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Journal of International Dental and Medical Research ISSN 1309-100X
http://www.ektodermaldisplazi.com/journal.htm
Periodontal Regeneration of Bony defects in Smokers
Hossam A. Eid and Basma M. Zaki
EFFECT OF PLATELET-RICH PLASMA IN COMBINATION WITH BONE ALLOGRAFT IN
TREATMENT OF PERIODONTAL INTRA-BONY DEFECTS IN SMOKERS
Hossam A. Eid1, Basma M. Zaki2*
1. Assistant Professor, Oral Medicine and Periodontology Department , Faculty of Dentistry, Suez Canal University, Ismailia, Egypt,
Department of Periodontics, College of Dentistry, Gulf Medical University, Ajman, UAE.
2. Assistant Professor, Surgery and Oral Medicine Department, Oral and Dental Research Division, National Research Centre, Egypt.
Abstract
This study was conducted to evaluate the influence of smoking habit on the success of
periodontal regeneration in treating intra-bony periodontal defects when using Platelet Rich Plasma
(PRP) combined with Freeze Dried Bone Allograft (FDBA).
Thirty patients all diagnosed as having advanced chronic periodontitis were selected. The
patients were equally allocated into two equal groups: Group I; (n=15) which included non-smoking
patients having periodontal intra-bony defects managed with PRP and FDBA and Group II; (n=15)
included smoking patients having periodontal intra-bony defects managed with PRP and FDBA.
Clinical evaluation recording the plaque index (PI), gingival index (GI), pocket depth (PD), and
clinical attachment level (CAL) was done. Radiographic assessment was also carried out to
calculate the amount of bone gain. Estimation of the level of Platelet Derived Growth Factor
(PDGF-BB) was performed.
The results revealed that the clinical improvement, the amount of bone gain and the level of
PDGF-BB were more in the non-smokers group.
Smoking has a negative impact on the treatment outcomes of the periodontal intra-bony defects
following the combined treatment of PRP and FDBA.
Clinical article (J Int Dent Med Res 2016; 9: (1), pp. 55-63)
Keywords: Smoking, intra-bony periodontal defects, PRP, FDBA.
Received date: 19 February 2016
Introduction
The purpose of periodontal therapy is to
arrest the destruction accompanied with the
periodontal disease progression and to
regenerate the lost structures achieving optimal
comfort, function and esthetic appearance1.
The etiology of the chronic inflammatory
periodontal disease process is multifactorial in
nature. It results from the interaction between the
microbial infection and the host defense finally
leading to clinical attachment loss and alveolar
bone resorption 2-4.
*Corresponding author:
Dr. Basma Mostafa Zaki
Oral and Dental Research Division, National Research Centre, 33
El Bohouth Street, 12622 Dokki, Cairo, Egypt.
Phone: +201224901019
E-mail: [email protected]
Volume ∙ 9 ∙ Number ∙ 1 ∙ 2016
Accept date: 07 March 2016
Various studies conducted on animals
and humans proved that smoking can damage
the vascular and immunological systems tipping
the balance favoring the tissue breakdown 5. It
decreases the self-healing capacity of the tissues
of the periodontium. It was documented that, the
outcome of periodontal treatment in smokers is
less favorable as the host cytokine levels in biofluids is affected in smokers 6.
In
comparison
to
non
smokers,
periodontal pathogenic bacteria conquer higher
levels in smokers' patients. This is caused by the
direct modulation of the sub-gingival microflora
favoring the colonization of these pathogenic
bacteria 7.
In addition, there is increased evidence
that smoking may interrupt the normal healing
events of the periodontal tissues 8.
Clinical studies showed that after
adjusting the plaque accumulation to be similar in
both smokers and non-smokers the individuals
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who currently smoke presented deeper pockets
probing depth, greater loss of attachment, more
loss of bone, increased accumulation of supragingival calculus deposits and presence of less
number of teeth 9. Revascularization which is
mandatory for soft tissue healing and periodontal
regeneration in periodontal surgeries outcome
and implant placement can be negatively
affected by smoking. The nicotine products in
cigarettes can bind to root surface as reported in
vitro studies, leading to alteration of fibroblast
attachment and integrin expression with
decrease in collagen production and increase in
collagenase activity. Additionally, root surfaces of
extracted teeth from smokers were having less
periodontal ligament (PDL) fibroblast attachment
when compared to those teeth from nonsmokers10.
