Clinical Research

Tobacco Smoking and Radiographic Periapical Status:A Retrospective Case-Control StudyJos�e L�opez-L�opez, MD, PhD, DDS,* Enric Jan�e-Salas, DDS, PhD,* Jenifer Mart�ın-Gonz�alez, DDS,†

Lizett Castellanos-Cosano, DDS,† Jos�e Mar�ıa Llamas-Carreras, MD, PhD, DDS,‡

Eugenio Velasco-Ortega, MD, PhD, DDS,‡ and Juan Jos�e Segura-Egea, MD, PhD, DDS†

Abstract

Introduction: The aim of this study was to investigateradiographically the relationship of tobacco smokingand periapical status by using a retrospective case-control study design. Methods: The records of 79controls and 79 age- and sex-matched cases were exam-ined. Case was defined as a patient who has at least 1radiographically detectable periapical lesion in a tooth.Control was defined as a patient who has no radio-graphically detectable periapical lesion in any teeth.Periapical status was assessed by using panoramicradiographs and the periapical index score. The historyof smoking and diabetes, the number of teeth androot-filled teeth, and the quality of root fillings wererecorded. Statistical analyses were conducted by usingthe Cohen kappa test, c2 test, Student’s t test, andlogistic regression analysis. Results: Among the casesubjects, 75% had antecedents of smoking, whereasin the control group only 13% had been smokers(odds ratio, 20.4; 95% confidence interval, 8.8–46.9;P = .0000). After multivariate logistic regressionanalysis adjusting for covariates (age, gender, numberof teeth, root-filled teeth, root-filled teeth with aroot filling technically unsatisfactory, and diabetes), astrong association was observed between the presenceof at least 1 radiographically detectable periapicallesion and antecedents of smoking (odds ratio, 32.4;95% confidence interval, 11.7–89.8; P = .0000).Conclusions: After adjusting for age, gender, numberof teeth, endodontic status, quality of root filling, anddiabetic status, tobacco smoking is strongly associatedwith the presence of radiographically diagnosed periap-ical lesions. (J Endod 2012;38:584–588)

Key WordsApical periodontitis, endodontics, oral epidemiology,oral medicine, root canal treatment, tobacco smoking

From the *Department of Odontostomatology, School of DentistrSevilla, Sevilla; and ‡Department of Stomatology, School of Dentistr

Address requests for reprints to Dr Juan Jos�e Segura-Egea, Facsegurajj@us.es0099-2399/$ - see front matter

Copyright ª 2012 American Association of Endodontists.doi:10.1016/j.joen.2012.02.011

584 L�opez-L�opez et al.

Since the U.S. Public Health Service published the first surgeon general’s report onsmoking and health detailing the harmful effects of cigarettes on various health

conditions (1), many adults throughout the world have successfully quit smoking.However, about 35% of men and 22% of women in developed countries and 50% ofmen and 9% of women in developing countries smoke tobacco (2).

In relation to oral health, some studies suggest that smoking increases the risk ofcaries (3, 4), and cigarette smoking has been identified as a significant risk factor forperiodontal disease and accounts for more than half the cases in the population (5).The harmful effects of tobacco smoking on the periodontal bone have been demon-strated in several cross-sectional and longitudinal studies (6, 7). On this basis, itwas assumed that smoking might be a risk factor for apical periodontitis, but untilrecently there had been no suggestion of a possible link between smoking andapical periodontitis or endodontics in general (8). Kirkevang and Wenzel (9) reportedfor the first time an epidemiologic study demonstrating the association between tobaccosmoking and apical periodontitis, suggesting that a delay in periapical healing mightprovoke the higher prevalence of apical periodontitis in smokers. Since then, severalinvestigations have analyzed the possible association between smoking and endodonticvariables, ie, prevalence of periapical lesions and root canal treatment, with incon-gruous results (10–15). However, these studies were cross-sectional in design, andsome of them had small number of patients (11, 15). More studies such as case-control and observational cohort studies are required to make firm conclusions.

The objective of this retrospective case-control study was to investigate therelationship of tobacco smoking and radiographically diagnosed apical periodontitisby using a case-control study design. The null hypothesis was that smoking is notassociated with an increased risk of radiographically detectable periapical lesions.

Materials and MethodsSubjects

The protocol was approved by the Ethic Committee of the Dental Faculty ofBarcelona, Spain, and each subject signed a consent form after being advised of thenature of the study.

