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    Smoking interferes with theprognosis of dental implanttreatment: a systematic reviewand meta-analysis

    Strietzel FP, Reichart PA, Kale A, Kulkarni M, Wegner B, Kuchler I. Smoking interferes

    with the prognosis of dental implant treatment: a systematic review and meta-analysis.J Clin Periodontol 2007; 34: 523544. doi: 10.1111/j.1600-051X.2007.01083.x.

    Abstract

    Aim: This systematic literature review was performed to investigate if smokinginterferes with the prognosis of implants with and without accompanyingaugmentation procedures compared with non-smokers.

    Methods: A systematic electronic and handsearch (articles published between 1989and 2005; English and German language; search terms dental or oral implantsand smoking; dental or oral implants and tobacco) was performed to identifypublications providing numbers of failed implants, related to the numbers of smokersand non-smokers for meta-analysis. Publications providing statistically examined dataof implant failures or biologic complications among smokers compared with non-smokers were included for systematic review.

    Results: Of 139 publications identified, 29 were considered for meta-analysis and 35for systematic review. Meta-analysis revealed a significantly enhanced risk for implantfailure among smokers [implant-related odds ratio (OR) 2.25, confidence interval(CI95%) 1.962.59; patient-related OR 2.64; CI95% 1.704.09] compared with non-smokers, and for smokers receiving implants with accompanying augmentationprocedures (OR 3.61; CI95% 2.265.77, implant related). The systematic reviewindicated significantly enhanced risks of biologic complications among smokers. Fivestudies revealed no significant impact of smoking on prognosis of implants withparticle-blasted, acid-etched or anodic oxidized surfaces.

    Conclusion: Smoking is a significant risk factor for dental implant therapy andaugmentation procedures accompanying implantations.

    Key words: dental implants; meta-analysis;odds ratio; smoking; success rate; survival rate

    Accepted for publication 18 February 2007

    Conflict of interest and source offunding statement

    The authors declare that they have noconflict of interest.None of the authors received any benefit ofany kind from commercial or official par-ties related directly or indirectly to thesubject matter of this article. No grant orfunding from any party was received toprepare or perform this work.

    Frank Peter Strietzel1

    , Peter A.Reichart1, Abhijit Kale2, Milind

    Kulkarni2, Brigitte Wegner3 and

    Ingeborg Kuchler3

    1Department of Oral Surgery and Dental

    Radiology, Campus Virchow Clinic, Centre

    for Dental Medicine, Charite Medical

    University Berlin, Berlin, Germany ; 2Clinic

    of General and Restorative Dentistry and

    Dental Implantology, Maharashtra Medical

    Foundations Joshi Hospital, Pune, India;3Campus ChariteMitte, Institute for Biometry

    and Clinical Epidemiology, Charite Medical

    University Berlin, Berlin, Germany

    Smoking was shown to be a primary risk

    factor for general health, responsible formany serious diseases, as for 90% of alllung cancers, 70% of chronic lung dis-

    eases, 80% of myocardial infarctions

    before the age of 50, and 30% of chronicischaemic heart diseases and strokes(Fielding 1985, La Veccia et al. 1991,Peto et al. 1996). Currently, there are anestimated 1.3 billion smokers world-wide, and 4.9 million people die fromtobacco smoking-related diseases peryear (WHO 2005).

    Besides the prominent role of healthprofessionals to play in tobacco controland smoking cessation generally, certainaspects concerning current dental ther-apy should be considered in smokers forthorough patient information before oral

    surgical procedures and implant therapy

    planning. The increased risk of woundhealing complications (Meechan et al.1988, Miller 1988, Jones & Triplett1992, Sands et al. 1993) as well as therisk of peri-implant bone loss andincreased implant failure rates (Haaset al. 1996, Lindquist et al. 1996, Lem-ons et al. 1997) have to be emphasized.Impaired wound healing has to beexpected due to less collagen production(Jorgensen et al. 1998), reduced periph-eral blood circulation (Lehr 2000) andcompromised function of polymorpho-nuclear leucocytes and macrophages

    J Clin Periodontol 2007; 34: 523544 doi: 10.1111/j.1600-051X.2007.01083.x

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    (Kenney et al. 1977, MacFarlane et al.1992). Moreover, smoking was indi-cated a significant subject-based riskfactor for periodontitis by recently pub-lished literature reviews (Palmer et al.2005, Ramseier 2005). Although notcompletely investigated, the known

    mechanisms of action of smoking onperiodontitis were found to be the long-term chronic effect due to impairing thevasculature of periodontal tissues andaffection of multiple functions of neu-trophils and inflammatory responseas well as impairment of fibroblasts(Palmer et al. 2005).

    Therefore, identification of the smok-ing patient is required. Patient question-naires considering general health issues,but also asking for smoking habits andalcohol consumption, seem to be neces-sary, though not generally used as a

    matter of routine yet (Reichart et al.2000).Thorough patient information about

    the planned treatment course and theexpected outcomes, but also about risksand risk-associated factors is necessaryto support the patients decisionmaking before implant therapy (Striet-zel 2003). Therefore, a systematic ana-lysis of the literature focusing onexpected interactions between implantprognosis and smoking seemed to benecessary to provide quantitative factsincluding the likelihood of smoking-

    associated risks for implant prognosisand outcomes after augmentation pro-cedures accompanying implant surgery,to support a risk analysis before therapy,and to substantiate the patient informa-tion.

    This meta-analysis and systematicreview focused on the question, if thereis a significantly enhanced risk ofimplant failures in smokers comparedwith non-smokers. The influence ofsmoking on implants inserted withaccompanying augmentation procedureswas additionally investigated.

    Material and Methods

    Search strategy

    A systematic literature search in electro-nic databases was conducted, using thefollowing search term combinations:dental implants AND smoking,dental implants AND tobacco,oral implants AND smoking andoral implants AND tobacco.

    Furthermore, a manual search wasapplied to three German-language

    peer-reviewed dental journals, focusingon articles related to the effect ofsmoking on dental implant treatmentoutcomes.

    Inclusion criteria

    Literature search was performed toidentify meta-analyses and systematicreviews as well as randomized-con-trolled clinical trials, prospective orretrospective clinical studies, cohort stu-dies or casecontrol studies.

    Publications were included for meta-analysis or systematic review, if theywere published between January 1989and December 2005 in English languageand listed in electronic databases Med-line/Pubmed or Embase, or were pub-lished in German language in Deutsche

    Zahnarztliche Zeitschrift (January

    1968December 2005), Zeitschrift furZahnarztliche Implantologie (January1998December 2005) and Implantolo-gie (January 1996December 2005).

    Publications were included for meta-analysis, if implant survival rates or thenumber of failed implants were reportedon an implant- or patient-related basisand the number of smoking as well asnon-smoking patients were publishedand could be related to the number offailed and remaining implants, respec-tively.

    Moreover, publications were

    included for systematic review althoughnot meeting the inclusion criteria formeta-analysis, if odds ratios (OR), riskratios (RR) or hazard ratios (HR) forimplant failures among smokers werereported, or reports on biologic compli-cations and findings known to influencethe success of implant-prosthetic ther-apy in smokers compared with non-smokers were given, and if the resultswere statistically analysed consideringthe effects of smoking on treatmentcourse or outcome.

    As definition of smokers were differ-

    ent in several studies regarding quanti-ties of smoked cigarettes per day andtherefore were accordingly categorizeddifferently, any patient who smoked wasconsidered a smoker, following the defi-nition given by Wallace (2000).

    Selection of studies and data extraction

    Titles and abstracts of the publicationsidentified by electronic databases andhandsearch using the search terms men-tioned above were screened initially bytwo independent reviewers (F. P. S. and

    A. K. or M. K.). Publications wereincluded for full text evaluation if thestudy design and content of the abstractsmet the inclusion criteria and matchedthe focused question. Agreementbetween the reviewers was determinedperforming k-statistic. Disagreements

    were resolved by evaluation of the fulltexts and discussion. Final authority forselection disagreements rested withF. P. S.

    Full text assessment and data extrac-tion were performed by the reviewerswithout any disagreements. The processof identification of the included studiesfrom the initial yield is described inFig. 1.

