAA GC-3'; probe sequence: 5'-AGA ACT CAG AGA TGG GTT TGT GCC TTA GGG-3'; amplicon size: 80 base pairs (bp). During PCR amplification, hybridization of the forward and reverse primers to the target genomic material and cleavage of all the probes caused the separation of the reporting dyes and quenchers, leading to the increase in fluorescence that, once crossed the threshold cycle, gave the CT value and the final quantification of the viable and total bacterial DNA count (Copies/μL) present in all the clinical sample solutions. Each clinical sample solution was analyzed in duplicate.


Verification of the experimental setup validity of the polymerase chain reaction test kit

The individual reaction mixtures (Mastermix) of the positive, negative, and internal controls were prepared and subjected to real-time thermocycling parameters, as per the manufacturer's instructions that yielded the following quantification findings and the resultant quantification curves (analysis software Rotor-Gene Q).

The cyclic runs of the five serial dilutions of the positive control, and the negative control, gave the total number of bacterial DNA copies/μL traceable in each control template [Table 1] and [Table 2].{Table 1}{Table 2}

Consequently, the following standard curves were generated for the calibration of the exact concentration of the bacterial DNA copies of the template present in these positive standard tubes against their CT values (number of cycles required for the template DNA of each standard tube to cross the threshold line, get detected, and emit fluorescence) [Graph 1] and [Graph 2].[INLINE:1][INLINE:2]

[Graph 1] shows that bacterial DNA concentration (x-axis) had an inverse function with the CT value. Thus, a higher concentration of bacterial DNA in a given standard tube corresponded to a lower number of amplification cycles required for the identification and quantification of the bacterial DNA.

The sigmoid-shaped [Graph 2] shows that each standard tube had had enough template bacterial DNA to cross the threshold line, give the corresponding CT value, and emit fluorescence. It was noted that as the level of dilution of the standard tubes increased from A to E, the concentration of the bacterial DNA in the standard tubes decreased from A to E. This in turn showed that the number of amplification cycles required for the identification, i.e. the CT values increased from A to E.

Standard B was used as the reference template for the quantification of the bacterial DNA present in all the clinical sample solutions. The raw data in terms of bacterial DNA copies/μL derived from qRT-vPCR were then taken up for statistical analysis with the help of SPSS software (Version 22) for Windows.

Mean bacterial DNA copies/μL of male and female subjects for viable and total DNA values and the results of independent sample t-test

The mean bacterial DNA copies/μL for viable DNA found in male and female subjects were found to be 503076.49 and 474587.85, respectively. Independent samples t-test revealed a nonsignificant mean difference between the genders (t = 0.263; P = 0.795).

In the case of total DNA count, again independent samples t-test revealed a nonsignificant mean difference between male and female subjects. The observed “t” value of. 058 was found to be nonsignificant (P = 0.954). In other words, male and female subjects had statistically similar values both in viable and total DNA bacterial copies/μL [Graph 3] and [Table 3].{Table 3}[INLINE:3]

Mean viable bacterial counts for anterior (S1) and posterior (S2) sites with descriptive statistics

A significant difference of 163490 (site 2 mean: 570577.17; site 1 mean: 407087.17) was observed in the mean viable bacterial DNA copies/μL between site 1 and site 2 (F = 20.214; P = 0.001) irrespective of the gender. From the mean table, it was evident that the mean viable bacterial DNA copies/μL at site 2 was significantly higher than site 1.

However, when the difference between sites for mean viable bacterial DNA copies/μL was analyzed against gender, a nonsignificant interaction was observed with F value of 0.309 and P value of 0.590. The mean difference or change between male and female subjects for viable bacterial DNA copies/μL from site 2 to site 1 was 143270.94 and 183709.06, respectively. Hence, even if a slightly higher change was seen in the bacterial DNA count from anterior to posterior sites for females, as compared to males, the overall statistical value was non-significant [Graph 4] and [Table 4].{Table 4}[INLINE:4]


