10.59987/ads/2015.1.21-28
Aim. To evaluate the impact of smoking and previous periodontal disease on peri-implant microbiota and health in medium to long-term maintained patients.
Methods. A retrospective evaluation of partial edentulous patients restored with dental implants and enrolled in a regular supportive therapy was performed. Inclusion criteria were: medium to long-term periodontal and implant maintenance (at least 5 years), a minimum of 2 implants placed in each patient, absence of systemic diseases that may affect osseointegration. 30 implants in 15 patients were included in the study. Subjects were divided in smokers or non-smokers and between patients previously affected by periodontal disease and periodontally healthy. Peri-implant and periodontal parameters were assessed (PD,BoP, mPI). Microbiological samples were collected around implant and an adjacent tooth. Real- Time Polymerase Chain Reaction (RT-PCR) analysis was performed.
Results. In all the three groups no differences in bacterial counts between dental and implant sites were observed. Non smoker, healthy patients: healthy clinical parameters, significant counts of spirochetes in isolated patients. Non smokers with previous periodontal disease: occasional positive BoP values, significant high counts of pathogenic bacteria. Smokers with previous periodontal disease: clinical signs of inflammation including deep pockets and slight bone resorption, significant counts of pathogenic bacteria.
Conclusions. Over a follow-up of 5 to 7 years, it is possible to state that the absence of smoking habit and previous periodontal disease positively influences the peri-implant microbiological and clinical conditions in partial edentulous patients restored with dental implants and enrolled in a strict regular supportive therapy.
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Annali di stomatologia
long-term maintenance
The impact of smoking and previous periodontal disease on peri-implant microbiota and health: a retrospective study up to 7-year follow-up
Text.Serial.Journal
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Original Article
2022-08-12
2022-08-12
2015-03-01
2023-12-04
21-28
Ann Stomatol (Roma)
I. Vozza
2015
10.59987/ads/2015.1.21-28
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1971-1441
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long-term maintenance
en
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The impact of smoking and previous periodontal disease on peri-implant microbiota and health: a retrospective study up to 7-year follow-up
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                                                                                                  Original article



    The impact of smoking and previous periodontal
    disease on peri-implant microbiota and health:
    a retrospective study up to 7-year follow-up




                                                                                                     i
                                                                                                   al
                                                                                                on
    Alessandro Quaranta, DDS, PhD1                            were observed. Non smoker, healthy patients:
    Bartolomeo Assenza, DDS, MD2                              healthy clinical parameters, significant counts of
    Orlando D’Isidoro, DDS3                                   spirochetes in isolated patients. Non smokers
    Fabia Profili, RDH4                                       with previous periodontal disease: occasional
    Antonella Polimeni, MD, DDS5                              positive BoP values, significant high counts of




                                                                                       zi
    Iole Vozza, DDS, PhD5                                     pathogenic bacteria. Smokers with previous peri-
                                                              odontal disease: clinical signs of inflammation in-
                                                              cluding deep pockets and slight bone resorption,




                                                                          na
    1 Division of Periodontology, Department of Oral Sci-     significant counts of pathogenic bacteria.
      ences, Faculty of Dentistry, University of Otago,       Conclusions. Over a follow-up of 5 to 7 years, it is
      New Zealand                                             possible to state that the absence of smoking
    2 Private Practice, Milano, Italy                         habit and previous periodontal disease positively
    3 School of Dentistry, Division of Periodontology, Uni-   influences the peri-implant microbiological and




                                                                er
      versity Politecnica delle Marche, Ancona, Italy         clinical conditions in partial edentulous patients
    4 School of Dental Hygiene, University Politecnica        restored with dental implants and enrolled in a
      delle Marche, Ancona, Italy                             strict regular supportive therapy.



                                                        t
    5 Department of Oral and Maxillo Facial Sciences,

      Sapienza University of Rome, Italy
                                                     In       Key words: microbiota, periodontal disease,
                                                              smoking, dental implants, long-term maintenance.

    Corresponding author:
    Alessandro Quaranta                                       Introduction
                                                 ni
    Faculty of Dentistry, University of Otago
    310 Great King Street, PO BOX 647, Dunedin, New           The development of biofilm on implant surfaces
    Zealand
                                     io

    E-mail: alex.quaranta@otago.ac.nz                         The introduction of dental implants as surgical and-
                                                              prosthetic procedures to replace lost natural teeth,
                                                              due to dental caries, trauma or periodontal disease,
    Summary                                                   has been a major advance in the management of fully
                           iz