    A categorization considering theduration of the observation periodsreported in the studies identified formeta-analysis was performed addition-

    ally (group 1: observation period 41year; group 2:41 and45 years; group3: 45 years).

    Furthermore, studies involvingimplant-prosthetic rehabilitation afteraugmentation procedures to enhancebone quantity at the implant site [sinusfloor elevation and augmentation(SFEA) and/or lateral alveolar ridgeaugmentation by guided bone regenera-tion (GBR)] providing survival data ofimplants were considered for meta-analysis to evaluate the risk of smokingconcerning augmentation procedures.

    The frequency and percentage distri-bution of smokers and non-smokersregarding the frequency of implant suc-cess or failure were extracted from thestudies included for meta-analysis.Furthermore, the distributions of maleand female patients, and of implants inthe maxilla and mandible with specialrespect to the groups regarding differentobservation periods were considered.

    To rule out the cumulation of indivi-dual risks, studies publishing patient-related data were considered separatelyfrom those reporting implant-related

    data for meta-analysis.Considering studies publishing

    implant-related data, implants were con-sidered failures if they failed to osseoin-tegrate (Balshi & Wolfinger 1999,Grunder et al. 1999, Keller et al. 1999,Kronstrom et al. 2001, Mayfield et al.2001, Kumar et al. 2002, van Steen-berghe et al. 2002), were lost orremoved for any reason (Bain & Moy1993, De Bruyn & Collaert 1994, Bain1996, Minsk & Polson 1998, De Bruynet al. 1999, Jones et al. 1999, Berge &Grnningsaeter 2000, Lambert et al.

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    2000, Olson et al. 2000a,b, Schwartz-Arad et al. 2000, Geurs et al. 2001,Widmark et al. 2001, Ortorp & Jemt2002, Penarrocha et al. 2002, Schwartz-Arad et al. 2002, Beschnidt et al. 2003,van Steenberghe et al. 2004, Moheng &Feryn 2005) or exceeded more than 50%bone loss (Bain & Moy 1993, Bain1996) or more than 4 mm of verticalbone defect (Berge & Grnningsaeter2000), if they failed one or more of the

    criteria proposed by Smith & Zarb(1989) (Kan et al. 2002), revealed mobi-lity (without having removed implantprostheses for individual implant mobi-lity test), persistent pain, peri-implantradiolucency and/or infections attributa-ble to the implant (Gorman et al. 1994,Wallace 2000), or if they showed biolo-gic complications (peri-implantitis)(Karoussis et al. 2003).

    Considering publications providingwith patient-related data, the treatmentof one patient was accounted as failureif one or more implants were considered

    a failure due to the above-mentionedcriteria.

    Excluded studies

    Publications were excluded if they didnot meet the inclusion criteria (i.e. ifthey were considered case reports, ani-mal or in vitro experiments, educationalstatements, expert opinions), if they didnot provide implant- or patient-related

    data on failures or complications inimplant treatment related to the smokinghabit, or if they did not contain materialmatching the focused question.Excluded studies and the reasons forexclusion are listed in the reference list.

    Statistical analysis

    A funnel plot of the log odds ratiosversus their SE was calculated to pre-vent a selected subset of studies, whichis widely accepted to detect potentialpublication bias when the actual treat-

    ment effects of an intervention or theoutcomes after exposure to certain para-meters are homogeneous (Light &Pillemer 1984). Assuming that theunderlying true exposure effect in eachstudy is the same, a general non-para-metric fixed-effects selection model was

    applied to the entire collection of theselected studies to estimate the extentand size of undetected reports (Hedges1992, Blettner & Schlattmann 2005).

    Furthermore, a mixed random-effectsmodel was applied since deviations ofthe estimated effect sizes may also beexplained by a random error. Therefore,a mixed model for calculation of hetero-geneity was used to detect heterogeneitybetween the studies selected (Blettner &Schlattmann 2005).

    For dichotomous parameters (smo-kers and non-smokers) and outcomes

    (lost implants and successful implants),the estimate of the effect of the para-meter smoking was expressed as oddsratio (OR) together with the 95% con-fidence interval (CI95%) after perform-ing univariate analysis, utilizing the dataobtained from the studies providing withinformation about failed and successfulimplants related to smokers and non-smokers. According to the patient- orimplant-related data basis, the synthe-sized ORs were calculated separately.

    As calculation of an OR is undefinedif one value of the cells of the cross table

    is equal to zero, for the studies con-cerned, 0.5 was added to the values ofall cells as suggested by Gart & Zweifel(1967) and Fleiss (1981).

    As sample sizes of the included stu-dies were different, the weighed meanvalues of the distributions of frequenciesand SD regarding smokers and non-smokers, male and female patients andimplants in the maxilla and mandiblewere calculated and compared.

    Statistical calculations were per-formed using SPSS software version12.0 (SPSS Inc., Chicago, IL, USA)

    and SAS software version 8.2 (SASInstitute Inc., Cary, NC, USA).

    Results

    Of the entire yield of 139 publicationsidentified with electronic and hand-search, 75 were finally excluded frommeta-analysis and systematic reviewafter full text assessment.

    Information on failures as well assuccess proportions of implants amongsmokers and non-smokers on patient-related and/or implant-related basis

    Handsearch

    Result: 1 abstract

    Final decision:

    29 publications included for meta-analysis35 publications included for systematic review

    Independent selection of abstracts:

    Reviewer 1: 59 abstracts included Reviewer 2: 58 abstracts included80 abstracts excluded 81 abstracts excluded

    agreement with 47 included and 70 excluded abstracts

    score = 0.712

    Full text assessment and discussion:

    Reviewer 1: 60 publications included Reviewer 2: 59 publications included79 publications excluded 80 publications excluded

    agreement with 57 included and 78 excluded publications

    score = 0.985

    Search with

    electronic databases

    Result: 138 abstracts

    Fig.1 . Search strategy and results of identification and inclusion of publications considered

    for meta-analysis and systematic review. The k-score expresses the agreement between thereviewers.

    Smoking interferes with the prognosis of dental implant treatment 525

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    were retrieved for meta-analysis from29 included studies. Of these, 15 wereprospective studies (three reportingpatient-related data, nine reportingimplant-related data and three reportingboth patient- and implant-related data)and 14 were retrospective studies (threereporting patient-related data, ninereporting implant-related data and tworeporting both patient- and implant-related data).

    Furthermore, 35 studies wereincluded for systematic review, report-ing on implant failures or biologiccomplications or findings known tonegatively influence the success ofimplant-prosthetic therapy and compli-cations in connection with augmentationprocedures, related to smoking habit. Ofthese 35 studies, one was a randomizedcontrolled trial, 11 were prospective and21 retrospective studies. Additionally,one meta-analysis and one systematicreview were included.

    The risk of implant failures in smokers

    compared with non-smokers: Results

    obtained from meta-analysis

    First, the existence of publication biashad to be investigated. Figure 2a and bshow the funnel plots of the ORs by theinverse of the variances of each studyincluded for meta-analysis, calculatedon an implant-related as well aspatient-related basis. Assuming thateffects of smoking are homogeneous,no asymmetry indicating missing trialswas detected. Considering the implant-

    related data obtained from the studiesincluded for meta-analysis, the slope ofthe regression line was 0.014 (CI95% 0.0480.020, p50.412), and forpatient-related data, the slope of theregression line was 0.084 (CI95% 0.5290.361, p50.682), revealingno significant differences of the slopeof regression lines from zero. Therefore,no publication bias was detected, andthe sample of the selected studies was

    considered adequate for meta-analysis.The overview of the characteristics ofstudies included for meta-analysis isgiven in Table 1. The weighed meanvalues of frequencies distributions ofsmokers and non-smokers, gender andimplant sites among maxilla and mand-ible of the studies considered for meta-analysis are shown in Tables 24.

    Analysis of studies providing implant-

    related data

    Implant-related data were obtained from

    18 studies. Calculations of pooled riskby applying the fixed-effects modelwithout covariates on studies providingimplant-related data showed an OR of2.25 (CI95% 1.962.59), revealing evi-dence for a significant associationbetween smoking and implant failure.The test of heterogeneity of includedstudies yielded p50.013. Because ofthe heterogeneity further calculationsusing the mixed model taking intoaccount the random effects of the stu-dies on implant-related studies revealedan OR of 2.38 (CI95% 1.932.93).