Under a dysbiotic environment, the shift of microorganisms to more Gram-negative ones has been stated to be the major etiological factor in cases of advanced peri-implantitis.[17],[18],[19],[20],[21],[22],[23],[24],[25] Among these Gram-negative periodontopathogens, some are initiators of a diseased state to the tissues, while others are more responsible for maintaining a constant progression of the virulence factors. Aggregatibacter actinomycetemcomitans is one such purple complex bacterium, which with its innate virulence factors can help expedite the biofilm expansion causing an inevitable disruption of the health of the peri-implant tissues. These are namely the factors promoting intraoral colonization and persistence, factors interfering with host defenses, and factors causing destruction of host tissues. Factors promoting adhesion and colonization are adhesins, invasins, bacteriocins, and serotype-specific antibiotic susceptibility. Adhesins may include a variety of structural projections (fimbriae, vesicles, and extracellular amorphous material) that may either consist of glycoproteins, proteoglycans, or lipopolysaccharides (LPS). These not only serve to facilitate the bacteria to attach to the host substratum via specific receptors in saliva, tooth, and surrounding gingival tissues but also withstand shear forces, obtain nutrients, and aid in metabolism, transport, buoyancy control, and enzyme storage. Invasins cause the formation of bacterial cell surface craters leading to endocytosis into the host cell cytoplasm. Bacteriocins are heterogeneous proteinaceous particles that add to the survival-colonization advantage by lessening the competition with other organisms for both space and nutrients.[26] Antibiotic resistance is conferred to this bacterium owing to its seven different serotypes which have a diverse geographical distribution and a marked heterogeneity in the levels of antibiotic consumption across different countries. Thus, it is difficult to form an uniform hypothesis regarding the susceptibility rates of the different serotypes to different antibiotics.[27] Factors interfering with host defenses include leukotoxin (LtxA), LPS, chemotactic inhibitors, and cytolethal distending toxin (CDT).[26] LtxA, highly specific to hematopoietic cells, activates inflammophilic changes in neutrophils, monocytes, and macrophages which bring about a massive release of pro-inflammatory cytokines (interleukin [IL]-1β and IL-18), lysosomal enzymes, and matrix metalloproteinases, ultimately inducing apoptosis in lymphocytes.[28] LPS induces the antigenic variability in the different serotypes and causes the production of IL-1, IL-6, IL-8, TNF-α, etc., activating the complement and coagulation cascade.[29] Chemotactic inhibitor helps in disruption of neutrophil chemotaxis while CDT, a genotoxin, mediates DNase activity, inhibits phagocytic activity, affects the proliferation of gingival fibroblasts, and causes bone resorption. Finally, the factors bringing about the destruction of host tissue directly are collagenases, heat shock proteins, bone-resorbing agents, and cytotoxins, which can bring about osteolysis and impair proliferation of epithelial cells, osteoblasts, and fibroblasts.[26] There are studies to confirm that the exposure of any host peri-implant tissue to A. actinomycetemcomitans showed a low release of cytokine and chemotactic factors, with simultaneous areas of DNA damage and subsequent repair hinting at an overall stress response. Both these findings showcased A. actinomycetemcomitans to mediating a low degree immune response and having survival-colonization advantage against the host immune system.[12] Leonhardt et al. have detected pronounced microbial loads of A. actinomycetemcomitans in and around failing implants as compared to healthy implants.[30] Owing to these findings, it can be said with certainty that A. actinomycetemcomitans does exhibit a concealed progression of symptoms, promoting adhesion, invasion, and progression of peri-implantitis.

It can be stated that healthy peri-implant tissue is characterized by the absence of BOP, and marginal bone loss <2 mm. Features of peri-implant mucositis include a positive BOP, PPD >5 mm, and marginal bone loss ≤2 mm. Peri-implantitis is identified as a combination the features of peri-implant mucositis and a marginal bone loss >2 mm.[15]

Hence, literature states that the process of disease progression from peri-implant mucositis to peri-implantitis is extremely similar to that of the progression from gingivitis to periodontitis. However, there exists no mandate that peri-implant mucositis will necessarily progress to peri-implantitis, and can be reversed when effectively treated. Thus, the prime objective of management of peri-implant diseases lies in the interception of signs and symptoms at an early stage and the elimination of the etiological factor.

It is imperative to understand the etiology and the risk profile for peri-implant diseases for an accurate diagnosis and treatment planning. Carl E. Misch states that the most common etiologies include poor oral hygiene and biofilm mediation inflammation, unfavorable osseous density, untreated endodontic or periodontal lesions, systemic comorbidities like untreated diabetes mellitus, deleterious habits like alcohol consumption, smoking, etc., lack of cleansability, poorly placed implants, overcontoured prostheses, unfavorable biomechanical stresses, and presence of excess residual cement. Further, there may be a delayed hypersensitivity reaction after exposure to Ti alloy.