                                                              and partially edentulous individuals. The surfaces of
    Aim. To evaluate the impact of smoking and pre-           the inserted implants represent a new opportunity for
    vious periodontal disease on peri-implant micro-          bacterial colonization and lead to a microbial profile
           Ed




    biota and health in medium to long-term main-             that might be substantially different from the one
    tained patients.                                          found on natural teeth. The immune-blot technique,
    Methods. A retrospective evaluation of partial            used for the study of bacterial colonization in os-
    edentulous patients restored with dental implants         seointegrated implants, has led to the recognition of
    and enrolled in a regular supportive therapy was          five different species: Porphyromonas gingivalis, Pre-
    performed. Inclusion criteria were: medium to             votella intermedia, Actinomycesnaes lundii, Fusobac-
IC




    long-term periodontal and implant maintenance             terium nucleatum, Treponemasocranskii (1). The re-
    (at least 5 years), a minimum of 2 implants placed        sults showed that implants in partially edentulous
    in each patient, absence of systemic diseases             subjects were colonized by periodontal pathogens as
    that may affect osseointegration. 30 implants in          early as 14 days after the exposure to the oral envi-
C




    15 patients were included in the study. Subjects          ronment and that the establishment of a complex
    were divided in smokers or non-smokers and be-            subgingival microbiota occurred as early as 28 days
    tween patients previously affected by periodontal         after exposure. Biofilm development on teeth and im-
    disease and periodontally healthy. Peri-implant           plants was also compared during a 3-week study of
©




    and periodontal parameters were assessed                  experimental gingivitis and peri-implant mucositis us-
    (PD,BoP, mPI). Microbiological samples were col-          ing phase contrast microscopy (2). It was evident that
    lected around implant and an adjacent tooth. Re-          the biofilm revealed similar proportions of coccoid
    al-Time Polymerase Chain Reaction (RT-PCR)                cells, motile rods, and spirochetes (spp) on both teeth
    analysis was performed.                                   and implants at baseline and after three weeks of
    Results. In all the three groups no differences in        plaque accumulation. The development of biofilms on
    bacterial counts between dental and implant sites         titanium surfaces was also examined in partially

    Annali di Stomatologia 2015; VI (1): 21-28                                                                    21
    A. Quaranta et al.


    edentulous subjects who required implants (3). High-        of 10 years, statistically significant differences existed
    er counts of complex species were detected on the           between implants and matching control teeth with re-
    tooth surfaces at all time points, particularly at 2        gard to most of the clinical and radiographic parame-
    weeks. At later time points, the differences between        ters with the exception of plaque index and recession.
    the sampled sites were less marked, although com-           Marginal bone level at implants at 10 years was also




                                                                                                          i
    plex species were still at higher levels in the dental      associated to smoking and general health condition.




                                                                                                        al
    sites compared to implant ones. The above studies
    indicate that the early development of biofilms on im-
    plant surfaces is similar to the one observed on nat-       Dental implant prognosis in periodontally com-




                                                                                                     on
    ural teeth. Studies about the development of biofilms       promised partially edentulous patients
    on natural teeth showed that attachment of bacterial
    occurred within minutes and that the increase in spe-       The outcome of implant treatment in periodontally
    cific species could be detected in a time period as         compromised partially edentulous patients has not
    short as 2-6 hours. It is likely that biofilm develop-      been completely clarified. In this regard, it is signifi-




                                                                                           zi
    ment on the implant follows a similar course and that       cant a recent review from Karoussis et al. (10). The
    maturation is well under way by 2 weeks as provided         Authors completed a comprehensive and critical re-
    by Quirynen et al. (4).                                     view of all the studies regarding the short-term and




                                                                             na
                                                                long-term prognosis of osseointegrated implants
                                                                placed in periodontally compromised patients. 15
    The microbiological pattern in partially edentulous         prospective studies were selected, including seven
    subjects                                                    short-term and eight long-term studies. The results of




                                                                  er
                                                                this review revealed that no statistically significant dif-
    The literature comparing the bacterial profile around       ferences in both short-term and long-term implant
    implants in fully edentulous subjects with the micro-       survival exist between patients with a history of
    biota in partially edentulous subjects confirms the role    chronic periodontitis and periodontally healthy individ-
    of the remaining dentition as a major source for colo-


                                                          t     uals. However, patients with a previous history of
    nization. Studies comparing the peri-implant micro-
    biota with the bacteria of adjacent teeth described
                                                       In       chronic periodontitis may exhibit significantly greater
                                                                long-term probing pocket depths, peri-implant margin-
    several similar aspects in the two sites. In partial        al bone loss and incidence of peri-implantitis com-
    edentulous subjects, bacterial counts did not signifi-      pared with periodontally healthy subjects. Alterations
    cantly differ between subgingival dental and implant        in clinical parameters around implants and teeth in
                                           ni
    samples (5). Moreover, the bacteria around healthy          aggressive periodontitis patients may not follow the
    implant and dental sites were extremely similar. This       same pattern, in contrast to what has been reported
    observation suggests that the major influence on the        for chronic periodontitis patients. Therefore, more
                                 io

    peri-implant microbiota was the bacteria present on         studies are required to evaluate implant prognosis in
    the remaining teeth.                                        this form of periodontitis. Other systematic reviews
                                                                (11-13) have provided the highest level of evidence
                                                                supporting the favorable long-term prognosis of im-
                         iz



    The association between periodontal and peri-im-            plant therapy in the general population. However,
    plant conditions                                            fewer data seem to be available concerning the prog-
                                                                nosis of implants placed in periodontally compro-
          Ed