    Considering the groups of differentmean observation periods as covariates,the OR for implant failures in smokerscalculated from studies with a meanobservation period of up to 1 year(n58) was 2.83 (CI95% 2.083.85).An OR of 2.25 (CI95% 1.902.67) wascalculated from studies reporting dataregarding mean observation periodsbetween more than one up to 5 years(n513). The implant-related ORs after

    observation periods after up to 1 year aswell as between 1 and 5 years revealed asignificantly enhanced risk of implantfailures in smokers and did not differsignificantly (p50.1892). The OR ofimplant failures in smokers of threestudies with a mean observation periodof more than 5 years was 1.33 (CI95%0.842.11), which showed no signifi-cantly enhanced risk for implant failuresin smokers. Considering both groups ofobservation periods of more than 1 yearcombined, the ORs calculated with themixed fixed-effects model with the cov-

    ariate observation period were 2.83(CI95% 2.083.85) for studies with amean observation period up to 1 yearand 2.12 (CI95% 1.802.48) for a meanobservation period of more than 1 year,which were not significantly different(p50.0939).

    Two studies reporting on implantswith surfaces microstructured with acidetching and/or particle blasting (Grun-der et al. 1999, Kumar et al. 2002), asummarized OR for implant failure insmokers of 1.49 (CI95% 0.643.46) wascalculated, considering implant-related

    60.0050.0040.0030.0020.0010.000.00

    weighting factor (1/variance) weighting factor (1/variance)

    5.00

    4.00

    4.00

    3.00

    3.00

    2.00

    2.00

    1.00

    1.00

    0.00

    0.00

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    1.00

    2.00

    logo

    dds

    ra

    tio

    logo

    dds

    ra

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    8.006.004.002.000.00

    Fig.2. (a) Funnel plot of the log OR calculated for studies providing implant-related data (

    n524). (b) Funnel plot of the log OR calculatedfor studies providing patient-related data (n512).

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    Table1

    .Character

    isticsofstud

    ies

    include

    dformeta-analys

    is

    Stu

    dy

    Implantcharacterist

    ics

    Stu

    dydesign

    Smokers

    Non-s

    mokers

    Samplesizes

    Impl.successful

    Fai

    lure

    Impl

    .successful

    F

    ailure

    Group1:meanobservationperiodperiod

    41year

    Bain

    (1996)

    Mac

    hine

    dtitanium

    ,threadedn

    Prospect.

    38

    9

    166

    1

    0

    223implants

    78patients

    Balsh

    i&Wol

    finger

    (1999)

    Mac

    hine

    dtitanium

    ,threadedn

    Retrospect.

    1P

    1P

    27P

    5

    P

    227implants

    34patients

    w

    De

    Bruyn

    &Col

    laert

    (1994)

    Mac

    hine

    dtitanium

    ,threadedn

    Retrospect.

    max

    illa

    man

    dible

    7111P

    3610P

    7 5P

    0 0P

    163

    43P

    171

    45P

    3 2

    P

    1 1

    P

    244implants

    61patients

    208implants

    56patients

    Gormanetal

    .(1994)

    Notreporte

    d

    Retrospect.

    604

    64P

    4218P

    1373

    208P

    4

    7

    2

    0P

    2066implants

    310patients

    Kronstrometal

    .(2001)

    Mac

    hine

    dtitanium

    ,threadedn

    Retrospect.

    3P

    9P

    37P

    3

    1P

    80patients

    Kumaretal

    .(2002)

    Large-gr

    itblaste

    dan

    d

    acid

    -etc

    hed,threaded

    Prospect.

    261

    8

    899

    1

    5

    1183implants

    461patients

    Schwartz-A

    radetal

    .(2000)

    Mac

    hine

    dtitanium

    ,threadedan

    d

    HA-coated

    ,threadedan

    dcy

    lindric

    Retrospect.

    5

    1

    45

    5

    56implants

    z

    43patients

    van

    Steen

    berg

    heetal

    .(2002)

    Mac

    hine

    dtitan

    ium

    ,threadedn

    Prospect.

    148

    8

    1088

    1

    9

    1263implants

    399patients

    van

    Steen

    berg

    heetal

    .(2004)

    Mac

    hine

    dtitanium

    ,threadedn

    Prospect.

    immed

    iate

    load

    ing

    (Brane-m

    arknovum

    ),man

    dible

    11P

    2P

    28P

    4

    P

    150implants

    45patients

    Widmar

    ketal

    .(2001)

    Mac

    hine

    dtitanium

    ,threadedn

    Prospect.max

    illa

    ,SFEAgrafte

    d

    sitesnon-gra

    fted

    416 35

    26179

    117

    7047

    1

    4

    8 6

    198implants

    43patients

    101implants

    97implants

    Group2:meanobservation

    period41and45years

    Bain

    &Moy

    (1993)

    Mac

    hine

    dtitanium

    ,threadedn

    Prospect.

    346

    44

    1718

    8

    6

    2194implants

    540patients

    Berge

    &Grnn

    ingsaeter

    (2000)

    Ceram

    icimplants

    ,threaded

    Prospect.

    40

    21

    48

    7

    116implants

    30patients

    Beschni

    dtetal

    .(2003)

    Mac

    hine

    dtitanium

    ,threadedn

    Prospect.

    47

    4

    152

    1

    1

    214implants

    76patients

    Geursetal

    .(2001)

    Notreporte

    d

    Retrospect.max

    illa

    ,SFEA

    55

    7

    266

    1

    3

    341implants

    Grunderetal

    .(1999)

    Aci

    d-etc

    hedtitanium

    ,threaded

    Prospect.

    55

    0

    161

    3

    219implants

    74patients

    Jonesetal

    .(1999)

    Cyl

    indrica

    lHA

    -or

    TPS

    -coated

    implants

    Prospect.

    115

    12P

    117P

    212

    42P

    5 2

    P

    343implants

    63patients

    Kanetal

    .(2002)

    HA

    -coatedthreadedan

    dnon-threaded

    ,titanium

    Retrospect.max

    illa

    ,SFEA

    58

    12

    147

    1

    1

    228implants

    60patients

    Kel

    leretal

    .(1999)

    Mac

    hine

    dtitanium

    ,threadedn

    Retrospect.max

    illa

    ,SFEA

    13

    4

    106

    1

    6

    Smoking interferes with the prognosis of dental implant treatment 527

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    Table1

    .(Contd

    .)

    Stu

    dy

    Implantcharacterist

    ics

    Stu

    dydesign

    Smokers

    Non-s

    mokers

    Samplesizes

    Impl.successful

    Fai

    lure

    Impl

    .successful

    F

    ailure

    139implants

    37patients

    Lam

    bertetal

    .(2000)

    Notreported

    Retrospect.

    874

    85

    1813

    1

    15

    2887implants

    May

    fiel

    detal

    .(2001)

    TPS-coate

    dan

    dmac

    hinedtitanium

    ,

    threadedan

    dcy

    lindric

    Prospect.

    SFEA,

    GBR

    6 1P

    7 2P

    2612P

    0 0

    P

    39implants

    15patients

    Moheng

    &Feryn

    (2005)

    Cyl

    indrica

    lTPScoated

    ,an

    dpart

    icle

    -blasted

    threaded

    implants

    Prospect.

    11P

    4P

    75P

    3

    P

    93patients

    Olsonetal

    .(2000a)

    HA

    -coatedan

    dnon-c

    oate

    dtitanium

    ,

    threadedan

    dcy

    lindric

    Retrospect.max

    illa

    ,SFEA

    48

    3

    65

    0

    116implants

    36patients

    Ortorp

    &Jemt

    (2002)

    Mac

    hine

    dtitanium

    ,threadedn

    Prospect.

    33P

    10P

    78P

    5

    P

    729implants

    126patients

    Penarrochaetal

    .(2002)

    TPS-coate

    d,threaded

    Retrospect.