Different types of bone grafts have been
studied with different outcomes all aiming at
regeneration of periodontal defects. Autogenous
bone grafts are capable of providing viable
osteogenic cells. The use of allografts produced
either from humans from living donors or
cadavers as a source of osteogenic cells. In
addition they have the ability to act as space
fillers maintaining room under guided tissue
membranes. They can act as a vehicle for growth
factors as well 11.
Platelet Rich Plasma (PRP) is a
component of autologous plasma having a
platelet concentration above baseline rich in
platelet derived growth factors (PDGF) and
transforming growth factors (TGF-ß). It is
obtained by isolation and concentration of human
platelets by gradient density centrifugation
forming platelet gel 4.
It has been acknowledged that PRP can
decrease the bleeding during and after the
operations both at the donor and recipient sites
due to their potential in healing acceleration. It
can help in initially stabilizing the grafted tissue at
the recipient sites due to its cohesive and
adhesive nature as played in the wound healing
process 11.
Demineralized Freeze Dried Bone
Allograft (DFDBA) has proven to show significant
outcomes in the soft and hard clinical tissue
parameters when used in treatment of
intraosseous
periodontal
defects.
The
substances present in this grafting material i.e.
the bone morphogenic proteins is capable of
stimulating the local cells to produce new bone.
Volume ∙ 9 ∙ Number ∙ 1 ∙ 2016
Periodontal Regeneration of Bony defects in Smokers
Hossam A. Eid and Basma M. Zaki
The cell morphology and the chemical integrity
are still maintained even after the cells were
destroyed by the freezing and the drying process
4
. The process of its manufacturing eliminates the
concerns about the immunological responses
and the possibility of transmitting disease and
infection. Several studies reported the successful
use of PRP together with various bone grafts for
correcting periodontal osseous defects 12.
The goal of the current contemplate was
to clinically and radiographically evaluate the
treatment outcomes resulting from combining
both PRP and DFDBA to correct periodontal
intra-bone defects in smokers.
Patients and Methods
Thirty systemically healthy patients (18
males and 12 females), with an age range
between 20-45 years (mean age 32.8 ± 1.25)
diagnosed with advanced chronic periodontitis
according to the classification of the American
Academy of Periodontology 200013. These
patients were selected from the outpatient's
clinics at the Department of Oral Medicine and
Periodontology, Faculty of Dentistry, Suez Canal
University, Ismailia, Egypt and the dental clinic in
the medical services unit at the National
Research Centre (NRC). The study protocol was
approved from the Ethical Committee for Dental
Studies at the Faculty of Dentistry, Suez Canal
University, Ismailia, Egypt and the selected
patients signed an informed consent form
approving their participation after all the study
procedures were explained to them. The selected
patients have a total of forty intra-bony defects.
Patients included in the study were systemically
healthy with no contraindications to perform the
surgical operation and are having normal platelet
counts. They did not receive antibiotics in the
past six months prior to treatment and no
periodontal therapy in the past two years also.
The patients should have at least one vertical
osseous defect with probing pocket depth > 5mm.
It should be a radiographic evidence of
vertical/angular bone loss in the affected sites (at
least one site in the quadrant) and had at least 2
mm of keratinized gingiva on the facial aspect of
the selected tooth. Patients who are allergic or
sensitive to any medications and / or local
anesthesia used in the study were excluded from
the study. Also pregnant and lactating mothers
were not included in this contemplate. Teeth with
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severe attrition and extensive mobility were
excluded from the selection of the cases.
Initial Periodontal Therapy
Scaling and root planing (SRP) was
performed for all the patients in addition to oral
hygiene instructions teaching.
Study Design
All the thirty patients selected to be
included in this experiment were equally divided
into two groups: Group I; (n=15) which included
non-smokers patients with periodontal intra-bony
defects corrected with PRP and FDBA and
Group II; (n=15) included smoking patients with
periodontal intra-bony defects corrected with
PRP and FDBA.
Periodontal assessment was carried out
before starting the initial therapy (baseline) and
at 6 and 9 months after treatment for both groups.
