Received: 27 April 2022 | Revised: 22 August 2022 | Accepted: 1 December 2022

DOI: 10.1111/clr.14026

ORIGINAL ARTICLE

Photobiomodulation in dental implant stability and

post-­surgical healing and inflammation. A randomised
double-­blind study

Gisela C. V. Camolesi1,2 | José M. Somoza-­Martín1,2 | Maria D. Reboiras-­López1,2 |

Fabio Camacho-­Alonso3 | Andrés Blanco-­Carrión1,2 | Mario Pérez-­Sayáns1,2

1
Oral Medicine, Oral Surgery and
Implantology Unit (MedOralRes), Abstract
Faculty of Medicine and Dentistry,
Background: The aim of this randomized clinical trial was to evaluate the effect of
University of Santiago de Compostela,
Santiago de Compostela, Galicia, Spain diode laser photobiomodulation (PBM) on post-­surgical healing, inflammation and im-
2
Health Research Institute of plant stability.
Santiago (IDIS) (ORALRES),
Santiago de Compostela, Spain
Methods: Forty dental implants were inserted into 13 patients. The implants were
3
Department of Oral Surgery, University randomly divided into two groups. The test group (PBM+) underwent two sessions of
of Murcia, Murcia, Spain PBM (combined diode laser of 630 and 808 nm), the first of which after surgery, and
Correspondence the second, 7 days after the surgical procedure. The control group (PBM−) received
Mario Pérez-­Sayáns, Oral Medicine, simulated laser treatment. The implant stability quotient (ISQ) was determined im-
Oral Surgery and Implantology Unit
(MedOralRes), Faculty of Medicine and mediately after the surgical procedure, and 7 days, 4 and 8 weeks later. Post-­surgical
Dentistry, University of Santiago de inflammation was assessed following the criteria described by Bloemen and Cols.
Compostela, Entrerríos s/n, Santiago de
Compostela C.P. 15782, Spain. Healing was calculated using the healing index (HI).
Email: [email protected] Results: No differences were found in terms of the mean values of implant stability
Funding information between the test and control groups over time. Only two of the implants (18.2%) from
Nueva Galimplant; University of Santiago the PBM− group were classified with the maximum healing index (HI = 5), whereas in
de Compostela, Grant/Award Number:
USC-­2019-­CE178 the PBM+ group, nine implants (45%) were classified with the aforementioned index
(P < 0.0001). Using the logistic regression, it was determined that the non-­application
of the laser in the PBM− group caused an OR of 4.333 times of presenting inflamma-
tion (IC95% 1.150–­16.323; P = 0.030).
Conclusions: The application of 808 nm infra-­red laser for bone tissue, and 630 nm for
mucosal tissue in two sessions is considered to be an effective way of reducing inflam-
mation and improving early healing. More studies are needed to confirm these results.

KEYWORDS
mucosal healing, mucosal inflammation, osseointegrated dental implants, photobiomodulation

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction
in any medium, provided the original work is properly cited and is not used for commercial purposes.
© 2022 The Authors. Clinical Oral Implants Research published by John Wiley & Sons Ltd.

Clin Oral Impl Res. 2023;34:137–147.  wileyonlinelibrary.com/journal/clr | 137

138 | CAMOLESI et al.