    27P

    7P

    70P

    1

    0P

    441implants

    114patients

    Schwartz-A

    radetal

    .(2002)

    Notreported

    Retrospect.

    175

    205

    402

    1

    77

    959implants

    261patients

    Wal

    lace

    (2000)

    Mac

    hine

    dtitanium

    ,threadedn

    Retrospect.

    60

    12

    107

    8

    187implants

    56patients

    Group

    3:meanobservat

    ion

    period45years

    De

    Bruynetal

    .(1999)

    Microtexturean

    dHA

    -coate

    d,threaded

    Prospect.max

    illa

    248P

    6 2P

    237P

    9 6

    P

    62implants

    23patients

    Karouss

    isetal

    .(2003)

    TPS-coate

    dhollowscrews

    Prospect.

    26

    2

    81

    3

    112implants

    53patients

    Minsk

    &Polson

    (1998)

    Notreported

    Retrospect.

    HRTz

    non-

    HRTz

    269

    1698

    266 6

    908

    47253

    6

    0

    2 2

    2

    1263imp

    lants

    116patients

    z

    71HRT

    379non-

    HRT

    nBranemarkfixturesorrelatedimplanttype

    s.

    wAllpatientssufferedfromdiabetesmellitus.

    zImmediateimplants.

    Biologiccomplicationsconsideredfailure(spontaneousimplantexposure,

    requiringorn

    otrequiringsurgicalinterventionorcomplete

    implantfailure).

    zFemalepatientsabovetheageof50years,

    dividedintotwogroups:patientsreceivingp

    ostmenopausalhormonereplacementtherapy

    (HRT)andpatientsnon-receivingHRT(non-H

    RT).

    P,

    patient-relateddata;HA-coated

    ,hydroxy

    apatite-coated;TPS-coated,titaniumplasmas

    pray-coated;Prospect.,

    prospectivestudies;R

    etrospect.,

    retrospectivestudies.

    SFEAimplantsinsertedinconjunctionwith

    sinusfloorelevationandaugmentation.

    GBRimplantsinsertedinconjunctionwith

    bonedefectaugmentationbyguidedbonereg

    eneration.

    528 Strietzel et al.

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    data and observation periods of 6 and 34months, respectively. After second stagesurgery and prosthetic loading, noimplant failure was noted (Grunderet al. 1999).

    Table 5 shows the ORs and CI95% ofthe studies reporting implant-related data.

    Data of studies reporting on implantsinserted with accompanying augmenta-tion procedures are not included here.

    Analysis of studies providing patient-

    related data

    Patient-related data were obtained fromten studies. Calculations of pooled riskby applying the fixed-effects modelwithout covariates on studies providingpatient-related data showed an OR of2.64 (CI95% 1.704.09). Test of hetero-geneity of included studies yielded

    p5

    0.07, revealing no heterogeneity ofincluded studies.Table 6 shows the ORs and CI95% of

    the studies reporting patient-related data.Data of studies reporting on implantsinserted with accompanying augmenta-tion procedures are not included here.

    Analysis of studies considering

    augmentation procedures

    Considering studies providing implant-related data for implant treatment withaccompanying augmentation procedures

    as covariate, the calculation using themixed effects model procedure revealedan OR of 2.15 (CI95% 1.862.49) forimplant failures in smokers withoutaugmentation procedures (n518 stu-dies), and an OR of 3.61 (CI95% 2.265.77) for implant failures in smokersundergoing augmentation procedures(n56 studies), which was significantlydifferent (p50.039).

    Although in three studies at most atendency (Geurs et al. 2001) or nosignificant associations were foundbetween smoking and enhanced fre-

    quency of implant failures in augmentedsites (Keller et al. 1999, Olson et al.2000a,b), three studies showed a sig-nificantly enhanced risk of implant lossin augmented sites in smokers, whichclearly exceeded the ORs for implantfailures calculated for smokers withoutaccompanying augmentation procedures(Mayfield et al. 2001, Widmark et al.2001, Kan et al. 2002).

    Only one study provided patient-related data allowing for calculation ofthe OR for implant failures in smokersundergoing augmentation procedures.T

    able2

    .Weighedmeanva

    lues

    (WMV)an

    dstan

    dard

    dev

    iations

    (SD)ofpercentage

    distri

    butionsofsmokers

    (S)an

    dnon-smokers

    (NS)cons

    ider

    ing

    differentobservat

    ionper

    iods(group

    1:observat

    ion

    period41year;group

    2:4

    1an

    d45years;group

    3:45years

    )an

    dstud

    iescons

    idered

    Observationperiod

    Implant-re

    late

    d

    Pat

    ient-r

    elated

    WMV(%)

    SD(%)

    WMV(%)

    SD(%)

    Group

    1

    S24

    .0

    S20

    .1

    1.22

    NS76

    .0

    0.58

    NS79

    .9

    Bain

    (1996),

    De

    Bruyn

    &Col

    laert

    (1994)

    ,

    Gormaneta

    l.(1994),Kumaretal

    .(2002),

    Schwartz-Ar

    adetal

    .(2000),van

    Steen

    berg

    heetal

    .(2002)

    ,

    Widmar

    ketal

    .(2001)

    B

    alsh

    i&Wol

    finger

    (1999)

    ,

    D

    eBruyn

    &Col

    laert

    (1994)

    ,

    G

    ormanetal

    .(1994),Kronstrometal

    .(2001),

    K

    umaretal

    .(2002)

    ,van

    Steen

    bergheetal

    .(2004),

    W

    idmar

    ketal

    .(2001)

    Group

    2

    S28

    .3

    0.51

    S30

    .4

    1.60

    NS71

    .4

    NS69

    .3

    Bain

    &Moy

    (1993)

    ,Beschni

    dtetal

    .(2003),Geursetal

    .(2001)

    ,

    Grun

    dereta

    l.(1999),Jonesetal

    .(1999),Kanetal

    .(200

    2),

    Kel

    leretal.

    (1999)

    ,Lam

    bertetal

    .(2000),May

    fiel

    deta

    l.(2001)

    ,

    Olsonetal.

    (2000a),Schwartz-A

    radetal

    .(2002)

    ,Wallac

    e(2000)

    B

    erge

    &Grnn

    ingsaeter

    (2000),

    G

    runderetal

    .(1999)

    ,Jonesetal

    .(1999),

    M

    ayfiel

    detal

    .(2001)

    ,Moheng

    &Feryn

    (200

    5),

    O

    rtorp

    &Jemt

    (2002),Penarrochaetal

    .(2002)

    ,

    S

    chwartz-A

    radetal

    .(2002)

    ,Wal

    lace

    (2000)

    Group

    3

    S24

    .6

    1.14

    S28

    .9

    5.20

    NS75

    .4

    NS71

    .1

    De

    Bruynet

    al.

    (1999),Karouss

    isetal

    .(2003),Minsk

    &

    Polson

    (1998)

    D

    eBruynetal

    .(1999)

    ,Karouss

    isetal

    .(2003

    )

    Smoking interferes with the prognosis of dental implant treatment 529

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    Table 7 shows ORs and CI95% calcu-lated from studies reporting implant- orpatient-related data, including augmen-tation procedures.

    Results obtained from the systematic

    literature review

    Implant failure

    Five studies reporting on RR or HR forimplant failures in smokers, amongthem one study reporting on HR forimplant failures among smokers afteraugmentation procedures are listed inTable 8. Apart from one study consider-ing a 10-months observation period(Eckert et al. 2001), for smokers, theRR or HR for implant failures with or

    without augmentation procedures werereported significantly enhanced.

    Furthermore, three studies reportedon significantly enhanced implant fail-ure frequencies in smokers, comparedwith non-smokers. In contrast, one study(Lemmerman & Lemmerman 2005) andone meta-analysis (Bain et al. 2002)including implants with recently intro-duced implant surfaces microstructuredby acid-etching, revealed no significantinfluence of smoking on implant failurefrequency (Table 9).

    The risk of peri-implant inflammation

    Soft tissue and inflammatory peri-implant complications associated with

    current tobacco smoking were assessedby five retrospective and two prospec-tive studies, revealing an enhanced riskfor smokers to develop peri-implant softtissue complications. One prospectivestudy investigating the effect of smok-ing on implants in a small cohort of

    periodontally compromised patientsshowed an enhanced risk of implantfailures in smokers (Leonhardt et al.2003) (Table 10).