Participants were recruited among new patients presenting consecutively seekingroutine dental care (not emergency care) at the Dental Clinic of the University ofBarcelona Spain. Subjects who met the inclusion/exclusion criteria of this study wereasked to voluntarily participate. Inclusion criteria were as follows: patients > 18 years,having at least 8 remaining teeth, who agreed to a radiographic examination. Exclusioncriteria encompassed patients < 18 years old, having < 8 remaining teeth, or who didnot agree to a radiographic examination.

y, University of Barcelona, Barcelona; †Department of Endodontics, School of Dentistry, University ofy, University of Sevilla, Sevilla, Spain.ultad de Odontolog�ıa, University de Sevilla, C/Avicena s/n, 41009 Sevilla, Spain. E-mail address:

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Clinical Research

Case was defined as a patient who has at least 1 radiographically

detectable periapical lesion in a tooth. Control was defined as a patientwho has no radiographically detectable periapical lesion in any teeth.Three hundred patients were examined; 251 (83.6%) were eligibleto take part in this study on the basis of the inclusion/exclusion criteria.After the radiographic examination, 79 (31.5%), 50 men and 29women, ranging from 23–83 years old (52.0� 15.5 years), were clas-sified as cases because they had at least 1 periapical lesion (case group,n = 79). Among the remaining 172 patients (68.5%) who did not showany periapical lesion (controls), 79 were age- and sex-matched withthe case patients, constituting the control group (51.8 � 15.3 years).

Anamnestic and Radiographic ExaminationSmoking history was obtained by interviewer-administered ques-

tionnaires as previously described (12, 13). Patients were classifiedas nonsmokers if they answered ‘‘no’’ to the question: ‘‘Have youever smoked?’’. On the contrary, patients who answered ‘‘yes’’ tothe previous question were classified as smokers. Investigations inrepresentative population samples provided evidence that self-reported smoking status is accurate (16). Other characteristics of thestudied subjects that were relevant to the objective of the study, suchas the number of teeth and the presence of diabetes, are displayed inTable 1.

Radiographic periapical status was diagnosed on the basis ofexamination of digital panoramic radiographs of the jaws. Two trainedradiographic technicians who used a digital orthopantograph machine(Promax, class 1, type B, 80 KHz; Planmeca, Helsinki, Finland) took thepanoramic radiographs.

One observer with 12 years of clinical experience in endodonticsexamined the radiographs. The periapical status was assessed by usingthe periapical index (PAI) (17) as described previously (13, 15).Briefly, before evaluation, the observer participated in a calibrationcourse for PAI system, which consisted of 100 radiographic imagesof teeth, some root-filled and some not. Each tooth was assigned to1 of the PAI scores by using visual references for the 5 categories withinthe scale. After scoring the teeth, the results were compared with a goldstandard atlas, and a Cohen kappa was calculated (0.75). Intraobserverreproducibility was evaluated by the repeat scoring of 50 patients2 months after the first examination. These patients were randomlyselected. Before the second evaluation of the radiographs, the observerwas recalibrated in the PAI system by scoring the 100 standard images.The intraobserver agreement test on PAI scores on the 50 patientsproduced a Cohen kappa of 0.79. A score > 2 (PAI$ 3) was consid-ered to be a sign of periapical pathology. The worst score of all roots wastaken to represent the PAI score for multirooted teeth.

All teeth were recorded. Teeth were categorized as root-filled teethif they had been filled with a radiopaque material in the root canal(s).The quality of root fillings was evaluated according to the criteriadescribed previously (19). Briefly, the root filling was considered tech-nically satisfactory when both the adaptation of root filling to canal wallsand the length of root filling were adequate.

The following information was recorded on a structured form foreach subject: (1) number of teeth present, (2) number and location ofteeth having identifiable periapical lesions, (3) number and location ofroot-filled teeth, (4) number and location of root-filled teeth havingidentifiable periapical lesions, and (5) number of root-filled teethwith a root filling considered technically unsatisfactory.

Statistical AnalysisRaw data were entered into Excel (Microsoft Corporation, Red-

mond, WA). All analyses were done in an SPSS environment (Version

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11; SPSS, Inc, Chicago, IL). Data are reported as mean � standarddeviation. Chi-squared analysis and Student’s t test were used to analyzethe distribution of study factors between the case and control groups.Furthermore, a logistic regression analysis was performed to measurethe strength of the association between smoking and the presence ofapical periodontitis adjusted for the presence of covariates.