Since the onset of the disease, there may be a variety of symptoms encountered at the affected site that include clinical attachment loss of both hard and soft peri-implant tissues, presence of peri-implant pockets, marginal bone loss, bleeding on probing, exudate discharge, mucosal swelling, and local erythema.[3] Now, the clinical signs such as redness, swelling, mobility of the prosthesis, and pus discharge may be noticed a bit too late by the patient as most of the times, there is no pain involved. Thus, emphasis has been put to understand the various systemic, local, environmental, and genetic factors at play at the initial stages itself to integrate these considerations in the treatment planning.

When it comes to prevalence, there may exist multiple variables involved, thus leading to heterogeneous inconclusive data. Pertaining to gender, a blend of varied results has been observed for predilection of peri-implantitis. Horikawa et al., and Koldsland et al., have suggested there might be a higher propensity for males to be affected with peri-implantitis more than females. However, Attard and Zarb demonstrated that women showed more peri-implant bone loss than men.[31],[32],[33] Marcantonio et al., after having evaluated 30 females with a total of 118 implants placed and 18 males with 79 implants placed, over a period of about 8-10 years, concluded that 4 males and 10 females had developed symptoms of peri-implantitis. However, this result was not statistically significant.[34] This was in congruence with the results published by Negri et al., who inference that a statistically insignificant relation existed between marginal bone loss and the implant platform.[35] There are studies like that of Anderson et al., who had conducted a retrospective search of the patients' clinical notes to identify the documented cases of peri-implantitis. Results showed that out of 28 cases of peri-implantitis, about 60.7% of males and 39.3% of females had had symptoms of the diseased state. However, the authors may have taken this as an isolated finding as they had postulated that racial distribution, a previous history of periodontitis, prevalent respiratory or cardiac conditions and the jawbone involved and had had more of a correlation with peri-implantitis.[36] Other studies and reviews have reported that gender had had no effect on peri-implantitis.[37],[38] With regards to the gender-based predilection for the specific bacterial colonization by A. actinomycetemcomitans, the authors have stated that a higher prevalence exists for the female gender, manifested generally between puberty and 25-30 years of age.[39],[40] With regards to the site, A. actinomycetemcomitans is known to have an affinity for the permanent molar and incisor area, as in the case of localized aggressive periodontitis causing an angular pattern of interproximal bone loss.[41] Though one would expect that the rich blood supply, thin spongy cortical bones, and bone marrow with struts would make maxilla, less prone to colonization. But in cases of A. actinomycetemcomitans-mediated peri-implantitis, there are other factors involved which govern the bone-implant contact, such as the degree of osseointegration, bone mineral density, width of platform, diameter and length of implant, occlusal load borne by the implant, tissue architecture, etc. Taking into consideration, all these factors, generally it is found that mandibular implants tended to have smaller marginal bone loss than that seen in maxilla. The denser mandibular bone can withstand loading more efficiently in a less tilted fashion to the implant axis while undergoing slower remodeling around the implant than the maxilla.[35] This result has been corroborated by other studies, which have shown that peri-implantitis and implant failure are seen more commonly in maxilla as compared to mandible.[36],[42],[43],[44]

Despite these findings, there does exist, an obscurity on the effect of sex and site specificity on the prevalence of peri-implant diseases, which has been addressed by the current article. When evaluated for gender predilection, there existed no significant results for viable or total bacterial DNA counts, as is showcased in [Table 3] and [Graph 3]. However, when analyzed for site specificity, it was evident that irrespective of gender, the mean viable and total bacterial DNA counts were overall higher at the posterior region, as compared to the anterior region.

When evaluating the difference between sites for means viable and total bacterial DNA counts against gender, it was seen that both male and female subjects had yielded statistically similar values for viable bacterial DNA counts for either of the two sites individually. These can be well explained by [Table 4] and [Graph 4].

With regard to site specificity, it could be concluded that implants placed in the posterior region have the potential to house more bacteria than those placed anterior region. These results could be attributed to the higher mineral bone densities found in the anterior region as compared to posterior region, be it maxilla or mandible. Additionally, the former generally has higher plaque and gingival bleeding scores due to deficient or callous cleansing and brushing techniques followed. A reduced visual perception of the posterior region could equate to higher chances of the inflammatory effects of microbial challenge on the implant and peri-implant tissues.