    The risk of peri-implant bone loss

    Thirteen studies focused on radio-graphic assessment of peri-implantbone loss. In 11 studies, a significantlyenhanced marginal bone loss was foundin smokers, compared with non-smo-kers, including two studies investigatingthe effect of smoking on marginal bone

    loss around implants in patients under-going a periodontitis or peri-implantitistreatment.

    Two studies considered implants withmicrostructured surfaces conditioned byparticle blasting and/or acid-etching oranodic oxidization. One of these studiesrevealed no significant differences ofmarginal bone loss around implants insmokers compared with non-smokers(Aalam & Nowzari 2005). In anotherstudy significantly more bone loss wasfound at implants in smokers with peri-apical radiographs, which was not repro-

    ducible in panoramic radiographassessment, however (Penarrocha et al.2004) (Table 11).

    Smoking as a risk factor for

    augmentation procedures

    Four retrospective studies consideredthe impact of smoking on the courseand outcome of horizontal and/or verti-cal augmentation procedures, SFEA andGBR for the treatment of alveolar ridgedefects before or simultaneously withimplantation. Although the augmenta-

    tion methods and materials as well asbarrier materials used were different,three studies reported significantlymore failures and complications in smo-kers, compared with non-smokers. Thedefect filling in smokers was found lesscompared with non-smokers but showedno significant difference, however(Table 12).

    In a systematic review smoking wasconfirmed as a significant risk factor forimplant failure in connection with SFEAprocedures (0.03opo0.05) (Strietzel2004).

    Table 3. Weighed mean values (WMV) and standard deviations (SD) of percentage distributionsof female (F) and male patients (M) considering different observation periods (group 1:observation period 41 year; group 2:41 and 45 years) and studies considered

    Observation period WMV (%) SD (%)

    Group 1 F 57.0 1.80M 43.0

    Balshi & Wolfinger (1999), De Bruyn &Collaert (1994), Schwartz-Arad et al. (2000),Kronstrom et al. (2001), van Steenberghe et al.(2002), van Steenberghe et al. (2004), Widmarket al. (2001)

    Group 2 F 54.6 1.44M 45.3

    Bain & Moy (1993), Berge & Grnningsaeter(2000), Beschnidt et al. (2003), Grunder et al.(1999), Jones et al. (1999), Kan et al. (2002),Keller et al. (1999), Mayfield et al. (2001),Moheng & Feryn (2005), Olson et al. (2000a),Penarrocha et al. (2002), [28-1]Wallace (2000)

    Table 4. Weighed mean values (WMV) and standard deviations (SD) of percentage distributionsof implant sites (maxilla Mx; mandible Md) considering implant-related data and differentobservation periods (group 1: observation period41 year; group 2: 41 and45 years; group 3:45 years) and studies considered

    Observation period WMV (%) SD (%)

    Group 1 Mx 62.8 1.10Md 37.2

    Balshi & Wolfinger (1999), De Bruyn &Collaert (1994), Kumar et al. (2002), Schwartz-Arad et al. (2000)

    Group 2 Mx 51.0 0.62Md 49.0

    Bain & Moy (1993), Beschnidt et al. (2003),Grunder et al. (1999), Jones et al. (1999),Lambert et al. (2000), Penarrocha et al. (2002),Wallace (2000)

    Group 3 Mx 72.9Md 27.1

    De Bruyn et al. (1999)

    530 Strietzel et al.

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    Discussion

    Methods of evidence-based dentistryhave been introduced for optimizationof decision making processes in dentaldiagnostics and treatment, and for acomprehensive patient information in

    preparation of diagnostic and therapeu-tic interventions, particularly beforeelective treatment. Therefore, patientsdecision making before implantpros-thetic rehabilitation should be supportedby information about risks and risk-associated factors.

    This meta-analysis and systematicreview were performed to provide asummary of cumulative informationon smoking-associated risks for implantprognosis and outcomes after augmenta-tion procedures. Moreover, smokingreduction advice, given in conjunction

    Table 5. Odds ratios (OR) and confidence intervals (CI95%) calculated from studies reporting implant-related data without consideration ofaugmentation procedures

    nCalculated following the suggestion by Gart & Zweifel (1967) and Fleiss (1981).wFemale patients above the age of 50 years, divided into two groups: patients receiving postmenopausal hormone replacement therapy (HRT) and

    patients non-receiving HRT (non-HRT).

    Table 6. Odds ratios (OR) and confidence intervals (CI95%) calculated from studies reporting patient-related data without augmentation procedures

    nCalculated following the suggestion by Gart & Zweifel (1967) and Fleiss (1981).

    Smoking interferes with the prognosis of dental implant treatment 531

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    with dental health information mayhave a marked effect on smokersattitude to their habit and providesufficient incentive to cut down oreven stop smoking as well (Macgregor1996).

    Although tobacco smoking is widelyaccepted as a risk factor for oral healthgenerally (Sham et al. 2003), smokingwas considered a risk factor for implanttreatment since first publication on thisissue by Bain & Moy (1993). Never-theless, the impact of consideration ofthe patients status as a smoker or non-

    smoker in implant treatment planningseems not to be controversial but indis-tinct. A national questionnaire to NHS-consultants to evaluate their attitudesconcerning relevant medical and oralfactors considered in patient selectionfor dental implant treatment in 1999revealed, that among others smokingwas one of the most important medicalfactors contra-indicating implant treat-ment (Butterworth et al. 2001).

    A survey among Finnish dentistsevaluating the association of variouspatient characteristics or possible con-

    tra-indications for dental implant treat-ment revealed, that significantly moredentists working in the public or privatesector recommended implant therapycompared with staff of dental schoolsin case of smoking patients (p50.002).Older dentists (4049 years) were foundmore in favour for implant therapy insmokers than were younger dentists(3039 years) (Heinikainen et al.2002). Estimating smoking as a riskfactor for treatment decisions thereforemight differ among dentists. Thisimpression seems to be confirmed by

    different attempts made to quantify theamount of smoked cigarettes per day:some studies included for meta-analysisand systematic review considered apatient a smoker regardless quantity ofsmoked cigarettes per day or quality oftobacco smoking (Bain & Moy 1993, DeBruyn & Collaert 1994, De Bruyn et al.1999, Jones et al. 1999, Geurs et al.2001). In other studies light and heavysmokers were distincted by quantifica-tion: patients smoking up to 10 cigar-ettes per day (Schwartz-Arad et al.2002) or less than 20 cigarettes per

    day (Gruica et al. 2004) were consideredlight smokers, whereas patients smoking10 (Schwartz-Arad et al. 2002) or 20cigarettes per day or more (Gruica et al.2004) were considered heavy smokers.As quantification of smoking was dif-ferent considering the included studies,in this meta-analysis and systematicreview, any patient who smoked wasconsidered a smoker according to Wal-lace (2000). In all included studies,patient questionnaires were used todetect the smoking status. The relativelyhigh reliability of patient self-reports of

    smoking habits were shown in severalstudies (Fox et al. 1989, OLoughlinet al. 2002).

    Treatment outcome evaluation criter-ia were different in several includedstudies. Besides calculation of differ-ences between cumulative success ratesor implant failure frequency betweensmokers and non-smokers, frequenciesof implant failures or biologic compli-cations were recorded. The risk ofoccurrence of implant failures for smok-ing patients was expressed as OR, cal-culated from studies included into meta-

    analysis by the fixed-effects model aswell as the random-effects model, andcalculated for single studies on basis ofunivariate analysis.

    Our meta-analysis revealed a signifi-cantly enhanced risk for implant failureamong smokers compared with non-smokers, expressed by synthesizedORs of 2.4 considering all includedstudies providing implant-related data,or 2.6 considering all included studiesproviding patient-related data. Compar-ing the implant-related ORs for implantfailure in smokers considering different

    observation periods, the risk of implantfailure for smokers ranged from 2.8 afterup to 1 year decreasing to about 2.3 upto 5 years, indicating a higher risk ofearly implant failure. Nevertheless, therisk of implant failures among smokerswas found significantly enhanced evenafter 5 years considering the findings ofthe systematic review. Here, the effectsof smoking on the enhanced frequencyof peri-implant soft tissue complica-tions, limited peri-implantitis treatmentoutcomes and enhanced peri-implantbone loss, known as factors limiting

    the long-term implant prognosis wereemphasized.