    It may be assumed that the peri-implant tissue re-          mised patients and the incidence of implant biological
    sponse to the bacterial challenge may follow patterns       complications appear to be higher in patients previ-
    similar to that of the periodontal tissues in a suscepti-   ously affected by periodontitis.
    ble host (6, 7). So far, it has not yet been clarified
    whether a host susceptible for periodontitis will also
    be susceptible for peri-implantitis. However, there is      Smoking and dental implant failure
IC




    evidence for the association between periodontitis
    and peri-implantitis (8). It is sure also that smoke, lo-   Cigarette smoking has been related with an in-
    cal and systemic conditions and the presence of sub-        creased risk for peri-implantitis, marginal bone loss
    gingival pathogenic bacteria play an important role in      around implants, and loss of implants (14-16).
C




    the occurrence of complications. However, the biolog-       It is therefore essential that the dental team explain
    ical impact of these factors on the long-term progno-       the patient that smoking can contribute to complica-
    sis of oral implant is still to be defined. Karoussis et    tions following implant insertion.
    al. (9) compared in a prospective study the clinical        Several historical follow-up studies have shown that
©




    and radiographic changes in periodontal and peri-im-        cigarette smoking is a significant risk factor from im-
    plant conditions in a population susceptible to peri-       plant failure (17, 18).
    odontal diseases. This study investigated the associ-       Smokers are more susceptible to both periodontitis
    ation of changes in periodontal parameters and peri-        and peri-implantitis because of impairment of immune
    implant conditions over a mean observation period of        response (19) and compromised wound healing (20).
    10 years (8-12 years) following implant installation.       Increased probing depths, plaque indices and bleeding
    The results of this study indicated that after a period     on probing values have been observed in smoker sub-

    22                                                                              Annali di Stomatologia 2015; VI (1): 21-28
    The impact of smoking and previous periodontal disease on peri-implant microbiota and health: a retrospective study up
    to 7-year follow-up

    jects restored with dental implants. A systematic re-         Reproducibility of probing procedure was evaluated
    view of the literature that assessed implant loss, bone       by clinical assessment in 9 implants in 5 patients dur-
    loss greater than 50%, implant mobility, persistent           ing two separate sessions 1 week apart and linear
    pain, or peri-implantitis, reported that smokers had a        weighted kappa (κ) score was calculated.
    significantly enhanced risk of peri-implantitis (21).         Later, microbiological samples of the subgingival




                                                                                                           i
    The aim of the present study was to evaluate the im-          biofilm were collected by carefully removing supra




                                                                                                         al
    pact of smoking and previous periodontal disease on           gingival plaque and inserting five paper points in
    the microbiota and peri-implant health in a group of          each implant site and an adjacent tooth. The samples
    partial edentulous patients restored with dental im-          were then analyzed by Carpegen© Perio Diagnostics,




                                                                                                      on
    plants. All the subjects included in this retrospective       Munster, Germany. This analysis is based on a Real-
    study had been enrolled in a regular supportive thera-        time PCR procedure that detects and quantifies the
    py program fora medium to long term period (5-7               presence of the following bacterial species: Aggregati
    years of restoration function).                               bacter Actinomycetem comitans (A.a.), Fusobacteri-
                                                                  um nucleatum (F.n.), Porphyromonas gingivalis




                                                                                             zi
                                                                  (P.g.), Prevotella intermedia (P.i.), Treponemadenti-
    Materials and methods                                         cola (T.d.), Tannerella forsythia (T.f.). The PCR-Real
                                                                  Time parameters were the following:




                                                                                na
    Selection of patients:                                        - a detection limit for each of the five pathogens of
    Patients were enrolled during January to February                 100 bacteria within a patient’s sample;
    2014 in a private dental practice (B.A.) in Milan, Italy.     - a linear range for quantification that comprehends
    A retrospective search for patients restored with fixed           seven orders of magnitude for each pathogen;




                                                                     er
    partial dentures supported by dental implants and en-         - a coefficient of variation is 15%.
    rolled in regular supportive periodontal therapy (at          The bacterial genomic DNA was isolated and purified
    least four times per year) was performed. The study           with the AGOWAs mag DNA Isolation Kit Sputum
    was conducted in compliance with the “Ethical princi-         (AGOWA GmbH, Berlin, Germany). Primers and
    ples for medical research involving human subjects”


                                                           t      probes for Carpagen Perio Diagnostics were de-
    of Helsinki Declaration.
    Inclusion criteria were the following:
                                                        In        signed to match highly specifically to ribosomal DNA
                                                                  (rDNA) of the five bacterial pathogens. The exact
    - medium to long-term implant and periodontal                 primer and probe sequences were selected with the
        maintenance (at least 60 months after the delivery        Primer Express software (Applied Biosystems, Foster
        of the final implant supported restoration)               City, CA, USA), which checks the primer and probe-
                                                 ni
    - 2 to 3 dental implants (Bone System, Milan, Italy)          sets for matching the guidelines that are recommend-
        previously inserted in each partial edentulous patient    ed for real-time PCR with TaqMan’s probes. The
    - no uncontrolled diabetes                                    primers and probes were obtained from Applied
                                     io