However, there seems to exist, no gender predilection for the viable bacterial DNA counts with regards to either anterior or posterior sites and has been quantified to be between ranges of 1.2 × 105-8.4 × 105 copies/μL for the anterior and 2.7 × 105-9.7 × 105 copies/μL for the posterior region.

There are direct implications of these results on the type of case selection and the maintenance phase, which need to be curated according to the clinical scenario.

Now, the recent times advocate for the basis of success to be long-term implant maintenance rather than the osseointegration and surgical factors. Since peri-implant mucositis may exhibit apical progression after only 3 months of plaque build-up around implants, therefore, a 3-month maintenance regimen is recommended within the 1st year of implant placement to evaluate tissue health and patient home care. If after the 1st year, implants are healthy, then maintenance interval is extended to 6 months.[3],[45]

Maintenance may be done via in-office decontamination or reinforcement of patient home care instructions. In office decontamination may be done via surgical or non surgical therapies. Surgical therapies include regenerative or resective therapies. Nonsurgical therapies include surface mechanical or chemical debridement via, air powder abrasives, lasers, etc. Patient home care should be followed stringently with the use of specific dentifrices, manual and electromechanical devices such as power brushes, interproximal brushes, dental floss, oral irrigator, etc.[3]

Furthermore, the clinician could follow prognostic models such as the Implant Quality scale by Suzuki-Misch-Hsaio scale[46] or the scale for diagnosis and treatment planning by Misch,[3] which would allow the clinician to trace the clinical condition of an implant from optimum health to disease, to diagnose and place a particular implant in a certain group based on the established criteria and thus devise and proceed with an appropriate treatment plan.

Scope of further research lies in the inclusion of larger sample sizes and testing against other causative peri-implant micro biota. Furthermore, correlations should be drawn between definitive clinical/ radiographic parameters such as BOP, PPD, radiographic bone loss; and the bacterial counts. Ultimately, a deeper analysis should be carried out to understand the prevalence of microbial colonization and peri-implant diseases on the individual surfaces of implant prosthesis (mesial, mesiobuccal, mesiolingual, distal, distolingual, and distobuccal).


Bacterial biofilm mediates a challenge on the overall success and prognosis of any implant prosthetic rehabilitation by causing peri-implant diseases. It is necessary to understand all the underlying risk factors that could have a role in the overall disease progression for early interception, management, and reversal of the symptoms noted. The subgingival biofilm isolated from posterior peri-implant sulcus harbors higher concentration of A. actinomycetemcomitans as compared to the one isolated from anterior site. Owing to the pathogenicity and virulence of this bacterium, the clinician should render more scrutiny for an implant placement planned for the posterior sites, whether maxilla or mandible to avoid complications or failure. Furthermore, a thorough emphasis should be put on other predisposing factors for any complication, like a history of periodontitis, poor oral hygiene, uncontrolled systemic comorbidities such as diabetes mellitus and the consumption of tobacco (chewables, smoking, etc.). Ultimately, postrehabilitative implant care is the key to the longevity of any implant prosthesis, and hence a thorough maintenance profile should be maintained for each patient.


We sincerely acknowledge and express our heartfelt gratitude toward the Indian Society of Oral Implantologists (ISOI) for having provided us with the financial aid for the current study in the form of the annual ISOI Research Grant, March 2021 (Ref No. MAHBH21180318300/ISOI). The amount has been duly used for the smooth conduct of our study.

Financial support and sponsorship

Indian Society of Oral Implantologists (Ref No. MAHBH21180318300/ISOI).

Conflicts of interest

There are no conflicts of interest.