1 | I NTRO D U C TI O N
One-­Sentence Summary
Osseointegrated dental implants are used for replacing lost teeth and
This article is a double blind randomized clinical study that
they offer a high success rate (Howe et al., 2019). Bone quantity and
compares the effect of photobiomodulation on bone and
quality are predictive factors in achieving proper primary stability and
tissue healing after implant placement surgery.
in defining whether rehabilitation should be carried out with early
or immediate loading (Elias et al., 2012; Monje et al., 2019; Shokri &
Daraeighadikolaei, 2013). The clinical success of a dental implant over
time is determined by bone quantity, bone quality, and, in particular, and osteogenesis (Bozkaya et al., 2021; Chen et al., 2017; Dompe
adequate osseointegration (Fornaini et al., 2015; Mills et al., 2018). et al., 2020; Tang & Arany, 2013). Moreover, laser reduces in-
The primary stability of dental implants is defined by the bio- flammation and pain, accelerates wound healing, (Agha-­Hosseini
mechanical stability that is obtained when inserting the implant. et al., 2012) and stimulates nerve regeneration (Farivar et al., 2014).
Secondary stability occurs later on, and it depends on osseointegra- Although, other clinical studies have not been able to demonstrate
tion, that is to say the bone formation process in the bone-­implant differences in the levels of stability of dental implants (Bozkaya
interface (Monje et al., 2019; Shokri & Daraeighadikolaei, 2013). et al., 2021; Mandić et al., 2015) or orthodontic mini-­implants
Low-­level laser therapy (LLLT) or photobiomodulation (PBM) has (Marañón-­Vásquez et al., 2019) between the laser group and the
been proposed as a method that could be used to enhance the bone control group, it is important to highlight the great differences be-
cicatrisation process by reducing the healing time for osseointegra- tween the few existing controlled clinical studies. For example, in
tion in preclinical studies (Karakaya & Demirbaş, 2020). However, the study by Lobato et al. (2020), the implants were placed in fresh
other randomized clinical trials have not confirmed these results sockets, which creates a situation of healing and primary stability
(Torkzaban et al., 2018). very different from that of implants placed in healed sites, as in the
PBM consists of low energy density laser and/or LED light ther- study by Kinalski et al. (2021).
apy, so it does not generate heat. To induce photochemical effects and In relation to the healing of hard tissues, some clinical studies
stimulate cell replication (Bayat & Jalalifirouzkouhi, 2017; Karoussis have shown that PBM can reduce the healing time after grafting the
et al., 2017; Santinoni et al., 2021), there is a broad spectrum in extraction socket. Histological evidence suggests that new bone for-
terms of wavelength, ranging from red to infrared (600-­1100 nm) (Qu mation in the sockets appeared within 60 days after PBM treatment
et al., 2022), nevertheless there is no specific guideline to achieve the compared to a minimum of 120 days in the control group (Monea
best results in terms of osseointegration healing (Kazem Shakouri et al., 2015). Moreover, in a computed tomography and histomorpho-
et al., 2010; Riboldi et al., 2009). The most recent published studies metric analysis of human alveolar bone repair developed by Romão
addressing PBM for osseointegration applied a protocol quite similar et al. (2015), the relative bone volume was significantly higher in the
to the one used in our study (Kinalski et al., 2021; Lobato et al., 2020), laser group (P < 0.0001) suggesting that PBM is able to accelerate al-
however the present study presents as a novelty the use of both fre- veolar bone repair after molar extraction, leading to a more thin and
quencies (dual laser, red and infrared wavelength) with the aim of im- close trabeculae. In molecular terms, the study of Palled et al. (2021)
proving the effects at the bone and soft tissue level. showed a significant rise in osteoprotegerin levels of the test group
Several clinical methods have mentioned the use of invasive at 3 months contrary to significant decline in the control group, sug-
techniques to measure the stability of dental implants, such as re- gesting that the healing of peri-­implant hard and soft tissues may
moval torque or histomorphometric analysis (Matys et al., 2017). be enhanced with the use of PBM during the postoperative period.
However, the Periotest and resonance frequency analysis (RFA) are However, although some studies have been developed in relation to
used more often (Marquezan et al., 2012). RFA analysis is carried out the effect of PBM at the microbiological level (Bozkaya et al., 2021),
with specific devices with a transducer or “smart peg” being inserted limited studies have been developed regarding the clinical healing
into the implant or abutment to measure and quantify stability. The and inflammation around implants after PBM.
implant stability quotient (ISQ) is presented using a numerical scale The aim of this clinical trial was to evaluate the effect of 808 nm
from 0 to 100, and it is translated from an intensity frequency of diode laser PBM on implant stability using RFA measurements, and
3500–­8500 Hz (Torkzaban et al., 2018). Higher ISQ values result in a the effect of 660 nm diode laser PBM on inflammation and post-­
higher mean stability (Marquezan et al., 2012). surgical healing.
Studies evaluating the effect of PBM on the stability of dental
implants have reported that the development of secondary stabil-
ity does not take as long because fibrocartilage callus development 2 | M ATE R I A L A N D M E TH O D
increases during the initial stage of bone healing (Kazem Shakouri
et al., 2010). Therefore, the bone-­implant contact (BIC) factor in- 2.1 | Trial design, participants, and setting
creased after the laser irradiation on the peri-­implant site (Lopes
et al., 2005; Matys et al., 2018). Using laser after a surgical proce- The study was a randomised, double-­blinded clinical trial comprised
dure that involves hard and soft tissues enhances healing and has a of a control group and a test group. Participants were exclusively
biostimulating effect over osteoblastic and fibroblastic proliferation, recruited from the University of Santiago de Compostela's Faculty
CAMOLESI et al. | 139