    - no pregnancy and lactation                                  Biosystems. Real-time PCR was carried out with 2 ml
    - no use of antibiotic or corticosteroids in the last         of the isolated DNA as template in a reaction mixture
        three months                                              containing the appropriate primer probesets and the
    - no active, untreated periodontal infection of the nat-      TaqMans Universal PCR Mastermix. The PCR was
                           iz



        ural dentition assessed at the clinical evaluation.       carried out in a real time PCR cycler (LightCycler®
    A total of 15 patients and 30 implants have been selected.    480 II” Roche Diagnostics Ltd., Rotkreuz, Switzer-
    Patients were subdivided in the following three sub-          land). A laboratory code has been assigned to each
           Ed




    groups according to previous periodontal disease and          patient (Tab. 1).
    smoking habit:                                                All the data were assembled, results analyzed and
    - Group 1: Non smoker, periodontally healthy pa-              manuscript written by first author (A.Q.) from August
        tients.                                                   to December 2014 at the Department of Oral Sci-
    - Group 2: Non smoker subjects previously affected            ences, Faculty of Dentistry, University of Otago, New
        by periodontitis.                                         Zealand.
IC




    - Group 3: Smokers, previously affected by peri-
        odontitis.
    Periodontally healthy smoker patients that fulfill the        Results
    inclusion criteria were not found within the entire pop-
C




    ulation of the dental practice.                               A total of 15 patients (9 males-6 females) was en-
                                                                  rolled in the present study. The average age of male
                                                                  patients was 53.3 years; the average age of female
    Clinical and microbiological procedures                       patients was 53.4 years, the mean patients’ follow-up
©




                                                                  was 60.5 months (range 5 to 12 years).
    All the patients were recalled for supportive therapy         Microbiological results described the counts for each
    and the following procedures were carried out:                pathogenic species and its proportion compared to
    first, on each implant site, the following biometric pa-      the total bacterial load found in the analyzed sites. In
    rameters were evaluated: probing depth (PD), bleed-           all the three groups, no significant differences in pro-
    ing on probing (BoP), modified plaque index (mPI),            portions of bacterial species were observed between
    the presence of keratinized tissue (KT).                      dental and implant sites.

    Annali di Stomatologia 2015; VI (1): 21-28                                                                           23
                                                         ©
                                             Table 1. Biometric parameters and microbiological profile of all the patients included in the study.




  24
                                                                        C
                                             name smoking sex age biotype position mes dist cent            ml dl l  bop bopl mPI keratinized previous           Lab.-No.   A.a.       F.n.       P.g.       P.i.      T.d.        T.f.       Total
                                                  habit                            pd  pd pd                pd pd pd v            tissue      period                                                                                          bacterial
                                                                                                                                              disease                                                                                         load
                                             BA     0         m    59   T        #20      3     3     3     2    2   2   1    0     0     1           N          1084749    <100       <100       <100       <100      <100        <100       3,4E+06
                                                                                 IC
                                                                                                                                                                                                                                                          A. Quaranta et al.