    In an earlier literature review onstudies reporting on threaded implantswith a machined surface (Branemarktype fixtures) predominantly, consensushad been reached that smokinghas a negative influence on implantsurvival (Esposito et al. 1998). Findingsof our meta-analysis and systematicreview were obtained from studiesinvolving threaded titanium implantswith machined, TPS- or HA-coatedsurfaces predominantly, whereas

    Table 7. Odds ratios (OR) and confidence intervals (CI95%) calculated from studies reporting implant- or patient-related data, includingaugmentation procedures

    nSFEA.wLateral alveolar ridge augmentation/GBR).zCalculated following the suggestion by Gart & Zweifel (1967) and Fleiss (1981).

    532 Strietzel et al.

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    studies including implants withmicrostructured surfaces recently intro-duced (acid etched and/or particleblasted) meeting the inclusion criteriafor this meta-analysis were rarelypublished.

    One study on wide diameter-threaded

    machined titanium implants revealed anon-significant HR of 2.4 for implantfailure in smokers after a 10-monthsobservation period (Eckert et al. 2001).Apart from three more studies includedinto systematic review indicating a sig-nificantly enhanced risk of implant fail-ure for smokers (Wilson & Nunn 1999,Kourtis et al. 2004, Ortorp & Jemt2004), four studies (Grunder et al.1999, Kumar et al. 2002, Aalam &Nowzari 2005, Lemmerman & Lem-merman 2005) and one systematicreview (Bain et al. 2002) on implants

    with acid-etched, particle-blasted oranodic oxidized surfaces, revealed noassociations between implant failuresand smoking nor significant differencesof implant failure frequencies amongsmokers and non-smokers, respectively.Furthermore, a comparison betweenthreaded implants with machined andanodic-oxidized surfaces showed no sig-nificant influence of smoking on implantfailures for implants with an anodic-oxidized surface (Rocci et al. 2003).Although smoking was shown to be asignificant risk factor within the limits

    of this meta-analysis and systematicreview referring to studies reporting onimplants with machined or TPS-or HA-coated surfaces predominantly,future studies focusing on implant sur-face condition using acid etchingand/or particle blasting should be ana-lysed regarding influence of tobaccosmoking on early as well as long-term outcomes to allow for a moresubstantiated statement concerning thisissue.

    Our findings considering the implant-related OR for implant failures in smo-

    kers were similar to those published byHinode et al. (2006), who performed ameta-analysis on the influence of smok-ing on osseointegrated implants, basedon implant-related data. As earlierinvestigations revealed a within-patientdependence of implant success rates(Herrmann et al. 1999, 2003), patient-related ORs were calculated separatelyto exclude cumulative effects of indivi-dual risk factors. Compared with 18studies providing implant-related data,only five prospective and five retrospec-tive studies reported patient-related dataT

    able8

    .Character

    isticsofstud

    iesreportin

    gontheriskof

    implant

    failures

    ,includedintothesystemat

    icreview

    Stu

    dy

    Implantsystem

    Stu

    dydesign

    Meanobservat

    ionperiod

    HRORRR

    CI95%

    p

    Samplesizes

    Bae

    lum

    &Ellegaard

    (2004)Threa

    ded,TPS

    -coate

    dorpart

    icle

    -blasted

    Retrospect.

    4

    6years

    HR2.6n

    0.9

    7.6

    o

    0.05

    258impla

    nts:

    man

    dible:

    57,

    max

    illa:

    201

    140patien

    tsw

    Chuangetal

    .(2002b)

    HA

    -or

    TPS-c

    oate

    dor

    uncoated

    /pass

    ivated

    screw-l

    ikes

    hapew

    ithfins

    Retrospect.

    48years

    HR2.9z

    1.6

    5.3

    o

    0.01

    2349imp

    lants:

    man

    dible:

    934,max

    illa:

    1415

    677patien

    ts

    Eckertetal

    .(2001)

    Mac

    hine

    dtitaniumthreaded

    1,z

    Retrospect.

    10months

    HR2.4n

    Notreported

    5

    0.16

    85implan

    ts:

    man

    dible:

    57,

    max

    illa:

    28

    55patients

    Moyetal

    .(2005)

    Different;m

    ost

    implants

    mac

    hine

    dtitanium

    ,threaded

    Retrospect.

    Notreported

    ,

    implante

    dbetween

    1982an

    d2003

    RR1.56k

    1.0

    2.4

    o

    0.05

    4680imp

    lants:

    man

    dible:

    2427

    ,max

    illa:

    2253

    1140patie

    nts

    Augmentationofalveolarcrestwidthand/orheightorinternal

    orexternalsinusfloorelevationandaugm

    entation

    Wooetal

    .2004)

    HA

    -or

    TPS-c

    oate

    doruncoated

    /passivate

    d

    screw-l

    ikes

    hapew

    ithfins

    Retrospect.

    48years

    HR4.4nn

    2.0

    9.8

    o

    0.001

    677impla

    nts:

    man

    dible:

    252,max

    illa:

    425

    677patien

    ts

    (1implantcons

    ideredperpat

    ient

    )

    nCoxsproportionalhazardmodel.

    nnMultivariateCoxmodel.

    wPeriodontallycompromisedpatients.

    zClusteredCoxsregressionanalysis

    .

    Branemarkfixturesorrelatedimplanttype

    s.

    zBranemarkMark-I

    Iwideplatformandwid

    ediameterimplantswereusedexclusively.

    k

    Univariateanalysis

    .

    HR

    ,hazardratio;RR

    ,riskratio;expressing

    theriskofimplantfailuresamongsmokers,comparedwithnon-smokers.

    Smoking interferes with the prognosis of dental implant treatment 533

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    Table9

    .Character

    isticsofstud

    iesreportingonthe

    frequencyof

    implant

    failures

    insm

    okerscompare

    dw

    ithnon-smokers,

    include

    dintothesystemat

    icreview

    Stu

    dy

    Implantcharacterist

    ics

    Stu

    dy

    design

    Meanobservat

    ion

    perio

    d

    Samplesizes

    Eva

    luat

    ioncr

    iter

    ia,

    stat

    istics

    ,outcomes

    p

    Bainetal

    .(2002)

    Threaded

    ,mach

    ined

    titaniumn

    or

    acid

    -etc

    hed

    w

    imp

    lants

    Meta-analys

    is60

    .1mont

    hsn

    43.7

    mont

    hsw

    3prospect

    ivemu

    lticenterstud

    ies

    (2609implantsn

    in1013patients;

    6prospect

    ive

    stud

    ies

    (2274imp

    lants

    w

    in778patients

    )

    Imp

    lantsurv

    ival

    Kap

    lan-

    Meiersurv

    ivalanalys

    is

    3-year

    CSR

    Innon-smokers:

    92.8

    %nimp

    lants

    98.4

    %wimplants;

    Insmo

    kers:

    93.5

    %nimp

    lants

    98.7

    %wimplants

    Nosign

    ificant

    differenceo

    fimplant

    surv

    ivalwasobserved

    betweensmok

    ing

    andnon-smok

    ingpatients

    Kourt

    isetal

    .(2004)

    Cyl

    indric

    ,TPS-c

    oate

    dor

    threaded

    ,particle-

    blaste

    d

    implants

    Retrospective

    4.6years

    1692implants

    in405pat

    ients

    (853implants

    insmo

    kers;

    839implants

    innon-s

    mokers)

    Fai

    lure:

    implantremovalor

    loss

    w2test

    Signi

    ficant

    lyhigher

    failurerate

    insmo

    kers

    compare

    dw

    ithnon-s

    mokers

    o0.001

    Lemmerman

    &

    Lemmerman

    (2005)

