Keywords
antimicrobial agents - malodorous - two-stage dental implant systems
Introduction
Loss of dentition is still prevalent among societies, especially in the elderly and
middle-age people.[1] It is estimated that complete edentulism is seen in 7 to 69% of adults internationally.[2] For this mean, dental implants have been used to improve function and esthetic in
edentulous patients.[3] Dental implants are introduced as a treatment with a good prognosis. Most studies
indicate a success rate of more than 90% for dental implants.[1]
[4]
[5] They are offered in two general types of one-stage (tissue level) and two-stage
(bone level) implants.[6]
Although dental implants have a good predictability, both technical and biological
complications have been reported.[7]
[8]
[9] Biological complications (i.e., peri-implantitis and bone loss) may occur due to
reaction against microorganisms present in oral cavity.[9]
[10] Beside from implant failure, oral pathogenic bacteria—mostly anaerobic—are also
responsible for oral malodor, which is defined as an unpleasant odor coming out of
the mouth, nose, sinuses, or pharynx.[11]
Presence of pathogenic bacteria in unavoidable microleakages of implant-abutment interface
in two-stage dental implant systems may cause further malodor production and peri-implantitis.[12]
[13]
[14] According to studies and clinical observations, transmucosal depth of two-stage
implants is associated with anaerobic bacteria population, thereby producing malodor.[15] Several studies have demonstrated effectiveness of chlorhexidine in reducing oral
bacteria.[16]
[17] It has also been indicated that topical administration of tetracycline results in
significant reduction of oral bacteria.[18]
Malodorous followed by opening of the healing abutment is usually noticed by both
patients and the dentist. Patients may also ask their dentist about the possibility
of a persistent malodor. However, there are few studies focusing on malodor prevention
in this specific situation. Therefore, the aim of this study is to assess and compare
the effectiveness of two harmless topical antimicrobial agents in prevention of the
bad odor releasing after opening the healing abutments.
Materials and Methods
Study Design
The current study was a controlled clinical trial with “stratified randomization”
and “double blinding,” which was performed on patients who were referred to the implant
department of Isfahan University of Medical Sciences, Isfahan, Iran, for surgical
exposure of their two-stage implants from July 2021 to September 2021. We performed
our study using three equal groups, each containing 17 eligible participants.
Sample Size Calculation
The sample size was calculated based on a similar study[17] and the following formula, which indicated that with a sample of 17 participants
per group, the power of 0.8 would be obtained at 0.05 level of significance:
Inclusion Criteria
-
☑ Patients who were referred for surgical exposure of their two-stage implants, and
were treated with a SNUCONE implant system were included in this randomized clinical
trial.
-
☑ All patients included had healthy periodontal conditions (less than 10% bleeding
on probing) and a transmucosal depth—transmucosal depth (gingival height [GH]) evaluation
was performed using a color-coded Michigan Williams periodontal probe and was measured
at four points and the maximum depth was recorded—of 1 to 3 mm since these factors
can affect malodorous in this study.
Exclusion Criteria
-
⌧ The individuals who were either smokers or in any specific medical condition were
excluded from the study.
-
⌧ The individuals who showed current halitosis (halitosis was assessed using an organoleptic
method—the organoleptic measurement of breath was taken at a distance of 10 cm from
oral cavity by a single investigator who was trained and calibrated for this task,
and patients were then scored as follows: – = negative halitosis, + = positive halitosis)
during our primary assessment were also excluded.
-
⌧ The individuals who had used antibiotics during the past 4 weeks of their visit
were also excluded since it could cause bias in our results.
Using the stated criteria, 51 eligible patients were collected as samples, which were
then divided into three parallel and equal study groups (group 1, group 2, and group
3). To eliminate potential bias, we engaged in a stratified randomization procedure[19] to divide the samples into three equal subgroups.
Randomization
At first, samples were stratified (layered) into six blocks; two levels of gender
(male and female) and three levels of age (less than 40, between 40 and 60, and more
than 60 years old).
For assigning the participants within each block to one of the three study groups,
six potential sequences are possible. Therefore, a sequence was given to each block
randomly (i.e., the first participant of the first block enters group 1, the second
participant of the first block enters group 2, the third participant of the first
block enters group 3, etc.) ([Fig. 1]).
Fig. 1 Stratified randomization procedure.