                                             BA     0         m    59   T        #21      2     2     2     2    2   3   0    0     0     1           N          1084750    <100       5,0E+02    <100       <100      <100        <250       1,7E+07
                                             AG     0         f    70   T        #25      2     2     2     2    2   2   1    0     0     1           y          1084751    <100       <100       <100       <100      1,5E+04     4,6E+04    2,4E+07
                                             AG     0         f    70   T        #23      3     4     3     3    4   3   0    0     0     1           y          1084752    <100       <250       <100       <100      2,2E+04     1,2E+04    1,1E+06
                                             GM     1         m    48   T        #24      2     2     1     2    2   1   0    0     0     1           y          1084753    <100       <250       3,4E+03    <250      <250        1,5E+03    5,0E+05
                                             GM     1         m    48   T        #12      3     3     2     3    3   2   0    1     1     1           y          1084754    <100       2,5E+03    2,7E+04    <100      2,8E+03     2,9E+03    3,0E+06
                                             FR     0         f    45   T        #29      3     3     2     3    3   2   0    0     1     1           N          1084755    <100       <100       <100       <100      <100        <100       4,5E+07
                                             FR     0         f    45   T        #14      3     3     2     3    3   2   0    0     0     1           N          1084756    <100       <100       <100       <100      <100        5,0E+02    2,0E+06
                                                                                                    Ed
                                             FR     0         m    45   T        #10      3     2     3     2    2   2   0    0     0     1           N          1084757    <100       <100       <100       <100      <100        <100       1,6E+06
                                             MV     0         m    66   T        #10      2     4     4     4    2   2   2    1     1     1           Y          1084758    <100       3,8E+04    2,9E+06    3,2E+05   8,2E+06     1,6E+06    7,6E+07
                                             MV     0         m    66   T        #9       3     3     2     3    3   2   1    1     1     1           Y          1084759    <100       <100       1,8E+03    <100      2,6E+03     9,4E+02    1,7E+06
                                                                                                                     iz
                                             FG     1         m    50   t        #13      3     3     2     3    3   2   0    0     0     1           y          1084760    <100       <100       <100       <100      <100        <100       6,1E+04
                                             FG     1         m    50   t        #12      2     2     2     2    2   2   0    0     0     1           y          1084761    <100       1,2E+03    <100       <100      <100        <100       5,6E+05
                                             T      1         f    50   t        #2       4     3     3     4    4   3   0
                                                                                                                             io
                                                                                                                              0     1     0           y          1084762    <100       <100       <100       <100      <100        <250       2,5E+07
                                             T      1         f    50   t        #3       3     3     2     3    3   2   0    0     0     0           y          1084763    <100       <100       <100       <100      <100        3,6E+02    2,0E+06
                                             Y      0         f    27   t        #3       3     3     2     3    3   2   0    0     0     0           y          1084764    <100       <100       <100       <100      <100        <100       1,3E+06
                                             Y      0         f    27   t        #5       3     3     3     3    3   2   0    0     0     0           y          1084765    <100       <100       <100       <100      <100        <100       2,0E+06
                                             MS     0         m    37   T        #30      3     3     2     3    3   2   0    0     0     0           N          1084766    <100       2,2E+05    <100       <100      <100        8,1E+04    1,3E+07
                                                                                                                                        ni
                                             MS     0         m    37   T        #18      2     2     3     2    2   3   0    0     0     0           N          1084767    <100       3,7E+03    <100       <100      <100        <250       1,7E+06
                                             CG     0         m    66   T        #30      1     1                                         0           y          1084768    <100       <100       4,0E+03    2,3E+03   <100        4,6E+02    6,6E+06
                                             CG     0         m    66   T        #28      3     3     2     4    3   2   0    0     0     1           y          1084769    <100       4,0E+03    4,0E+02    <100      <250        <100       4,3E+06
                                                                                                                                                       In
                                             AG     1         m    66   T        #20      4     7     3     4    7   3   1    1     0     1           y          1084770    <100       <100       3,3E+04    1,2E+04   3,7E+03     2,0E+03    9,4E+05
                                             AG     1         m    66   T        #21      3     3     2     3    3   2   0    0     1     0           y          1084771    <100       <100       4,3E+02    2,9E+02   <250        <100       3,0E+06
                                             LGB    1         m    68   T        #3       3     3     2     4    4   2   0    0     1     0           y
                                                                                                                                                          t      1084772    <100       2,3E+04    3,8E+04    1,4E+04   5,4E+04     6,0E+03    3,9E+07
                                             LGB    1         m    68   T        #6       3     3     2     3    3   2   0    0     1     0           y          1084773    <100       6,2E+04    <100       <100      <100        <100       2,6E+06
                                             VC     1         f    75   T        #12      3     3     2     3    3   2   0    0     1     0           y          1084774    1,3E+03    <100       1,6E+04    <100      <100        3,1E+03    1,0E+05
                                             VC     1         f    75   T        #11      4     4     3     2    3   2   3    2     3     0           y          1084775    3,7E+04    <100       9,1E+03    <100      2,0E+03     8,6E+04    5,6E+06
                                                                                                                                                                      er
                                             CR     0         m    53   T        #5       3     3     2     4    4   3   0    0     0     0           y          1084776    <100       <100       7,0E+03    <100      <100        2,8E+03    2,5E+06
                                             CR     0         m    53   T        #28      4     4     3     3    3   2   0    0     0     0           y          1084777    <100       <100       <100       <100      <100        <100       1,1E+06
                                             CC     0         f    21   T        #19      3     2     3     3    2   3   0    0     0     1           N          2014028    <100       1,8E+03    4,8E+04    3,1E+03   1,2E+04     9,2E+03    1,7E+06
                                                                                                                                                                                   na
                                             CC     0         f    21   T        #8       3     3     3     3    2   3   0    0     0     1           N          2014029    <100       <100       <100       <100      <100        <100       5,9E+04
                                             0=NO (Under the columns “smoking habits” and “keratinized tissue”); 1=YES (Under the columns “smoking habits” and “keratinized tissue”); Y=yes; NA=not assigned; f=female; t=thin; m=male; T=thick; N=no
                                             A.a., T.f., P.g., P.i., T.d., F.n.: bacterial species as described in the section “Materials and methods”
                                             Note: Implant positions are reported according to the universal numbering system (also known as the “american dental numbering system”)
                                                                                                                                                                                                  zi



Annali di Stomatologia 2015; VI (1): 21-28
                                                                                                                                                                                                            on
                                                                                                                                                                                                               al
                                                                                                                                                                                                                 i
    The impact of smoking and previous periodontal disease on peri-implant microbiota and health: a retrospective study up
    to 7-year follow-up

    Intra-examiner reproducibility regarding the collection           GROUP 2) Non-smoker patients previously affect-
    of clinical parameters was good with a linear weight-             ed by chronic periodontal disease (Tab. 3)
    ed kappa (κ) score of 0.85.
                                                                      Seven implant sites in four patients showed signifi-
                                                                      cant counts of all the pathogenic species. The implant