    Cyl

    indric

    ,TPS-c

    oate

    dz;

    threaded

    ,mac

    hin

    ed

    titaniumn

    andthreaded

    ,

    acid

    -etc

    hed

    w

    imp

    lants

    Retrospective

    5.3years

    1003implants

    in376pat

    ients

    146implants

    z

    348implantsn

    655implants

    w

    Fai

    lure:

    implantremovalor

    loss

    ANOVA

    Nocorrelat

    ions

    between

    smok

    ingan

    dimplant

    failures

    5

    0.945

    Ortorp

    &Jemt

    (2004)

    Threaded

    ,mach

    ined

    titanium

    implants

    RCT

    5years

    792implants

    in126patients

    Fai

    lure:

    imp

    lantremovalor

    loss

    Life-ta

    bleanalys

    is

    Signi

    ficant

    lyhigher

    failurerate

    insmo

    kers

    compare

    dw

    ithnon-s

    mokers

    pat

    ient-r

    elatedo0.01;

    implant-re

    late

    do0.05

    Wilson

    &Nunn

    (1999)Threaded

    ,TPS-c

    oate

    dor

    mac

    hine

    dimplan

    ts

    Retrospective

    Fai

    ledimplants:

    8months,

    success-

    fulimplan

    ts:

    3.2years

    33failed

    implants

    in

    27patients

    68successfu

    limp

    lants

    in38pat

    ients

    Fai

    lure:

    Imp

    lant

    lossor

    50%bone

    loss

    RR2.5

    (CI95%

    1.13

    5.5

    5)

    Log-r

    anktest

    Signi

    ficant

    lyhigher

    failurerate

    insmo

    kers

    compare

    dw

    ithnon-s

    mokers

    5

    0.024

    nBranemarkfixturesorrelatedthreadedtita

    niumimplantswithamachinedsurface.

    wThreadedtitaniumimplantswithanacid-e

    tchedsurface.

    zTPS-coatedcylindrictitaniumimplants.

    RCT

    ,randomizedclinicaltrial;RR

    ,riskratio;expressingtheriskofimplantfailuresamongsmokers,comparedwithnon-smokers.CSR

    ,cumulativesurvivalrate.

    534 Strietzel et al.

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    without consideration of accompanyingaugmentation procedures and wereincluded into meta-analysis. Thepatient-related OR for implant failuresamong smokers was calculated 2.6 andwas found significantly enhanced,although three studies (De Bruyn et al.

    1999, Penarrocha et al. 2002, van Steen-berghe et al. 2004) revealed no signifi-cantly enhanced ORs, and one study(Kronstrom et al. 2001) revealed a ten-dency of an enhanced OR for implantfailure. Nevertheless, this implicates,that even considering patient-relateddata, the risk of implant failures forsmokers should be considered criticallyin patient information.

    Besides univariate analysis and con-sideration of implant failures in smokersin the meta-analysis, peri-implant para-meters as there are peri-implant mucosal

    status or peri-implant bone level knownto be associated with the implant prog-nosis (Misch 1993, Buser et al. 1997,Roos et al. 1997, Sennerby & Roos1998, Schubert et al. 2001, Cochran etal. 2002) were included into the sys-tematic review concerning associationswith patients tobacco smoking status.The systematic review identified studiesinvestigating on peri-implant soft tissuesand the quality and components of theperi-implant crevicular fluid, revealing asignificantly enhanced risk for peri-implant inflammatory complications in

    in periodontally compromised smokers(Table 10). Although these studiesfocused on single aspects and thereforethe supposed complex mechanisms ofsmoking side effects on the peri-implantsoft tissues might not be completelydiscovered, an enhanced risk for inflam-matory peri-implant complicationsmight be expected among others due to tobacco smoking-associatedvasoconstrictive effects at the end-arter-ial gingival vessels (Sham et al. 2003)and the significant decrease of neutro-phil elastase activity in smokers, which

    might result in a reduced inflammatoryreaction in smokers (Ataoglu et al.2002). These effects seem to blur theinflammatory peri-implant reaction,whereas certain biomarkers for earlyperi-implant bone loss, as thereare pyridinoline (Oates et al. 2004) orb-glucuronidase levels (Schubert et al.2001) were found significantlyenhanced in peri-implantitis. Therefore,a regular and strict recall of smokersundergoing implant treatment is neces-sary for early detection of implant com-plications.T

    able11

    .(Contd

    .)

    Stu

    dy

    Implant

    characterist

    ics

    Stu

    dy

    design

    Meanobservat

    ionperio

    d

    Samp

    lesizes

    Statist

    ics,outcomes

    p

    Nitzanetal

    .(2005)

    Notreporte

    d

    Retrospective

    42.9

    months

    forsmokers;

    48.4months

    fornon-smokers

    646implants

    in161patients

    271implants

    in59smokers;

    375implants

    in

    102non-smokers

    t-test

    ANOVA

    Signi

    ficantly

    highermean

    bone

    loss

    aroun

    dimplants

    insmokers

    bot

    hin

    the

    max

    illaan

    dman

    dible,compare

    dwith

    non-smokers

    5

    0.0

    01

    Penarrochaetal

    .(2004)

    San

    d-blaste

    d,large-gr

    it,

    acid

    -etc

    hed,

    threaded

    implants

    Retrospective

    1year

    108implants

    in42patients

    47implants

    in16smokers,

    61implants

    in26non-smo

    kers

    ANOVA

    Assessmentofpanoram

    icra

    diograp

    hs

    showednosign

    ificantassociat

    ion

    betweenmargina

    lbone

    lossan

    dsm

    oking

    Per

    iapica

    lra

    diographsrevealedapos

    itive

    linearassociat

    ion

    betweensmok

    ing

    andperi-i

    mplant

    bone

    loss

    o0

    .01

    Schwartz-A

    radetal

    .(2005a)

    Notreporte

    d

    Retrospective

    37.9

    months

    277implants

    in61patients

    50implants

    ineigt

    hsmokers;

    227implants

    in53non-smo

    kers

    w2test

    Signi

    ficantlymorecerv

    ical

    boneloss

    at27of

    50imp

    lants

    insmokersan

    d

    at54of

    227implants

    innon-smoke

    rs

    o0

    .0001

    Investigationsontheeffectofsmokingon

    peri-implantbonelevel

    inpatientsundergoingtreatmentofperiod

    ontitisorperi-implantitis

    Wennstrometal

    .(2004a)

    Particle-

    blas

    ted,threaded

    titanium

    imp

    lants

    Prospective

    At

    least1

    year,

    upto

    5years

    148implants

    in51patients

    137implants

    in47patients

    t-test

    ,multipleregressionmodels

    Signi

    ficantlyen

    hanced

    bone-l

    evel

    changearound

    dental

    implantsafter

    a5

    -yearsobservat

    ionper

    iodin

    smo

    kerscompare

    dw

    ithnon-smokers

    5

    0.0

    22

    Wennstrometal

    .(2004b)

    Particle-

    blas

    ted,

    threadedtita

    nium

    implants

    Prospective

    5years

    47patients

    (15smokers,

    32non-s

    mokers)

    Stepw

    ise

    backwar

    dregressionanalys

    is

    Signi

    ficantgreater

    bone

    loss

    in

    smo

    kingpatientscompare

    d

    withnon-s

    mokers

    o0

    .05

    Smoking interferes with the prognosis of dental implant treatment 537

    r 2007 The Authors. Journal compilation r 2007 Blackwell Munksgaard

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    Smoking was also found to have asignificant negative impact on the mar-ginal bone level at implants withmachined or TPS- or HA-coated sur-faces, which again was not confirmed bytwo studies on implants with particle-blasted and acid-etched (Penarrocha

    et al. 2004) or dual acid-etched oranodic-oxidized surfaces (Aalam &Nowzari 2005), showing no associationbetween smoking and marginal boneloss. As shown for implant failure,microstructured implant surfaces seemto have positive influence on marginalbone level around implants in smokerswithin the limits of this literaturereview.