ResultsTable 1 shows the distribution of the study factors in both control

and case groups. There was no significant difference in age, gender, ornumber of teeth between control and case groups. The average numberof teeth per subject was 23.4� 6.0 and 23.0� 5.7 in the controls andcases, respectively (P > .05). Root-filled teeth were found morefrequently in the case group. The average number of root-filledteeth per subject was 2.1 � 2.1 in cases and 1.4 � 1.6 in controls(P < .05). One or more root-filled teeth were found in 57.0%(n = 45) and 73.4% (n = 58) of control and case subjects, respectively(odds ratio, 2.1; 95% confidence interval [CI], 1.1–4.1; P = .0299).Among cases, 36.7% (n = 29) had at least 1 root filling technicallyunsatisfactory (inadequate adaptation or length). Among control sub-jects, 13.9% (n = 11) had at least 1 inadequate root filling (odds ratio,3.6; 95% CI, 1.6–7.9; P= .0010). Type 2 diabetes was present in 17.7%of control subjects and in 27.8% of cases, but the difference was notsignificant (P > .05). No patient had type 1 diabetes.

A strong association was observed between smoking and the pres-ence of at least 1 radiographically detectable periapical lesion (case).Among the case subjects, 74.7% (n = 59) had antecedents of smoking,but in the control group only 12.7% (n = 10) had been smokers (oddsratio, 20.4; 95% CI, 8.8–46.9; P = .0000).

Multivariate logistic regressions were run with age, gender (male/female), number of teeth, diabetes (yes/no), smoking (yes/no), at least1 root-filled tooth (yes/no), and at least 1 root-filled tooth with a rootfilling considered technically unsatisfactory as independent variablesand radiographically diagnosed periapical lesion (present = case/absent = control) as the dependent variable (Table 2). In the multivar-iate analysis including all the above factors, smoking (odds ratio, 32.4;95% CI, 11.7–89.8; P= .0000) remained highly significant, whereas allother factors were not statistically associated with the periapical status.

DiscussionThe aim of this study was to investigate the possible association

between smoking and the radiographic periapical status by usinga case-control study design. Results reveal a statistically significant asso-ciation between tobacco smoking and the presence of radiographicallydiagnosed periapical lesions.

Because control subjects were age- and sex-matched with the casepatients, there were not significant differences between control and casesubjects in age or in gender. Moreover, the average number of teeth perpatient was similar in both groups. The study carried out by Lang et al(20) concluded that missing teeth (as well as number of teeth perpatient) performed well as an indicator of oral health status. As a result,it can be considered that the oral health status of control and casesubjects was comparable.

Although there seemed to be no standard criteria for the registra-tion of apical periodontitis in epidemiologic surveys for periapicalradiographs or panoramic radiographs, the PAI scoring system hasbeen modified and applied to epidemiologic (21, 22) and clinicalcomparative studies of treatment outcome (23, 24). PAI was firstdescribed for periapical radiographs (17), but numerous epidemio-logic studies have used this index for panoramic radiographs(25–30) or a combination of panoramic radiographs and periapical

Smoking and Periapical Status 585

TABLE 1. Distribution of Study Factors among Cases/Controls

Control, n = 79 (50%) Cases, n = 79 (50%) Total, n = 158 (100%) P value

Age, y t testMean � SD 51.8 � 15.3 52.0 � 15.5 51.9 � 15.4 >.05

Gender c2

Male 50 (63.3%) 50 (63.3%) 100 (63.3%)Female 29 (36.7%) 29 (36.7%) 58 (36.7%) >.05

No. of teeth t testMean � SD 23.4 � 6.0 23.0 � 5.7 23.2 � 5.8 >.05Median 25 25 25

Type 2 diabetes c2

Yes 14 (17.7%) 22 (27.8%) 36 (22.8%)No 65 (82.3%) 57 (72.2%) 122 (77.2%) >.05

Smoking c2

Yes 10 (12.7%) 59 (74.7%) 69 (43.7%)No 69 (87.3%) 20 (25.3%) 89 (56.3%) <.001

RFT c2

Any 45 (57.0%) 58 (73.4%) 103 (65.2%)None 34 (43.0%) 21 (26.6%) 55 (34.8%) <.05

No. of RFT t testMean � SD 1.4 � 1.6 2.1 � 2.1 1.7 � 1.9 <.05Median 1 1 1

RFT inadequate c2

Any 11 (13.9%) 29 (36.7%) 40 (25.3%)None 68 (86.1%) 50 (63.3%) 118 (74.7%) <.001

RFT, root-filled teeth; SD, standard deviation.

Clinical Research

radiographs (31–34). It has been reported that panoramic digitalimages achieve significantly higher percentages of teeth with PAIscoring $3 (29, 35, 36). On the contrary, other investigators havefound that an underestimation of lesions occurred when panoramicradiography was used (31, 37–39).