of Dentistry, within the Medicine, Surgery and Oral Implantology 2.2 | Intervention
Department. The trial was conducted between February 2020 and
July 2021, according to the Declaration of Helsinki, as reviewed in The patients were distributed into two groups: a test group that re-
2002. The study was approved by the Local Ethics and Research ceived an active application of PBM (PBM+); and a control group
Committee (Ref. 2019/169) and registered in Clini​calTr​ials.gov, with that received an inactive/sham application of PBM, or laser in off
the identifier: NCT03796494. mode (PBM−).
All the patients who met the inclusion criteria were fully informed
of the characteristics of the study and were invited to participate.
Each patient underwent a complete clinical and oral assessment, as 2.3 | Study products
well as a radiological study based on cone-­beam computed tomog-
raphy (CBCT) (i-­C AT-­FLX). The tests wed the recommended criteria Forty implants with internal hex connection and a diameter of
established in the Spanish CONSORT Statement (Cuschieri, 2019), 4 × 10 mm were used. Implants were placed in healed mature bone
as shown in Figure 1 and followed the SPIRIT statement. (more than 6 months after the extractions), according to the manu-
The patients included in this study all met the following in- facturer's guidelines (Model IPX, Nueva Galimplant). The model used
clusion criteria: (1) there was no presence of any systemic dis- was made of Ti IV and it had a macroscopic design that enhances pri-
eases which might be considered a contraindication, or if these mary stability in any circumstances. In all cases, aesthetical straight
were present they were controlled; (2) the informed consent abutments were placed with their respective gingival protectors. A
form required for participation in the study has been signed; (3) diode laser (Laser Duo, MMO-­São Carlos) was used with the follow-
they smoke <5 cigarettes per day; (4) they have sufficient bone ing parameters: (1) wavelength of 630–­8 08 nm, (2) output power of
quantity to insert 4 × 10 mm implants and ensure that no bone or 100 mW, (3) continuous mode and (4) dose of 0.1 J/s and (5) hand-
soft tissue grafts are needed in molar and premolar areas; and (5) piece with an output of 3 mm2.
they have a minimum primary stability value of 50 ISQ. The ex-
clusion criteria were: (1) they had undergone dental rehabilitation
in aesthetic areas 13–­23 and 33–­4 3; (2) they have implants with 2.4 | Surgical procedures
mechanical torques inferior to 20 N; (3) they smoke more than 5
cigarettes per day; (4) they are pregnant and/or lactating; (5) they The insertion of implants strictly followed the manufacturer's in-
have cancer or a potentially malignant injury in the area where structions regarding different bone types. Implants were placed
PBM is to be applied. mechanically and always 1 mm below the bone crest. Following the

F I G U R E 1 The consort flow diagram of

subject Progress through the phases of a
randomized trial
140 | CAMOLESI et al.