At baseline evaluation, all clinical parameters
were measured and mechanical treatment
including removal of all supra and sub-gingival
calcified deposits to obtain smooth and clean
surfaces was done. For each patient the oral
hygiene was checked every two weeks for 9
months. All patients were trained and
encouraged to maintain their dental health and
plaque control through brushing and flossing. All
clinical assessment measurements were taken
by one investigator. All subjects received clinical
examination including recording of the following
periodontal parameters for all the teeth; Plaque
index (PI) 14, gingival index (GI) 15, pocket depth
(PD) 16 and clinical attachment level (CAL). All
the clinical measurements were done at six
locations for all teeth named mesiobuccal,
mesiolingual, midbuccal, distobuccal, distolingual,
and midlingual. PI was assessed by measuring
the presence or absence of supragingival biofilm
with performing of a sweeping motion of the
probe around the buccal, mesial, distal, and
lingual sites of all teeth. Marginal gingival
bleeding was estimated with GI. PD was
recorded from the free-gingival margin to the
base of the periodontal pocket (measured in
millimeters) using UNC‑15 periodontal probe and
CAL was recorded from the cemento-enamel
junction of the tooth to the base of the
periodontal pocket (also recorded in millimeters).
Utilizing the Michigan 0 probe with Williams'
markings,
all
the
measurements
were
approximated to the most elevated whole
Volume ∙ 9 ∙ Number ∙ 1 ∙ 2016
Periodontal Regeneration of Bony defects in Smokers
Hossam A. Eid and Basma M. Zaki
millimeter. The CEJ determination was made by
using the anatomical CEJ or the apical extent of
the existing restoration margin on each tooth.
Plaque assessment using disclosing tablets were
assessed every two weeks along the whole 9
months study period.
Radiographic Assessment
Intraoral periapical radiographs were
taken using parallel technique with a Rinn XCP
film holder (ENDEX INSTRUM, Germany). The
distance from the alveolar crest (AC) 17 to the
base of the bone defect depth was recorded. The
point at which the periodontal ligament space is
continuously in width at the most coronal point is
considered the base of the defect (BOD). The
difference between the initial and the final defect
depth at the recall time intervals was considered
as the amount of defect fill or bone gain occurring.
Percentage of bone gain or defect fill was also
calculated 11.
Preoperative evaluation
Occlusal stents were fabricated with cold
cured acrylic resin on a cast model obtained from
an alginate impression for accurate positioning of
the periodontal probe aiming at reproducibility.
The occlusal stent was made to cover the
occlusal surface of the tooth being treated and
the occlusal surfaces of at least one tooth in
mesial and distal directions. Stents were also
extended apically on the buccal and lingual
surfaces to cover the coronal third of the teeth
involved 6. Post-surgical measurements were
done using the same probe position and
angulation grooves prior to surgery. All smokers
were advised to stop smoking at least for two
months following the surgical procedures and
were directed to smoking cessation program.
PRP Preparation
One hour before the surgery, 10 ml of
blood was withdrawn from the anticubital vein of
the patient and collected into vacutainer tube
containing sodium citrate as an anticoagulant. It
was then placed in an automated centrifuge. First
spin of 1200 rpm for 20 min separated the whole
blood into three fractions that is, platelet poor
plasma (PPP), PRP and red blood cells (RBC).
After discarding the RBC fraction a second spin
of 2000 rpm for 15 min was given that separated
the components into PPP and concentrated PRP
(cPRP) 18. After discarding the PPP, the
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remaining cPRP was activated by clot initiator
(human thrombin) and 10% calcium chloride to
obtain a sticky gel consistency. Platelet counts
were performed on each sample, including a
peripheral blood count and PRP count by
hemocytometer 19. Minimum 3 times increase in
platelet count (PC) from baseline PC were
considered adequate for use.
Surgical procedures
The surgical procedure was performed by
local infiltration of 2% xylocaine hydrochloride
with
adrenaline
1:80,000.
Buccal
and
lingual/palatal sulcular incisions were used, and
full-thickness mucoperiosteal flaps were elevated
with a blunt dissection using a periosteal
elevator. Care was excised to preserve as much
inter-proximal
tissue
as
possible.
After
meticulous defect debridement and removal of
granulation tissue, grafting materials were placed
up to the vertical height of the corresponding
adjacent bone level. Surgical flap was
repositioned and sutured with 3-0 black silk and
covered with a periodontal pack.