    The impact of smoking on the out-come of SFEA and GBR seems rarelyreported considering the studies identi-fied within this literature search. This

    might be due to the fact, that smoking isoften considered an exclusion criterionfor patient recruitment for prospectivestudies on SFEA or GBR procedures.Nevertheless, our meta-analysisrevealed a synthesized OR of about 3.6and, therefore a significantly enhancedrisk of implant failures for smokersundergoing augmentation procedures.These findings based on studies report-ing outcomes after SFEA and confirmedearlier findings from a systematicreview (Strietzel 2004). Two studies onGBR and ridge augmentation proce-

    dures showed a significantly enhancedrisk of graft or barrier membrane expo-sures requiring partial or complete graftor membrane removal (Strietzel 2001,Schwartz-Arad et al. 2005b). A study onoutcomes after alveolar ridge defectaugmentation using deproteinizedbovine bone mineral for defect fillingand a porcine collagen membrane forGBR revealed a reduced defect filling insmokers, which was not significantlydifferent from non-smokers (Zitzmannet al. 1999). Whether the use of collagenmembranes significantly minimizes the

    risk of negative treatment outcomes forGBR in smokers, was not confirmed dueto insufficient number of available stu-dies and data, respectively.

    Reviews identified within this litera-ture search confirmed, that smoking isone of the factors related to implantfailure by reporting conclusions of sev-eral studies showing that smoking isassociated with higher failure rates,complications and altered peri-implanttissue conditions (Esposito et al. 1998,Sennerby & Roos 1998, Sham et al.2003, Wood & Vermilyea 2004). AnT

    able12

    .Character

    isticsofstud

    iesreport

    ingonoutcomesofaugmentationprocedures

    andGBRbeforeorsimultaneouslyw

    ithimp

    lantat

    ion

    insmokerscompare

    dw

    ithnon-sm

    okers,

    included

    intothe

    systemat

    icreview

    Stu

    dy

    Augmentatio

    nproce

    dure

    Observat

    ionpara

    meters

    Samplesizes

    Statist

    ics,outcomes

    p

    Lev

    inetal

    .(2004)

    Autogenouson

    layb

    onegrafts

    (OBG)n

    ,sinus

    floor

    elevat

    ion

    andaugmentation

    (SFEA)nn

    Fol

    low-u

    pat

    least6

    months

    postsurgery

    Compl

    icat

    ions:

    graftexposureormo

    bilityn;

    swel

    ling

    ,sinus

    infectionnn

    64OBGin56patients;

    79SFEAin72patients

    ANOVA;

    Pearson

    scorrelat

    ioncoef

    ficient

    Compl

    icat

    ions

    follow

    ing

    OBG

    occurred

    in1/3ofsmokersan

    din7.7%ofnon-s

    mokers.

    Compl

    icat

    ions

    follow

    ing

    SFEAoccurred

    in

    23.2

    %

    ofsmo

    kersan

    d6%o

    fnon-s

    mokers

    5

    0.04

    Schwartz-A

    rad

    etal

    .(2005b)

    Autogenous

    bone

    blockgrafts

    for

    horizonta

    lan

    d/orve

    rtical

    ridgeaugmentation

    before

    implantation

    nobarr

    iermem

    bran

    es

    Compl

    icat

    ions:

    inflammatory

    symptoms,

    hematoma,swel

    ling,

    temporaryparesthesi

    a

    Fai

    lures:

    graftexposure

    /remov

    al

    56patients

    (11smokers)

    ,

    64autogenous

    bonegra

    fts

    w2test

    Pearson

    scorrelat

    ioncoef

    ficient

    compl

    icat

    ions

    in50%o

    fsmokersan

    din23%of

    non-smokers

    failures

    in33%of

    smokersan

    din7.7%ofnon-smokers

    5

    0.04

    Str

    ietzel

    (2001)

    Bonesu

    bstitutionm

    ater

    ialsw

    ithor

    withoutautogenous

    bone

    GBRw

    ithnon-resorbab

    lebarr

    ier

    mem

    branes

    (expand

    ed

    polytetrafluoro-e

    thylene)

    for

    horizonta

    lalveolarri

    dge

    defectaugmentation

    Prematuremem

    braneexposure

    ,

    requ

    iringmem

    brane

    removal

    72patients

    (19smokers)

    ,

    72augmentationsites

    w2test

    Therisk

    forprematuremem

    brane

    exposure

    in

    smokers

    issign

    ificantlyen

    hanced

    compare

    dw

    ithnon-smokers

    5

    0.04

    Zitzmann

    etal

    .(1999)

    Augmentationo

    fho

    rizontal

    defects

    (1-,

    2-,

    3-wal

    ldefec

    ts)around

    implants

    ,us

    ing

    deproteinize

    dbovin

    ebone

    mineralan

    daporcineco

    llagen

    barr

    iermem

    branefor

    GBR

    Defectre

    duct

    ionafte

    rre-e

    ntry

    75patients

    (24smokers)

    ,

    112implants

    ,

    112augmentationsites

    Wilcoxonstest

    ,w

    2test

    Themean

    defectre

    ductionat

    implants

    inserted

    in

    smokerswas

    foun

    dless

    (82%)compare

    dwith

    non-smokers

    (88%),but

    didnot

    differsigni

    ficant

    ly.

    Smok

    ingwasnot

    foun

    dto

    besigni

    ficant

    lyassociated

    withtreatmentsuccess

    (OR0.51

    ,CI95%

    0.211.28)

    5

    0.41

    5

    0.16

    538 Strietzel et al.

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    earlier review revealed a significantassociation between smoking and mar-ginal bone loss, biologic complications,reduced survival rate of implants(0.001opo0.05) and the outcome ofonlay bone grafts (po0.05) as well, butno significant correlation was found

    between complications after SFEA andsmoking (Levin & Schwartz-Arad2005).

    Besides the general suggestion to stopsmoking regarding a protocol suggested(Bain 1996) or to quit smoking conse-quently, the peri-operative use of anti-biotics (Gorman et al. 1994) as well asadditional local risk factors as for exam-ple the use of flat instead of high coverscrews should be considered in smokersto prevent postoperative and soft tissuecomplications (Schwartz-Arad et al.2002).

    Moreover, individual peculiarities ofthe patients medical history might besupposed to confound or even enhancethe risk of implant failures attributableto smoking. Three studies were includedinto meta-analysis, although confound-ing parameters might be expected due toselected patient cohorts. Although Bal-shi & Wolfinger (1999) did not find asignificant influence of smoking onosseointegration in a population of dia-betic patients undergoing metaboliccontrol, a rate of 5.7% of non-osseointe-grated implants at time of second stage

    surgery might indicate diabetes mellitusas a risk factor for osseointegration. Inpostmenopausal women undergoinghormone replacement therapy (HRT) toprevent osteoporosis (Minsk & Polson1998), a significant influence of smok-ing on the frequency of implant losswas found in contrast to patients notreceiving HRT as well as in theentire cohort. Thus, a detrimental inter-action between HRT and smoking wasconcluded. Besides smoking, hypothyr-eoidism was supposed to interfere withbone physiology even if correctly medi-

    cally managed. Attard & Zarb (2002)found no significant differences inosseointegration between hypothyroidpatients and a matched healthy controlgroup, but hypothyroid patients showedsignificantly more soft tissue complica-tions during the postoperativecourse and significantly more marginalbone loss compared with the controlgroup.

    Therefore, medical risk factorsshould be considered critically in con-text with a smoking history in decisionmaking before implant therapy.

    In conclusion, smoking was identifieda significant risk factor for dentalimplant therapy. This should beaddressed thoroughly in patient infor-mation before implant treatment.

    A strict recall regime throughout thewhole treatment course to early detect

    negative changes of peri-implant tissuesor implant failure is necessary. Thisrequires identification of smokers at all.

    As augmentation procedures com-prise enhanced potential risks of com-plications generally, smoking should beconsidered an additional risk and there-fore indication should be consideredcautiously and critically, evaluated incontext with additional risk factorsrevealed by medical history.

    A limited number of studies availableon implants with sand-blasted, largegrit, acid-etched and/or acid-etched or

    anodic-oxidized surfaces did not showsignificant associations between smok-ing and implant failure and marginalbone loss. Whether these implant sur-faces indeed significantly improve out-comes in smokers, has to be confirmedincluding more studies providing dataon implant failure in relation to smokersand non-smokers and by larger samplesizes as well.

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