                                                                                                                   i
    GROUP 1) Non-smoker patients with healthy peri-                   site with the most severe biometric parameters was




                                                                                                                 al
    odontal tissues; (Tab. 2)                                         also characterized by the highest total bacterial load
                                                                      and number of single pathogenic bacterial counts. In
    Significant counts of isolated red complex species                only 1 patient no significant presence of pathogenic




                                                                                                              on
    were observed in all the patients (Fig.1).                        species was observed around an implant site.
    However, this observation was not related to patho-               Bleeding on probing was positive and profuse in 3 im-
    logical PD values or peri-implant inflammation. Only 1            plants in 2 different patients. In both the patients, this
    patient showed BOP+, but this clinical observation                clinical observation corresponded to a microbiological
    did not correspond to a high total bacterial load nor             profile with an extremely high total bacterial load. mPI




                                                                                                   zi
    significant single pathogenic counts. mPI values were             values were considered relatively satisfactory in all
    considered satisfactory in all the subjects and ranged            the subjects and ranged from 0 to 2. The presence of
    from 0 to 1. The presence of keratinized tissue did               keratinized tissue was not related to healthier biomet-




                                                                                       na
    not correspond with healthier biometric parameters.               ric parameters (Fig. 2).

    Table 2. Clinical parameters and microbiological profile in non-smoker, periodontally healthy patients.




                                                                            er
                                        NO SMOKERS-NO PREVIOUS PERIODONTAL DESEASE
    PZ     Implant BOP        PD    mPI K        Lab.-No.    A.a.    F.n.       P.g.      P.i.      T.d.      T.f.    Total
           position                     tissue                                                                        bacterial
                                                                                                                      load
    B.A.   #20        vest                +      1084749

                                                               t
                                                             <100    <100    <100         <100      <100      <100    3,4E+06
           #21                            +      1084750
                                                            In
                                                             <100    5,0E+02 <100         <100      <100      <250    1,7E+07
    F.R.   #19                      +     +      1084755     <100    <100       <100      <100      <100      <100    4,5E+07
           #14                            +      1084756     <100    <100       <100      <100      <100      5,0E+02 2,0E+06
           #10                            +      1084757     <100    <100       <100      <100      <100      <100    1,6E+06
                                                 ni
    M.S.   #18                            -      1084766     <100    2,2E+05 <100         <100      <100      8,1E+04 1,3E+07
           #30                            -      1084767     <100    3,7E+03 <100         <100      <100      <250    1,7E+06
    C.C.   #19                            +      2014028     <100    1,8E+03 4,8E+04 3,1E+03 1,2E+04 9,2E+03 1,7E+06
                                     io

           #8                             +      2014029     <100    <100    <100    <100    <100    <100    5,9E+04
    vest= buccal side; +=present; - =absent
    A.a., T.f., P.g., P.i., T.d., F.n.: bacterial species as described in the section “Materials and methods”
                             iz



    Note: Implant positions are reported according to the universal numbering system (also known as the “american dental num-
    bering system”)
           Ed
IC
C
©




    Figure 1. Peri-apical x-rays of a non-smoker, periodontally healthy patient over a period of 7 years.


    Annali di Stomatologia 2015; VI (1): 21-28                                                                               25
    A. Quaranta et al.


    Table 3. Clinical parameters and microbiological profile in non-smoker patients with previous periodontal disease.

    NO SMOKERS-PREVIOUS PERIODONTAL DESEASE
    PZ     Implant BOP       PD   mPI k          Lab.-No.    A.a.    F.n.       P.g.       P.i.        T.d.     T.f.       Total
           position                   tissue                                                                               bacterial




                                                                                                                   i
                                                                                                                           load




                                                                                                                 al
    A.G.   #25       +                  +        1084751     <100    <100       <100       <100        1,5E+04 4,6E+04 2,4E+07
           #23                          +        1084752     <100    <250       <100       <100        2,2E+04 1,2E+04 1,1E+06




                                                                                                              on
    M.V    #10       vest-   +    +     +        1084758     <100    3,8E+04 2,9E+06 3,2E+05 8,2E+06 1,6E+06 7,6E+07
                     ling
           #9        vest-              +        1084759     <100    <100       1,8E+03 <100           2,6E+03 9,4E+02 1,7E+06
                     ling
    Y      #3                           -        1084764     <100    <100       <100       <100        <100     <100       1,3E+06




                                                                                                   zi
           #5                           -        1084765     <100    <100       <100       <100        <100     <100       2,0E+06
    C.G.   #30                          -        1084768     <100    <100    4,0E+03 2,3E+03 <100               4,6E+02 6,6E+06




                                                                                       na
           #28                          +        1084769     <100    4,0E+03 4,0E+02 <100    <250               <100    4,3E+06
    C.R.   #5                           -        1084776     <100    <100       7,0E+03 <100           <100     2,8E+03 2,5E+06
           #28                          -        1084777     <100    <100       <100    <100           <100     <100    1,1E+06
    vest=buccal side; ling=lingual side; +=positive; - =negative




                                                                            er
    A.a., T.f., P.g., P.i., T.d., F.n.: bacterial species as described in the section “Materials and methods”
    Note: Implant positions are reported according to the universal numbering system (also known as the “american dental num-
    bering system”)




                                                               t
                                                            In
                                             ni
                                   io
                             iz
           Ed
IC
C




    Figure 2. Peri-apical x-rays of asmoker, periodontally healthy patient over a period of 6 years.