surgical intervention, all of the patients received detailed instruc- registered immediately following the implant surgery and after
tions about oral hygiene; antibiotics (a 750 mg/8 h dose of amoxicil- 7 days, 4 and 8 weeks.
lin for 7 days); and painkillers (a 600 mg/8 h dose of ibuprofen for A standardised fixed length device was inserted (Smartpeg™
4 days). No provisional prosthesis was placed during the 8-­week ob- Integration Diagnostics) and it was screwed into each implant by
servation period. hand. The transducer probing (Osstell™ Mentor Probe) was carried
out by directing the tip of the handpiece to the small magnet located
on the upper part of the Smartpeg™ at a distance of 2–­3 mm, until
2.5 | Laser irradiation the instrument produced a beep and showed the implant stability
quotient (ISQ). These measurements were performed in buccal, lin-
After surgery, half of the implants were randomly assigned to re- gual, mesial and distal implant surfaces in order to obtaining a global
ceive a treatment with a low intensity active laser. The test group, average for the four surfaces.
PBM+, received intraoral irradiation for 100 s through a handpiece
that entered into contact with the mucosa and which was posi-
tioned to allow light to enter perpendicularly to the longitudinal 2.6.2 | Assessment of the healing
axe of the dental implant at 5 mm from the bone crest. Three process of the mucosa
points were irradiated: the buccal side (4J) and the palatal or lin-
gual side (4J) using the infrared light mode (808 nm), to stimulate The degree of post-­surgery inflammation and early healing was
bone tissue regeneration; and the occlusal side (2J) using the red-­ assessed by two independent operators (GCVC and MPS). Post-­
light mode (630 nm), to stimulate mucosal tissue regeneration and surgical inflammation was assessed subjectively and dichotomously
anti-­inflammatory effect. The laser treatment was performed im- (yes/no), through visual examination, following the criteria described
mediately after surgery and it was repeated 7 days later. On each above by Bloemen and Cols (Bloemen et al., 2012). Healing was cal-
session, safety measures were taken with both the patients and culated using the healing index (HI) by Hamzani & Chaushu (2018)
odontologists wearing dark protective glasses. The parameters and Landry (1988). Table 1 shows the final score HI, that ranges from
used for the irradiation were based on previous studies (Chen 0 to 5:0 for poor healing and 5 for excellent healing. The degree of
et al., 2019; Kinalski et al., 2021; Lobato et al., 2020). The total concordance was verified by both researchers, who performed inde-
irradiation per session was 10 J during 100 s, the total energy den- pendent evaluations on the total sample, using Cohen's Kappa index
sity per session was 33.3 J/cm2 , and the total energy density per (Mandrekar, 2011). The degree of agreement for the inflammation
implant was 66.6 J/cm2 . level was 0.91 and >0.90 at all HI levels.
The control group, PBM−, received a sham laser treatment, that
is, only the irradiation of the patient was simulated.
2.7 | Sample size calculation

2.6 | Measurement of primary and The following statistical criteria were established in order to calcu-
secondary objectives late the sample size: (1) a size of the expected increase or reduction
effect on the HI of at least 1.5 at 1 week after surgery, (2) an alpha
2.6.1 | Assessment of implants stability error of 0.05, and (3) a statistical power of 90%. These criteria were
taken into account and the variance contrast for independent sam-
Resonance frequency analysis (RFA) was performed using the ples was applied. It was determined that a sample of 18 implants
Osstell™ Mentor device (Integration Diagnostics), and it was con- would be required for each group, that is to say a total of 36 implants.
ducted by a trained and calibrated operator (GCVC) who was not The final sample size was 42, considering an estimated loss of 15%.
aware of which side would be irradiated. Measurements were The sample size was calculated using the G Power 3.1.5 programme.

TA B L E 1 Landry et al.'s healing index,

Clinical outcome parameters Score 0 Score 1
the final score ranges from 0 to 5, where
Bleeding, spontaneously or on Yes No 0 indicates poor healing and 5 indicates
palpation excellent healing
Granulation tissue Yes No
Tissue colour Redder than opposite side Like the opposite side
tissue tissue
Incision margins Incomplete flap closure/fibrin Complete flap closure/
clot/partial necrosis fine fibrin line
Suppuration Yes No
CAMOLESI et al. | 141

TA B L E 2 Full description of the sample variants

2.8 | Randomisation
PBM− n PBM+ n
Simple randomization was performed for both study groups (PBM+/ Variable (%) (%) P-­value

PBM−). Briefly, a random number generator (N = 40) was used for Sex
the two study groups, using a SPSS 28.0 macro. Men 5 (25) 5 (25) 1.000
Woman 15 (75) 15 (75)
Localisation
2.9 | Blinding Maxillary 6 (30) 6 (30) 1.000
Mandible 14 (70) 14 (70)
All of the assessments of the results of this study were double
Abutment type
blinded because neither the patients (due to the use of a placebo)
Straight 12 (60) 7 (35) 0.113
nor the evaluators (who were not involved in the LLLT process) knew
Slim 8 (40) 13 (65)
which treatment had been assigned to each patient.
Periodontal phenotype
Fine 2 (10) 1 (5) 0.548

2.10 | Statistical analysis Thick 18 (90) 19 (95)