Eventually, all layers were equally and randomly assigned into three parallel groups
of 17 people. Female–male ratio was equal between the three groups and according to
one-way analysis of variance, no statistically significant difference was found between
age averages of the three groups (p-value = 0.987).
Intervention
In the exposure surgery session, fixtures were exposed surgically applying a flap.
Then for the first group chlorhexidine 2% gel (Morvabon brand; made in Morvabon Company
in Iran) and for the second group tetracycline 3% ointment (made in Hakim Company
in Iran) was added to the internal surface of the fixtures with a sterile microbrush
[Fig. 3]). No additional intervention was performed on the third group. Eventually, the healing
abutments were screwed into the implants hand-tight using the screwdriver.
Fig. 2 Frequency distribution of malodor within the study groups.
Fig. 3 Applying chlorhexidine gel on a microbrush.
After the surgical procedure, patients were asked to brush their teeth (using toothbrush
and toothpaste) and floss once a day until their next visit. They were then given
postsurgery instructions and followed until their next visit.
Measurements
Measurements were conducted 4 to 5 weeks following second-stage surgery at the first
removal of the healing abutment. Patients were asked to have their breakfast meal
properly early in the morning and avoid eating or drinking for 2 hours prior to measurements.
Measurements included subjective odor score which was performed by a single independent
observer whose functioning of olfaction was tested using The Sniffin' Sticks test.[20] Malodor was scored by sniffing the abutment immediately after uncovering it. Odor
emitting from the healing abutment was scored as followed: 0 = odorless; 1 = odor.
-
▪ The organoleptic test (subjective assessment of odor) is not only a simple, low-cost
method, but is considered to be the gold standard for odor assessment.[21]
[22]
[23]
-
▪ The number of fixtures implanted for each patient varied from 1 to 4 fixtures. But
when measuring odor, even if only one of the patient fixtures was given a score of
1, we considered point 1 for that person considering that even one smelling fixture
can result in dissatisfaction.
Blinding: Our method was performed in three steps, each by an individual investigator:
-
The first investigator (A.F.) assessed the participants in terms of inclusion and
exclusion criteria and finalized the number of samples. He performed the whole randomization
process in the examination session and assigned the participants into the study groups.
A code was then given to each patient. Then, he transferred the list of the participants
of all three study groups to the surgeon. However, the patients were not informed
which group they were participated in.
-
The surgeon (M.R.) attended the exposure surgery session and performed the intervention
on the participants based on the group each were participated in. Again, patients
were not informed about the exact intervention during the exposure surgery.
-
The last investigator (S.N.) attended only the measuring session (3–4 weeks after
the exposure surgery when opening the healing abutments) and assessed the outcomes.
Conclusively, neither patients nor the outcome assessor was informed about the medication
used for each particular patient (double-blinded).
Statistical Analysis
Data was analyzed by IBM SPSS Statistics 24. For comparison of qualitative data between
groups, the chi-square test was used. A value of p < 0.05 was indicated as statistically significant.
Results
The aim of the current study was to evaluate the effectiveness of two antimicrobial
agents (chlorhexidine and tetracycline) in preventing malodor associated with two-stage
implants. The study sample included 51 patients who were referred to the implant department
for surgical exposure of their bone-level implants. Participants were divided into
three equal groups. Each group included 12 females (70.6%) and 5 men (29.4%). Baseline
and clinical characteristics of the patients are reported in [Table 1].
Table 1
Mean and standard deviation (SD) of age and gingival height within the study groups
|
Group category
|
Age (y)
Mean ± SD
|
Gingival height (GH) (mm)
Mean ± SD
|
|
Group 1 (chlorhexidine)
|
55.0 ± 10.18
|
2.03 ± 0.495
|
|
Group 2 (tetracycline)
|
54.5 ± 8.78
|
1.99 ± 0.508
|
|
Group 3 (control)
|
54.7 ± 9.50
|
1.93 ± 0.572
|
|
Total
|
54.7 ± 9.31
|
1.98 ± 0.517
|
According to one-way analysis of variance, the difference between mean age and mean
GH of the three groups was not statistically significant (p-value = 0.987 and 0.857).