    GROUP 3) Smoker patients previously affected by                   Two implant sites in two patients were characterized
                                                                      by high mPI values (3) and two additional implant
©




    chronic periodontitis (Tab. 4)
                                                                      sites in two subjects showed profuse bleeding on
    The microbiological analysis of peri-implant sites                probing. The implant site with the most severe bio-
    showed significant pathogenic counts in all the patients          metric parameters was characterized by a microbial
    (Tab. 4). T.f. morphotype was the bacterial specie with           profile with the highest total and pathogenic bacterial
    the greatest counts in most of thesites. Four implant             counts. The presence of keratinized tissue was not
    sites in four different patients showed deep PD values.           related to healthier biometric parameters (Fig. 3).

    26                                                                                      Annali di Stomatologia 2015; VI (1): 21-28
    The impact of smoking and previous periodontal disease on peri-implant microbiota and health: a retrospective study up
    to 7-year follow-up

    Table 4. Clinical parameters and microbiological profile in smoker patients with previous periodontal disease.

    SMOKERS-PREVIOUS PERIODONTAL DISEASE
    PZ     Implant BOP        PPD mPI K      Lab.-No. A.a.           F.n.       P.g.       P.i.      T.d.       T.f.    Total
           position                   tissue                                                                            bacterial




                                                                                                                  i
                                                                                                                        load




                                                                                                                al
    G.M. #24                              +      1084753 <100        <250    3,4E+03 <250            <250    1,5E+03 5,0E+05
         #12          ling                +      1084754 <100        2,5E+03 2,7E+04 <100            2,8E+03 2,9E+03 3,0E+06




                                                                                                             on
    F.G.   #13                            +      1084760 <100        <100    <100          <100      <100       <100    6,1E+04
           #12                            +      1084761 <100        1,2E+03 <100          <100      <100       <100    5,6E+05
    T.M.   #2                 +     +     -      1084762 <100        <100       <100       <100      <100       <250    2,5E+07
           #3                             -      1084763 <100        <100       <100       <100      <100       3,6E+02 2,0E+06




                                                                                                    zi
    A.G    #21        vest-   +           +      1084770 <100        <100       3,3E+04 1,2E+04 3,7E+03 2,0E+03 9,4E+05
                      ling
           #22                      +     -      1084771 <100        <100       4,3E+02 2,9E+02 <250            <100    3,0E+06




                                                                                       na
    V.C.   #5                             -      1084774 1,3E+03 <100           1,6E+04 <100         <100    3,1E+03 1,0E+05
           #28                +           -      1084775 3,7E+04 <100           9,1E+03 <100         2,0E+03 8,6E+04 5,6E+06
    L.G.B. #3                 +           -      1084772 <100        2,3E+04 3,8E+04 1,4E+04 5,4E+04 6,0E+03 3,9E+07
           #6                             -      1084773 <100        6,2E+04 <100    <100    <100    <100    2,6E+06




                                                                            er
    vest=buccal side; ling=lingual side; +=positive; - =negative
    A.a., T.f., P.g., P.i., T.d., F.n.: bacterial species as described in the section “Materials and methods”
    Note: Implant positions are reported according to the universal numbering system (also known as the “american dental num-
    bering system”)



                                                              t
                                                           In
                                                 ni
                                     io
                              iz
           Ed
IC
C




    Figure 3. Peri-apical x-rays of a smoker patient previously affected by periodontitis over a period of 7 years.


    Discussion                                                         scientific evidence about the association between pe-
©




                                                                       riodontitis and peri-implantitis (8). It is also possible
    It is well known that the peri-implant tissue response             to state that smoke, local and systemic conditions
    to the bacterial challenge may follow patterns similar             and the presence of subgingival, pathogenic bacteria,
    to that of the periodontal tissues in a susceptible                play an important role in the occurrence of implant
    host, although it has not yet been clarified whether or            complications, although the biological impact of these
    not a host susceptible for periodontitis will also be              factors on the long-term prognosis of oral implant is
    susceptible for peri-implantitis. Nowadays there is                still to be defined. In the present study, the absence

    Annali di Stomatologia 2015; VI (1): 21-28                                                                                27
    A. Quaranta et al.


    of deep PDs around implants in non-smoker patients                          nization of “pristine” pokets. J Dent Research. 2005b;
    with healthy periodontal tissues, seems to validate                         84:340-344.
    the positive role that the absence of modifying factors                5.   Quyrinen M, Listgarten MA. Distribution of bacterial mor-
                                                                                photypes around natural teeth and titanium implants ad mod-
    plays in peri-implant health. The results of the pre-
                                                                                um Branemark. Clin Oral Implants Res. 1990;1:8-12.
    sent study shows that previous periodontal disease