Bone type
The collected data was analysed using the SPSS software pro- I 3 (15) 1(5) 0.292
gramme, version 24.0 (SPSS Inc.). The IQS data for primary and II-­III-­IV 17 (85) 19 (95)
secondary stability was presented using central tendency measure- Visual examination
ments (mean) and variation (SD and CI of 95%). The variance was Without inflammation 6 (60) 13 (65) 0.027
analysed in order to examine changes to the ISQ during the observa-
With inflammation 14 (40) 7 (35)
tion period. The statistical significance of the differences amongst
HI
the observed parameters for IQS between the groups at each ob-
1 6 (30) 0 (0) <0.001
servation point was analysed using the T test for unpaired groups.
2 10 (50) 1 (5)
Contingency tables were created and the Chi Square and Kruskal
3 2 (10) 5 (25)
Wallis tests were applied to study the differences between the
groups in terms of post-­surgery healing and inflammation. A multiple 4 0 (0) 5 (25)

sequential logistic regression was employed to determine the risk 5 2 (0) 9 (45)

(OR) of inflammation associated with the use of PBM. The statistical Bold means that the have been statistically significant difference.
significance of all tests was defined as P < 0.05.
for PBM− and 69.7 ± 3.5 for PBM+ (P = 0.908). After 8 weeks, the
highest level of stability for the ISQ scale was achieved without dif-
3 | R E S U LT S ferences between both groups: 72.3 ± 7.4 for PBM− and 72.5 ± 4.3
for PBM+ (P = 0.938).
3.1 | Sample description

The sample was comprised of five male (38.4%) and eight female 3.3 | Postoperative inflammation
subjects (61.5%). Regarding the number of implants, a total of 40
implants were inserted, in 13 patients: 20 using PBM and 20 without A postoperative inflammation assessment was carried out 7 days
using it. With regards to the area, 28 of the implants were placed in after the clinical trial, the Figure 2 present the clinical aspect of the
the jaw (70%), 37 (92.5%) with a coarse periodontium, and 36 (90%) Landry et al. Healing Index(HI). The dichotomous method showed
with bone type II-­III-­IV. Table 2 shows the complete sample data. that the PBM+ group presented inflammation in seven implants
(35%), while the PBM− group presented inflammation in 14 implants
(70%) (P = 0.028). The healing index (HI) revealed variable heal-
3.2 | Primary and secondary stability ing levels in both groups. Nevertheless, the PBM+ group implants
showed better early healing (Table 3). Only two of the implants
The primary basal implant stability which was measured using the (18.2%) from the PBM− group were classified with the maximum
ISQ scale, showed results of 71.5 ± 8.8. The average basal stability healing index (HI = 5), whereas in the PBM+ group, nine implants
for the abutment was 71.9 ± 5.9, without significant differences. The (45%) were classified with the aforementioned index (P < 0.0001).
average stability 7 days after the laser application was 68.3 ± 8.6 for Considering HI as a quantitative variable, the PBM− group showed
the PBM− group, and 71.2 ± 5.9 for the PBM+ group (P = 0.228). an average healing of 2.1 ± 1.2, while PBM+ showed an average
After 4 weeks, the values became closer in both groups: 69.5 ± 7.4 HI of 4.10 ± 0.9 (P < 0.0001). Using the logistic regression, it was
142 | CAMOLESI et al.

F I G U R E 2 Clinical aspect of the Landry et al. healing index (HI), where 0 indicates poor healing and 5 indicates excellent healing