Post-operative Care
Patients were given analgesics (ibuprofen
400 mg every 8 h) and antibiotics (amoxicillin 500
mg every 6 h) for 5 postoperative days and were
advised to use 0.12% chlorhexidine mouth rinse
twice daily for 14 days. Subjects were recalled
after 1 week for suture removal, thereafter every
two weeks for oral hygiene condition assessment
during the whole experiment period.
Laboratory Investigations
GCF samples were gathered from the
post-surgical sites after periodontal pack removal.
Prior to GCF sampling, the supragingival plaque
was evicted from the surfaces with a sterile
curette carefully; these surfaces were desiccated
with water spray, dried gently by an air syringe
and isolated with cotton rolls. GCF was sampled
using filter paper strips (Perio-paper, IDE
Interstate, Amityville, NY, USA) carefully inserted
into the crevice until mild resistance was felt and
left there for 30 seconds. Care was taken to
elude any possible mechanical injury. Strips
contaminated with blood were discarded.
Immediately, the volume of the sample was
measured with the aid of a calibrated Periotron
8000 (Oraflow Inc., Amityville, NY, USA). After
volume measurements, the strips were placed
Volume ∙ 9 ∙ Number ∙ 1 ∙ 2016
Periodontal Regeneration of Bony defects in Smokers
Hossam A. Eid and Basma M. Zaki
into sterile eppendorf tubes containing 300 μL
PBS (Phosphate buffered saline). All GCF
samples were immediately stored at −20◦C until
subsequent analysis. The readings from the
Periotron 8000 were converted to an actual
volume (µL) by reference to the standard curve.
Later the samples were examined by Enzyme
Linked
Immuno-Sorbant
Assay
(ELISA)
technique (Quantikine Kit, R&D systems, UK) to
detect the concentrations of the Platelet Derived
Growth Factor (PDGF-BB), for the groups
included in this contemplate.
Statistical Analysis
Numerical data were presented as mean
and standard deviation (SD) values. Data's
normality was explored using KolmogorovSmirnov test of normality. Mann Whitney U test
was essential in comparing PI, GI, PD, and CAL
before and after treatment in both studied groups
at the different time periods. The percentage of
change between baseline and different follow up
times was explored in both groups using either
Mann-Whitney or student t-test according to the
normality of the data. Percentage of radio-opacity
was calculated, which was analyzed by chisquare test. The significance level was set at p ≤
0.05. Statistical analysis was performed with
SPSS 18.0, Chicago, IL, USA.
Results
The healing of soft tissue in all patients
included in this contemplate was uneventful and
lacked any inconvenience postoperatively during
the follow up period of nine months. Only during
the first week, analgesics were minimally used
because the patients experienced moderate pain
and discomfort. None of the patients showed
post-operative swelling. After one week pain
subsided completely.
1) Clinical Assessment:
Table (1) shows the mean ± standard
deviation (SD) and p- values of PI, GI, PD and
CAL before and after treatment in both groups I
and II.
a)
Plaque index (PI) measurements:
The results revealed no statistical
significant difference between Groups I and II
before treatment with p-value 0.0262. After
treatment there was a statistically significant
decrease in PI scores in both groups after 6
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months with p-value 0.059 and also after 9
months with p-value 0.023.
Periodontal Regeneration of Bony defects in Smokers
Hossam A. Eid and Basma M. Zaki
2) Radiographic Assessment
Standardized Periapical radiographs were
taken using the parallel technique with Rinn film
holders at baseline and during the follow up
periods for each case. These films were scanned
by Scanrom 4E scanner connected to IBM
computer. The images were analyzed by
software in the computer and the percentage of
radio-opacity was calculated, which was
analyzed by chi- square test. Qualitative
assessment of periapical films showed that there
was an increase in bone density in both study
groups along the different study periods. These
changes in the percentage of radio-opacity were
statistically significant at the different time
intervals as shown in table (2).