According to the chi-square test malodor frequency between the three groups was significantly
different (p-value = 0.023). According to Fisher's exact test there was no significant difference
between malodor in chlorhexidine and tetracycline group (p-value = 1). Moreover, chi-square test showed that there was a significant difference
between malodor scale in the chlorhexidine group and control group (p-value = 0.013) and there was also a significant difference between malodor scale
in the tetracycline group and control group (p-value = 0.037) [Table 2].
Table 2
Frequency distribution of malodor within the study groups
|
Scale of malodor
|
Study groups
|
Total
|
|
Chlorhexidine
|
Tetracycline
|
Control
|
|
No Malodor
0
|
Count
|
14
|
13
|
7
|
34
|
|
Percentage
|
82.4%
|
76.5%
|
41.2%
|
66.7%
|
|
Malodor
1
|
Count
|
3
|
4
|
10
|
17
|
|
Percentage
|
17.6%
|
23.5%
|
58.8%
|
33.3%
|
|
Total
|
Count
|
17
|
17
|
17
|
51
|
|
Percentage
|
100.0%
|
100.0%
|
100.0%
|
100.0%
|
Discussion
In this study, we aimed to evaluate the effectiveness of chlorhexidine and tetracycline
on preventing malodor associated with dental implants in comparison with the control
group. Our findings showed a statistically significant difference between malodor
in patients whom antimicrobial agents were used in their implants and the control
group. However, malodor in the chlorhexidine group and tetracycline group did not
show any significant difference.
Two-stage implants contain two components: the intraosseous (fixture) and the extraosseous
component (abutment or healing screw). Most mechanical and biological issues related
to dental implants originate from the implant-abutment interface.[24]
[25] For instance, bacterial contamination occurs in the microgap between the two components
both when the healing screw and when the permanent abutment is applied. When a healing
screw is removed, malodorous is a result of the presence of the bacteria and their
volatile sulfide compounds.[15]
[26]
[27] In 1997, Jansen et al reported that there are unavoidable microleakages at the implant-abutment
connection. They suggested that bacterial colonization that occurs in the microleakages,
close to the epithelial attachment, will result in further peri-implant bone resorption
and implant failure.[24] Furthermore, Resende et al concluded that saliva infiltration and bacterial growth
could occur in microgaps and cause inflammation and malodor.[28] Based on a recent pilot in
vitro study, obtaining a complete seal against bacterial colonization at the implant-abutment
interface is unlikely.[29] Scarano et al evaluated the efficacy of an antibacterial coating in the internal
chamber of the implant using real-time volatile organic compound measurement technique.
Based on their results, the antibacterial coating has been effective in reducing bacterial
activity.[30] In the present study, chlorhexidine and tetracycline were effective in prevention
of the malodorous when applied topically in the fixtures.
According to a study performed by Scarano et al, larger microgaps will result in more
bacterial growth.[31] Based on previous studies, microgap size is affected by materials and fabrication
methods, and significantly different microgap sizes have been reported among different
implant systems.[32]
[33] In the current study, a single implant system was assessed considering that various
systems are likely to have different sizes of microgaps. Therefore, our results may
not be extensible to other implant systems.
Researchers have shown that the anaerobic bacteria located in the back of the tongue
play an important role in the production of malodor, since this region is not cleaned
properly.[34]
[35]
[36] It has also been reported that the bacteria responsible for malodor are mostly Fusobacterium nucleatum and Porphyromonas gingivalis.[37]
[38]
[39] There are two general ways for assessing malodor: organoleptic and instrumental
technique. In organoleptic method, malodor is evaluated by the examiner's sense of
smell. For instrumental measurement, various devices are used. Despite the fact that
organoleptic measurement is known to be gold standard for this mean, it is associated
with undeniable bias due to its subjectivity, and therefore this was a limitation
of the present study.[21]
[22]
[23]
For one thing, our findings provided a better understanding of a common issue with
two-stage dental implants, which is particularly annoying for patients as well as
dentists. We found that chlorhexidine and tetracycline were both effective in reduction
of malodor when applying locally in the fixtures. Whether or not our findings can
generally be used as a probable predictive treatment in this condition needs further
investigation. It is also suggested for future studies to focus on identifying bacteria
responsible for this issue, and use specific antibiotics based on their susceptibility.
In conclusion, based upon the data from this study, it appears that local antimicrobial
agents including chlorhexidine and tetracycline result in less malodor production
within the implant-abutment interface.