1Heitz-Mayfield LJ, Salvi GE. Peri-implant mucositis. J Clin Periodontol 2018;45 Suppl 20:S237-45.
2Poli PP, Cicciu M, Beretta M, Maiorana C. Peri-implant mucositis and peri-implantitis: A current understanding of their diagnosis, clinical implications, and a report of treatment using a combined therapy approach. J Oral Implantol 2017;43:45-50.
3Misch CE. Contemporary Implant Dentistry. 4th ed. St. Louis, Missouri: Elsevier. [Last accessed on 2020 Jun]
4Vootla NR, Reddy KV. Osseointegration – Key factors affecting its success – An overview. IOSR J Dent Med Sci 2017;16:62-8.
5Monje A, Insua A, Wang HL. Understanding peri-implantitis as a plaque-associated and site-specific entity: On the local predisposing factors. J Clin Med 2019;8:279.
6Fürst MM, Salvi GE, Lang NP, Persson GR. Bacterial colonization immediately after installation on oral titanium implants. Clin Oral Implants Res 2007;18:501-8.
7Lasserre JF, Brecx MC, Toma S. Oral microbes, biofilms and their role in periodontal and peri-implant diseases. Materials (Basel) 2018;11:1802.
8Kröger A, Hülsmann C, Fickl S, Spinell T, Hüttig F, Kaufmann F, et al. The severity of human peri-implantitis lesions correlates with the level of submucosal microbial dysbiosis. J Clin Periodontol 2018;45:1498-509.
9Cosyn J, Van Aelst L, Collaert B, Persson GR, De Bruyn H. The peri-implant sulcus compared with internal implant and suprastructure components: A microbiological analysis. Clin Implant Dent Relat Res 2011;13:286-95.
10Cortelli SC, Cortelli JR, Romeiro RL, Costa FO, Aquino DR, Orzechowski PR, et al. Frequency of periodontal pathogens in equivalent peri-implant and periodontal clinical statuses. Arch Oral Biol 2013;58:67-74.
11Raja M, Ummer F, Dhivakar CP. Aggregatibacter actinomycetemcomitans – A tooth killer? J Clin Diagn Res 2014;8:ZE13-6.
12Ingendoh-Tsakmakidis A, Mikolai C, Winkel A, Szafrański SP, Falk CS, Rossi A, et al. Commensal and pathogenic biofilms differently modulate peri-implant oral mucosa in an organotypic model. Cell Microbiol 2019;21:e13078.
13Rahamat-Langendoen JC, van Vonderen MG, Engström LJ, Manson WL, van Winkelhoff AJ, Mooi-Kokenberg EA. Brain abscess associated with Aggregatibacter actinomycetemcomitans: Case report and review of literature. J Clin Periodontol 2011;38:702-6.
14Dreyer H, Grischke J, Tiede C, Eberhard J, Schweitzer A, Toikkanen SE, et al. Epidemiology and risk factors of peri-implantitis: A systematic review. J Periodontal Res 2018;53:657-81.
15Ahn DH, Kim HJ, Joo JY, Lee JY. Prevalence and risk factors of peri-implant mucositis and peri-implantitis after at least 7 years of loading. J Periodontal Implant Sci 2019;49:397-405.
16Rokaya D, Srimaneepong V, Wisitrasameewon W, Humagain M, Thunyakitpisal P. Peri-implantitis update: Risk indicators, diagnosis, and treatment. Eur J Dent 2020;14:672-82.
17Peri-implant mucositis and peri-implantitis: A current understanding of their diagnoses and clinical implications. J Periodontol 2013;84:436-43.
18Mombelli A, Lang NP. The diagnosis and treatment of peri-implantitis. Periodontol 2000 1998;17:63-76.
19Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman SR, Lang NP. Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res 1994;5:254-9.
20Salvi GE, Aglietta M, Eick S, Sculean A, Lang NP, Ramseier CA. Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clin Oral Implants Res 2012;23:182-90.
21Leonhardt A, Adolfsson B, Lekholm U, Wikström M, Dahlén G. A longitudinal microbiological study on osseointegrated titanium implants in partially edentulous patients. Clin Oral Implants Res 1993;4:113-20.
22Quirynen M, Vogels R, Peeters W, van Steenberghe D, Naert I, Haffajee A. Dynamics of initial subgingival colonization of 'pristine' peri-implant pockets. Clin Oral Implants Res 2006;17:25-37.
23Augthun M, Conrads G. Microbial findings of deep peri-implant bone defects. Int J Oral Maxillofac Implants 1997;12:106-12.
24Salcetti JM, Moriarty JD, Cooper LF, Smith FW, Collins JG, Socransky SS, et al. The clinical, microbial, and host response characteristics of the failing implant. Int J Oral Maxillofac Implants 1997;12:32-42.