Table 1. Showing the mean ± SD values of PI, GI,
PD and CAL at baseline, 6 and 9 months in both
study groups
b)
Gingival index (GI) measurements:
The results showed no statistically significant
difference between groups I and II before
treatment with p-value 0.661. Following treatment
there was a statistically significant drop of GI
scores in both groups after 6 months with p-value
of 0.022 and after 9 months with p-value of 0.021.
c)
Pocket depth (PD) measurements:
The results showed that there was no
statistically significant difference between group I
and II before treatment with p-value 0.696. After
treatment there was a statistically significant
reduction of PD values in both groups after 6
months with p-value of 0.017 and after 9 months
with p-value of 0.014.
d)
Clinical
attachment
level
(CAL)
measurements:
There was no statistically significant difference
between group I and II before treatment with pvalue 0.742. After treatment there was a
statistically significant decrease of CAL
measurements in both groups after 6 months
with p-value of 0.023 and after 9 months with pvalue of 0.008.
Volume ∙ 9 ∙ Number ∙ 1 ∙ 2016
Table 2. Showing the percentages of
improvement of the various measured clinical
parameters in both studied groups.
Looking to the results of the mean bone
gain; it was revealed that there was a statistically
significant increase in both groups I and II when
comparing the baseline with the 6 and 9 months
records with the more bone gain in Group I.
Meanwhile there was no statistically significant
gain of bone comparing the 6 and 9 months
records with the more bone gain in Group I.
The results revealed that at baseline there
was no significant difference in the percentage of
radio-opacity between group I (55%) and group II
(52%). After 6 months there was a statistically
significant increase in the percentage of radioopacity between groups I (75.4%) and II (62.1%).
After 9 months the percentage of radio-opacity
showed a statistically significant increase
between groups I (85.8%) and II (71.2%) as
shown in table (3).
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Periodontal Regeneration of Bony defects in Smokers
Hossam A. Eid and Basma M. Zaki
Discussion
Table 3. Shows the amount of bone gain and the
percentages of radio-opacities in both study
groups.
PDGF-BB Concentration:
ELISA was used to measure the PDGFBB concentrations in gingival crevicular fluid
(GCF) in both study groups at 3, 5 and 7 days as
shown in table (4). The highest level of PDGF
concentration was found in group I at the 3rd day
(1734 µg). Smokers group (II) showed a lowest
concentration of PDGF (553.9 µg).
Table
4.
Mean
Values
of
PDGF-BB
concentration (µg) in both study groups at 3, 5, 7
days.
At 5 days both groups still have a high
concentration of PDGF when compared to the
control (5531.74 µg). Group II which less level of
PDGF concentration (425 µg) than the control
group. At 7 days the only group that retained a
high PDGF concentration level was that of group
I. The value of PDGF concentration was (1361
µg) which was statistically more elevated than
that of group II.
Volume ∙ 9 ∙ Number ∙ 1 ∙ 2016
The main goal of treating diseased
periodontium is to create an environment capable
of maintaining optimum health, comfort and
function. Different clinical investigations have
compared the difference of responses of nonsmokers and smokers toward the various types
of periodontal disease treatment modalities
outcomes including both surgical and nonsurgical therapies 10.
The increased use of DFDBA currently is
related to its proved osteoinductive properties.
Different histological studies documented that it
is more effective in inducing periodontal
regeneration 10, 20.
The addition of growth factors can provide
extra stimulus for optimum regeneration through
modulation of cells residing within the
periodontium 21.
PRP is a rich source for obtaining growth
factors. PRP when added to hydroxyapatite,
bovine porous bone mineral and barrier
membrane has been used to treat periodontal
defects with documented good outcomes 22-24.
Our study revealed the significant
improvement in the measured clinical parameters
namely PI and GI scores, PD and CAL
measurements (at 6 and 9 months). Calculation
of the percentages of improvement showed that
the results are more favorable in the nonsmokers group. This is line with the explanation
in a study presenting that such changes in index
scores might be attributed to the maintenance of
oral hygiene along the time intervals of the
study25. Various studies have shown similar
improvements in plaque and gingival indices 26-28.
In different evaluations conducted to treat
intrabony defects investigating the influence of
smoking on the periodontal regenerative process
revealed less decrease in PD and gain of CAL in
smokers as compared to non-smokers patients 29,
30
. This was attributed primarily to the decrease
in gingival inflammation and shrinkage of pocket
wall after treatment. The study pointed out the
detrimental effect of smoking on the periodontal
regenerative process as 10.
Growth factors (GF) abundantly exist in
PRP. Bone regeneration is affected by some of
the GF such as PDGF and TGF-B. Successful
results were reported from various animal and
human studies provided solid evidence that PRP
is capable of enhancing the wound healing
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process and aids in the reconstruction of soft
tissues specifically in conjunction with bone
grafts 31.