determined that the non-­application of the laser in the PBM− group healing abutment is placed on the implant, to prevent the edges
caused an OR of 4.333 times of presenting inflammation (IC95% from moving closer. First intention healing usually results in faster
1.150–­16.323; P = 0.030). healing and it has a lower risk of infection compared to second
intention healing (Pippi, 2017).
After having placed one-­abutment-­one-­time implants with
3.4 | Adverse events a successful primary stability, it was observed that PBM+ group
was less affected by inherent adverse biological processes inher-
No adverse events related to the use of PBM were observed, except ent to the surgical procedure. The average stability remained well-­
for the inflammatory processes that are associated with the surgical balanced in all of the ISQ measurements, recording results similar to
procedure itself. those obtained by Torkzaban et al. (2018). In their revision, Gholami
et al. (2019b) reported that some studies observed increased bone
activity at metabolic and cellular levels of the irradiated bone, as
4 | DISCUSSION well as faster bone regeneration. Regarding the measurements
made in this study, the mean stability values progressed equally in
PBM is a non-­invasive therapy that uses photochemical and bio- both groups throughout the study, except on the seventh day com-
logical interactions to generate energy to help speed up cellular pared to the immediate postoperative period in the same group.
reparation and regeneration processes (Hamblin, 2017). Reports The same results were observed in the studies by García-­Morales
of the use of LLLT after implant surgery have been experiencing et al. (2012), Matys et al. (2019) and Torkzaban et al. (2018) that is
an increase, this is due to the demand for better and more predict- to say, in the PBM+ group, the tendency to reduce implant stabil-
able results in terms of healing and postoperative inflammation ity was slower in the measurements made in the first 10–­15 days.
(Bozkaya et al., 2021; Gholami et al., 2019a). To the best of these This may be justified by the increased bone activity associated with
authors' knowledge, and as reported in a recent systematic review PBM, which accelerates both bone remodelling and the implant os-
(Qu et al., 2022), this is the first study analyzing the effects of diode seointegration process (García-­Morales et al., 2012).
laser irradiation at wavelengths of 808 and 630 nm combined, in an After the reduction of the initial stability, both groups experi-
attempt to achieve a significant therapeutic effect with respect to enced a progressive increase in ISQ and at week 8 they reached val-
improvement in implant stability, inflammation and tissue healing, ues very similar to the initial ones. The reduction process followed
respectively. by increased implant stability has also been reported in other studies
With regards to the biological processes that take place fol- (Matys et al., 2019; Torkzaban et al., 2018). Animal model studies
lowing dental implant surgery, that is to say, osseointegration; have reported a significant increase in osseointegration in PBM+
although primary stability is achieved, nonetheless, in the first groups, using an infrared wavelength (Khadra et al., 2004; Lopes
days following the implant placement the bone suffers restruc- et al., 2005; Maluf et al., 2010; Pereira et al., 2009). In our study,
turation, therefore a temporary reduction in implant stability is the application of PBM did not significantly improve the final stabil-
expected (Insua et al., 2017). Gum healing can take place either ity of the dental implant in the long term, given that after 8 weeks,
by first intention—­w hen the implant stays submerged and edge-­ there were no significant differences between the two groups in
to-­e dge suturing is performed—­or by second intention—­w hen a terms of the average stability values, and this was also observed in
CAMOLESI et al. | 143

TA B L E 3 Descriptive classification of each implant according to healing index (HI)

Tissue Presence of Presence of Incision Presence of Inflammation visual

colour bleeding granulation tissue margin suppuration Total score (HI) evaluation

Case 1 0 1 0 0 1 2 Yes
Case 2 0 1 0 1 1 3 No
Case 3 0 0 0 1 1 2 No
Case 4 0 1 1 0 1 3 No
Case 5 0 0 0 0 1 1 No
Case 6 0 0 1 0 1 2 Yes
Case 7 0 1 0 0 1 2 Yes
Case 8 0 0 1 0 1 2 Yes
Case 9 0 0 0 0 1 1 Yes
Case 10 0 0 0 0 1 1 Yes
Case 11 0 1 0 0 1 2 Yes
Case 12 0 0 0 0 1 1 Yes
Case 13 1 1 1 1 1 5 Yes
Case 14 0 1 0 0 1 2 Yes
Case 15 0 1 0 0 1 2 Yes
Case 16 1 1 1 1 1 5 Yes
Case 17 0 1 0 0 1 2 Yes
Case 18 0 0 0 0 1 1 Yes
Case 19 0 0 0 0 1 1 Yes
Case 20 0 1 0 0 1 2 Yes
Case 21 1 1 1 1 1 5 Yes
Case 22 0 1 0 0 1 2 Yes
Case 23 0 1 0 1 1 3 Yes
Case 24 0 1 1 0 1 3 Yes
Case 25 1 1 1 1 1 5 No
Case 26 1 1 1 1 1 5 No
Case 27 0 1 1 1 1 4 No
Case 28 0 1 1 1 1 4 No
Case 29 1 1 1 1 1 5 No
Case 30 0 1 1 1 1 4 No
Case 31 1 1 1 1 1 5 No
Case 32 1 1 1 1 1 5 No
Case 33 0 1 1 0 1 3 Yes
Case 34 0 1 1 1 1 4 Yes
Case 35 1 1 1 1 1 5 No
Case 36 1 1 1 1 1 5 No
Case 37 0 0 1 1 1 3 Yes
Case 38 1 1 1 1 1 5 No
Case 39 0 1 1 1 1 4 No
Case 40 0 0 1 1 1 3 Yes