25Leonhardt A, Berglundh T, Ericsson I, Dahlén G. Putative periodontal pathogens on titanium implants and teeth in experimental gingivitis and periodontitis in beagle dogs. Clin Oral Implants Res 1992;3:112-9.
26Malik R, Changela R, Krishan P, Gugnani S, Bali D. Virulence factors of Aggregatibacter actinomycetemcomitans – A status update. J Int Clin Dent Res Organ 2015;7:137.
27Brígido JA, da Silveira VR, Rego RO, Nogueira NA. Serotypes of Aggregatibacter actinomycetemcomitans in relation to periodontal status and geographic origin of individuals – A review of the literature. Med Oral Patol Oral Cir Bucal 2014;19:e184-91.
28Belibasakis GN, Maula T, Bao K, Lindholm M, Bostanci N, Oscarsson J, et al. Virulence and pathogenicity properties of Aggregatibacter actinomycetemcomitans. Pathogens 2019;8:222.
29Benso B. Virulence factors associated with Aggregatibacter actinomycetemcomitans and their role in promoting periodontal diseases. Virulence 2017;8:111-4.
30Leonhardt A, Renvert S, Dahlén G. Microbial findings at failing implants. Clin Oral Implants Res 1999;10:339-45.
31Horikawa T, Odatsu T, Itoh T, Soejima Y, Morinaga H, Abe N, et al. Retrospective cohort study of rough-surface titanium implants with at least 25 years' function. Int J Implant Dent 2017;3:42.
32Koldsland OC, Scheie AA, Aass AM. The association between selected risk indicators and severity of peri-implantitis using mixed model analyses. J Clin Periodontol 2011;38:285-92.
33Attard NJ, Zarb GA. Long-term treatment outcomes in edentulous patients with implant-fixed prostheses: The Toronto study. Int J Prosthodont 2004;17:417-24.
34Marcantonio C, Nícoli LG, Malzoni CM, Susin C, Marcantonio Junior E, Zandim-Barcelos DL. Prevalence and risk indicators of peri-implantitis after 8 to 10 years of function. Rev Odontol UNESP 2021;50:e20210015.
35Negri M, Galli C, Smerieri A, Macaluso GM, Manfredi E, Ghiacci G, et al. The effect of age, gender, and insertion site on marginal bone loss around endosseous implants: Results from a 3-year trial with premium implant system. Biomed Res Int 2014;2014:369051.
36Anderson N, Lords A, Laux R, Woodall W, Abubakr NH. Retrospective analysis of the risk factors of peri-implantitis. J Contemp Dent Pract 2020;21:1350-3.
37Geckili O, Mumcu E, Bilhan H. The effect of maximum bite force, implant number, and attachment type on marginal bone loss around implants supporting mandibular overdentures: A retrospective study. Clin Implant Dent Relat Res 2012;14 Suppl 1:e91-7.
38Renvert S, Aghazadeh A, Hallström H, Persson GR. Factors related to peri-implantitis – A retrospective study. Clin Oral Implants Res 2014;25:522-9.
39Ferreira DC, Aguiar SM, Filho PN, de Queiroz AM, De Rossi Andiara. Localized aggressive periodontitis – Clinical, radiographic, microbiological and immunological findings. RSBO 2014;11:393-400.
40Cortelli JR, Roman-Torres CV, Aquino DR, Franco GC, Costa FO, Cortelli SC. Occurrence of Aggregatibacter actinomycetemcomitans in Brazilians with chronic periodontitis. Braz Oral Res 2010;24:217-23.
41Joshipura V, Yadalam U, Brahmavar B. Aggressive periodontitis: A review. J Int Clin Dent Res Organ 2015;7:11.
42Vervaeke S, Collaert B, Cosyn J, Deschepper E, De Bruyn H. A multifactorial analysis to identify predictors of implant failure and peri-implant bone loss. Clin Implant Dent Relat Res 2015;17 Suppl 1:e298-307.
43Mengel R, Heim T, Thöne-Mühling M. Mucositis, peri-implantitis, and survival and success rates of oxide-coated implants in patients treated for periodontitis 3- to 6-year results of a case-series study. Int J Implant Dent 2017;3:48.
44Mameno T, Wada M, Onodera Y, Fujita D, Sato H, Ikebe K. Longitudinal study on risk indicators for peri-implantitis using survival-time analysis. J Prosthodont Res 2019;63:216-20.
45Zitzmann NU, Berglundh T, Marinello CP, Lindhe J. Experimental peri-implant mucositis in man. J Clin Periodontol 2001;28:517-23.
46Suzuki JB, Misch CE. Peri implantitis. In: Resnik R, Misch CE, editors. Avoiding Implant Complications. Ch. 18. USA, St. Louis: Elsevier-Mosby; 2017.