It was evident from the results of the
present experiment that, using PRP in
combination with bone allografts to treat the bony
defects caused by the destructive process of
periodontal disease, can effectively improve all of
the tested clinical periodontal parameters. These
findings strengthen forward other studies 32-35.
The mechanism by which PRP aids the
regenerative process of the periodontium is not
completely understood. However, it has been
discussed that PDGF, present in PRP affects
mostly the osteoblastic cell proliferation process.
In addition, PRP contains high fibrin content that
provides a sticky nature working as a
haemostatic and stabilizing agent that might aid
in blood clotting and bone graft immobilization in
the defect area, hence, plays an important role in
periodontal regenerative procedures. PDGF
proved
to
stimulate
angiogenesis
and
differentiation of undifferentiated mesenchymal
cells. It can also activate macrophages which
play an essential role in secondary wound
healing 36. It was also documented by Marx et al
37
that adding concentrated platelets to bone
grafts results in increased maturation rate and
density of the autogenous grafts.
It is noteworthy to mention that, there are
some studies reporting that PRP preparation has
a limited potential to promote local bone
formation; using of PRP did not provide any
significant outcome on bone implant contact 38-39;
a limited bone formation was obtained with BioOss with or without PDGF 40. No obvious positive
effect on bone formation or working as
osteoinductive material was reported when PRP
was used after an implantation period of four
weeks and even no negative effect was
documented 41.
Results of the present study seem to be
not consistent with these findings. This
contradiction can be attributed to several factors
including: degree and severity of periodontal
disease affecting included patients; concentration
of PRP used; parameters used in assessment of
periodontal status before and after treatment,
time of evaluation during follow up as well as,
methodological
characteristics
of
each
investigation. The assessment of periodontal
condition of the patients included in the present
study was performed using more than one
Volume ∙ 9 ∙ Number ∙ 1 ∙ 2016
Periodontal Regeneration of Bony defects in Smokers
Hossam A. Eid and Basma M. Zaki
clinical parameter, as dependence upon only one
parameter can not reflect clearly the exact
disease or health status.
The absence of any allergic reactions,
abscesses, or rejection of the implanted
materials documented the high tolerance of the
materials used. This is in line with previous
studies proving the absence of allergic or foreign
body reactions 42.
Results of this contemplate reported the
high bone gain which is more obvious in the nonsmokers group denoting the detrimental effect of
smoking on the periodontal regenerative process.
A study was conducted in non-smokers
reporting the high amount of bone gain and the
increased percentage of bone fill in sites
managed with the combination of PRP and ßtricalcium phosphate (ß-TCP) 43. Also other
contemplate 44 adding PRP to bone grafts to treat
intrabony defects presented the beneficial effect
of this combination by the increased radiographic
maturation rates measured.
In line with our study greater bone height
was observed when PRP was used with
allogenic bone in treating periodontal bony
defects 44. The same results were obtained 45
after using hydroxyapatite with PRP showing the
significant defect fill.
On the other hand non-significant
difference was revealed in a contemplate by
Tamura et al examining the relative amounts of
mineralized bone when PRP was added to
porous ß-TCP in treating intra-bony defects 46.
Other studies conveyed an unfavorable
outcome after periodontal regeneration in
smokers having different types of periodontal
defects 47, 48, 49, 50.
Even though, the exact mechanism of
how smoking affects the periodontal regeneration
outcome is not clarified yet. Some in vitro studies
conveyed that the proliferation, attraction and
chemotaxis of periodontal ligament cells is
adversely affected by nicotine and smoking by
products. Not only this, but also the latter
intensifies the effect of periodontal pathogenic
toxins 51, 52, 53.
Moreover,
smokers
revealed
a
deteriorated peripheral blood supply owing to
vasoconstriction caused by nicotine and
debilitated oxygen transport and metabolism
caused by carbon monoxide 54, 55, 56, 57, 58, 59.
Therefore, since smoking seems to interrupt
stages of the reparatory/regenerative process in
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the periodontal wound it can thereby compromise
generally the healing process.
Conclusion
The results of the present contemplate
documented the negative effect of smoking that
can impair the healing outcomes of periodontal
regeneration.
Declaration of Interest
The authors report no conflict of interest
and the article is not funded or supported by any
research grant.
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