                                                                                                                           i
                                                                           6.   Seymour GJ, Gemmell E, Lenz LJ, Henry P, Bower R,Ya-
    has a role similar to smoking as risk factor for implant




                                                                                                                         al
                                                                                mazaki K. Immunohistologic analysis of the inflammatory in-
    complications. The presence of both these factors do                        filtrates associated with osseointegrated implants. Int J Oral
    not make peri-implant clinical conditions worse. Un-                        Maxillofac Implants. 1989;4:191-8.
    fortunately, no data about the number of cigarettes                    7.   Liljenberg B, Gualini F, Berglundh T, Tonetti M, Lindhe J.




                                                                                                                      on
    smoked per day were collected and this may be a                             Composition of plaque-associated lesions in the gingiva and
    confounding factor.                                                         the peri-implant mucosa in partially edentulous subjects. Clin
    The total bacterial load was not always related to the                      Periodontol. 1997;24:119-23.
    presence of significant pathogenic counts.                             8.   Karoussis IK, Salvi GE, Heitz-Mayfield LJ. Long-term implant
                                                                                prognosis in patients with and without a history of chronic pe-
    T.f. was the bacterial specie with the highest number




                                                                                                           zi
                                                                                riodontitis: a 10-year prospective cohort study of the ITI Den-
    of counts in each group but it was not associated to
                                                                                tal Implant System. Clin Oral Implants Res. 2003;14:329-39.
    significant counts of the other assessed bacteria.                     9.   Karoussis IK, Müller S, Salvi GE, Heitz-Mayfield LJ, Bräg-
    On the other hand, the inverse assumption resulted




                                                                                           na
                                                                                ger U, Lang NP. Association between periodontal and peri-
    consistently valid: a greater count of pathological                         implant conditions: a 10-year prospective study. Clin Oral Im-
    species was found in patients with a greater total                          plants Res. 2004;15:1-7.
    bacterial load.                                                       10.   Karoussis IK, Kotsovilis S, Fourmousis. A comprehensive and
    In general, the total bacterial load was not related to                     critical review of dental implant prognosis in periodontally com-
                                                                                promised partially edentulous patients I. Clin Oral Implants




                                                                            er
    pathological biometric parameters nor presence or
    absence of keratinized tissue.                                              Res. 2007;18:669-79.
                                                                          11.   Berglundh T, Persson L, Klinge B. A systematic review of the
    However, the implant site with the worst biometric pa-
                                                                                incidence of biological and technical complications in implant
    rameters was characterized by the greatest total bac-                       dentistry reported in prospective longitudinal studies of at least
    terial load and the larger number of single pathogenic


                                                                   t            5 years. J Clin Periodontol. 2002;29:197-212.
    species counts.
    Finally, in the present study significant pathogenic
                                                                In        12.   Lang NP, Pjetursson BE, Tan K, Brägger U , Egger M, M
                                                                                Zwahlen M. A systematic review of the survival and compli-
    counts were observed in both smoker and non smok-                           cation rates of fixed partial dentures (FPDs) after an obser-
    er subjects previously affected by periodontitis.                           vation period of at least 5 years. II. Combined tooth-implant-
                                                                                supported FPDs. Clin Oral Implants Res. 2004;15:643-53.
                                                 ni
                                                                          13.   Pjetursson BE, Tan K, Lang NP, Brägger U, Egger M,
                                                                                Zwahlen M. A systematic review of the survival and com-
    Conclusions
                                                                                plication rates of fixed partial dentures (FPDs) after an ob-
                                                                                servation period of at least 5 years. M. Clin Oral Implants Res.
                                      io

    Within the limits of the present study it is possible to                    2004;15:625-42.
    state that the absence of smoking habit and previ-                    14.   Rinke S, Ohl S, Ziebolz D, Lange K, Eikholz P. Prevalence
    ous periodontal disease positively influences the                           of peri-implant disease in partially edentulous patients: A prac-
    medium to long-term microbiological profile and
                            iz


                                                                                tice-based cross-sectional study. Clin Oral Implants Res.
    peri-implant health in partial edentulous patients.                         2011;22:826-833.
    Further studies on a larger number of patients and                    15.   Heitz-Mayfield LJ. Peri-implant diseases: Diagnosis and risk
    paying special attention to the number of cigarettes                        indicators. J Clin Periodontol. 2008;35(suppl 8):292-304.
           Ed




    smoked per day would be necessary in order to con-                    16.   Strietzel FP, Reichart PA, Kale A, Kulkarni M, Wegner B,
                                                                                Kuchler I. Smoking interferes with the prognosis of dental im-
    firm our conclusions.
                                                                                plant treatment: A systematic review and meta-analysis. J
                                                                                Clin Periodontol. 2007;34:523-544.
                                                                          17.   Bain CA, Moy PK. The association between the failure of den-
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IC




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©




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    28                                                                                             Annali di Stomatologia 2015; VI (1): 21-28