other studies with the similar monitoring time (Bozkaya et al., 2021; better than those obtained for the PBM− group. 65% of the PBM+
García-­Morales et al., 2012; Lopes et al., 2005; Mandić et al., 2015; group's implants did not present with any subjective inflammation,
Torkzaban et al., 2018). and 45% of the same group attained the maximum score in the
The inflammation and healing responses obtained for the HI scale. It was not possible to carry out a comparative analysis
PBM+ group in the objective assessment and HI were considerably given that no prior studies in which the effect of PBM on gum
144 | CAMOLESI et al.

postoperative implant surgery healing and inflammation were as- considering the time required without mechanical stimulation for
sessed were found. The healing scale applied (HI) was evaluated in implants with deferred load. This measurement could yield more
studies that tested the effect of PBM on gum healing and inflam- revealing data in the PBM+ group. Other studies with designs that
mation following dental extraction (Hamzani & Chaushu, 2018). allow ISQ measurements without the need for reverse-­torque to
This better inflammatory and healing response with the applica- the implants are necessary. Another limitation inherent to the tech-
tion of PBM seems to be related to possible antimicrobial effects, nology itself lies in the impossibility of evaluating the bone/implant
thus in the study by Bozkaya et al., the PBM+ group presents a surface (especially in the buccal area) that absorbs/reflects the laser
significant reduction in the level of periodontal pathogenic bac- rays. The use of postoperative antiseptics and antibiotics (both med-
teria when compared to the PBM− group (Bozkaya et al., 2021). ically and ethically necessary) could produce biases based on indi-
Furthermore, several studies have reported an increase in vidual variability. The role of the implant diameter in relation to the
growth factors and anti-­inflammatory molecules in PBM+ groups crestal bone should be evaluated in more specific studies.
(Gokmenoglu et al., 2014; Hamblin, 2017; Memarian et al., 2018;
Tsai & Hamblin, 2017). This therefore justifies the results obtained
in this study, given that the acceleration of osteogenic signalling 5 | CO N C LU S I O N S
and bone and mucosa vascularisation favours healing processes
(Insua et al., 2017). In addition, accelerating the healing of the Long-­term applications of PBM do not interfere with implant stabil-
surgery wound and reducing the inflammatory process could may ity, and they may provide a good alternative for professionals that
help to prevent marginal bone loss (Fernandes et al., 2021), which need to increase these values in early phases for prosthodontic
would increase the chance of dental implant survival (Aguirre-­ reasons. With regards to healing and inflammation, PBM showed
Zorzano et al., 2013; Insua et al., 2017). excellent results in this study. Therefore, the application of 808 nm
In this study, we used the combined application of short and long infra-­red laser for bone tissue, and 630 nm for mucosal tissue in two
wavelengths as recommended by Qu et al. (2022), to verify whether sessions (in the immediate postoperative period and 7 days after) is
this protocol may produce more significant therapeutic effects. PBM considered to be an effective way of reducing inflammation and im-
therapy was applied on two separate occasions. The dose applied proving early healing of mucosal tissue, but ineffective to increase or
in each session was 13.32 J/cm2, with longer wavelength (808 nm), accelerate the secondary stability of implants. Long-­term monitoring
2
for bone tissue and 6.66 J/cm , with shorter wavelength (660 nm), of these implants is required in order to assess the role of PBM in
for mucosal tissue. These values are within the therapeutic window terms of marginal bone loss.
range and they are compatible with those found in the scientific
literature (Carroll et al., 2014; Gholami et al., 2019b). The control AU T H O R C O N T R I B U T I O N S
of employed energy level is essential, given that a weak stimulation Gisela Cristina Vianna Camolesi: Conceptualization (equal); data
may not activate a cellular response, and, likewise, a high stimula- curation (lead); formal analysis (supporting); investigation (equal);
tion may inhibit or even deactivate the cellular response (Dompe methodology (supporting); project administration (equal); re-
et al., 2020; Gholami et al., 2019a; Lima et al., 2020; Na et al., 2018), sources (equal); validation (equal); writing –­ original draft (lead).
meaning that there is an optimum stimulation within an energetic Manuel Somoza-­Martin: Conceptualization (equal); investigation
density range (dose). This dose, which is known as the therapeutic (equal); methodology (equal); project administration (equal); super-
window, biphasic dose response, or Arndt-­Schulz curve (Dompe vision (equal). M Dolores Reboiras-­López: Data curation (equal);
et al., 2020; Huang et al., 2011; Lima et al., 2020), is the responsible supervision (supporting). Fabio Camacho-­Alonso: Formal analysis
for cellular activation. If stimulation is not achieved or if it was over- (supporting); validation (supporting); writing –­ review and edit-
shot, the PBM protocol would be inadequate and would not work. ing (supporting). Andrés Blanco Carrión: Formal analysis (equal);
The absence of a specific PBM protocol has been already high- methodology (equal); supervision (equal). Mario Pérez-­Sayáns:
lighted by several authors as a problem (Bozkaya et al., 2021; Khadra Conceptualization (equal); data curation (supporting); formal analy-
et al., 2005; Qu et al., 2022; Woodruff et al., 2004). This is due, among sis (lead); investigation (lead); methodology (lead); project admin-
other factors, to the heterogeneity of the characteristics and parame- istration (equal); resources (equal); supervision (lead); validation
ters of the laser devices available on the market (Khadra et al., 2005; (equal); writing –­ original draft (supporting); writing –­ review and
Lima et al., 2020). It is important to note that PBM parameters that editing (lead).
work on one cell group will not necessarily work on another. In other
words, the ideal therapeutic window for hard tissues is not the same F U N D I N G I N FO R M AT I O N
as for soft tissues, just as surely the window to produce favorable The study was supported by Nueva Galimplant and the University
results for osseointegration in animals does not have the same effec- of Santiago de Compostela (Ref. USC-­2019-­CE178). The funding
tiveness in humans (Chen et al., 2019; Memarian et al., 2018). source played no role in the design of this study, the data collec-
The main limitation of this study was the impossibility of mea- tion and analyses, the decision to publish, and the preparation of the
suring the ISQ in the period between the second and eighth weeks, manuscript.
CAMOLESI et al. | 145

C O N FL I C T O F I N T E R E S T Elias, C. N., Rocha, F. A., Nascimento, A. L., & Coelho, P. G. (2012).

The authors declare that there is no conflict of interest. Influence of implant shape, surface morphology, surgical technique
and bone quality on the primary stability of dental implants. Journal
of the Mechanical Behavior of Biomedical Materials, 16, 169–­180.
DATA AVA I L A B I L I T Y S TAT E M E N T https://doi.org/10.1016/j.jmbbm.2012.10.010
Data available on request from the authors. Farivar, S., Malekshahabi, T., & Shiari, R. (2014). Biological effects of low
level laser therapy. Journal of Lasers in Medical Sciences, 5, 58–­62.
Fernandes, P. F., Grenho, L., Fernandes, M. H., Sampaio-­Fernandes, J. C.,
ORCID
& Gomes, P. S. (2021). Microgap and bacterial microleakage during
Gisela C. V. Camolesi https://orcid.org/0000-0003-0757-638X the osseointegration period: An in vitro assessment of the cover
José M. Somoza-­Martín https://orcid.org/0000-0001-9386-784X screw and healing abutment in a platform-­switched implant sys-
Maria D. Reboiras-­López https://orcid. tem. The Journal of Prosthetic Dentistry. https://doi.org/10.1016/j.
prosd​ent.2021.07.030
org/0000-0001-5792-8350
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Fabio Camacho-­Alonso https://orcid.org/0000-0002-3739-1792 L., Lagori, G., & Meleti, M. (2015). Different laser wavelengths
Andrés Blanco-­Carrión https://orcid.org/0000-0002-7405-1834 comparison in the second-­stage implant surgery: An ex vivo study.
Mario Pérez-­Sayáns https://orcid.org/0000-0003-2196-9868 Lasers in Medical Science, 30, 1631–­1639. https://doi.org/10.1007/
s1010​3-­014-­1623-­3
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