In this study, not only groups, cases, and controls have been age-and sex-matched, but also several factors have been analyzed and usedas covariates in the logistic regression model to avoid bias in the results.It has been shown that root-filled teeth are more frequently affected byradiographically diagnosed periapical lesions than nontreated teeth(14, 22). A high odds ratio for smoking could potentially beexplained by latent root canal infection being more readily expressedas apical periodontitis among smokers than among nonsmokers.Because of the adverse effects of tobacco smoking on wound healingand the host tissue defense to infections in general, the healing phaseof apical periodontitis subsequent to root canal treatment might alsobe more delayed and even more often failing. Moreover, in thepresent study the average number of root-filled teeth per subjectwas significantly higher in cases (2.1 � 2.1) than in controls (1.4 �1.6) (P < .05). Furthermore, the quality of root canal filling hasbeen also shown to be a major predictor of persistent apical periodon-titis associated to root-filled teeth and also could act as a confoundingfactor (18). In the present study 37% of cases had at least 1 root filling

TABLE 2. Logistic Regression Analysis (multivariate analysis) of Influence of Inde

Independent variables B P value Odd

Age 0.0239 .2601 1.Gender �0.8128 .0877 0.No. of teeth �0.0151 .7789 0.Diabetes 0.5525 .3305 1.Smoking 3.4784 .0000 32.RFT 0.7582 .1492 2.Unsatisfactory root filling 0.6349 .2412 1.

Overall model fit. c2 = 81.3120; df = 7; P = .0000; B = regression coefficient.

Independent variables are age, gender, number of teeth, diabetes (yes = 1/no = 0), smoking status (yes =

(present = 1/absent = 0). Dependent variable is radiographic signs of apical periodontitis in at least 1 to

RFT, root-filled teeth.

586 L�opez-L�opez et al.

technically unsatisfactory, but only 14% of controls had at least 1inadequate root filling (P = .0010). Thus, in the present investigationthe number of root-filled teeth and the quality of root fillings couldbe acting as confounding factors, biasing the results. However, neitherthe number of root-filled teeth nor the presence of technically unsatis-factory root filling correlated significantly with periapical status in theoverall model fit.

The results of a number of studies suggest that radiographicallydiagnosed chronic apical periodontitis could be associated to diabetesmellitus (24, 30, 40). In this study, there were no differences betweencontrol and case groups in the antecedents of diabetes. Thus, diabetes isnot acting as a confounding factor.

The inclusion question that addressed smoking history was‘‘Have you ever smoked?’’. This question has been used in previousstudies to classify smoker and nonsmoker subjects (12, 13).However, this inclusion question does not imply the assumption thatlight smoking for a short period long ago is relevant as heavypermanent smoking. Caraballo et al (16) showed that self-reportsmoking and biochemical measurement of serum cotinine concentra-tion give approximately the same overall estimates of smoking preva-lence, concluding that self-reported smoking status among adultrespondents to a population-based survey is accurate. However, theaccuracy of self-report must be carefully differentiated and not used

pendent Variables on Dependent Variable

s ratio 95% CI inferior limit 95% CI superior limit

0242 0.9825 1.06774436 0.1745 1.12779850 0.8862 1.09487376 0.5710 5.28824067 11.6915 89.82541344 0.7618 5.98018869 0.6526 5.4560

1/no = 0), at least 1 RFT (present = 1/absent = 0), and at least 1 RFT with unsatisfactory root filling

oth (present/absent).

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Clinical Research

interchangeably with the duration and quantity of smoking. Furtherstudies must be carried out to relate the periapical status to dataregarding frequency and timing of smoking.

Cigarette smoking has been associated to periodontal disease.Cross-sectional and longitudinal studies have demonstrated the harmfuleffects of tobacco smoking on the periodontal bone (7). On this basis, itwas assumed that it might be a risk factor for apical periodontitis,exerting a negative influence on the apical periodontium of endodonti-cally compromised teeth, facilitating the extension of the process ofperiapical bone destruction, and/or interfering with healing and repairevents after root canal treatment. Consequently, an increased numberand/or size of periapical lesions would be expected in smokers (10).

The main purpose of the present study was to investigate thepossible association between the radiographic periapical status andantecedents of smoking. Results show that a high percentage of cases(75%) had antecedents of smoking, whereas only 13% of controlsubjects had been smokers (P = .0000). Multivariate regression anal-ysis has shown that smoking remained significantly associated toperiapical status after adjusting for age, gender, number of teeth,endodontic status, and diabetes (odds ratio, 32.4; 95% CI, 11.7–89.8; P = .0000). These results are in agreement with the results re-ported by Kirkevang and Wenzel (9), who found a statistical associationbetween smoking and apical periodontitis (P = .05; odds ratio, 1.64;95% CI, 1.0–2.8). Moreover, current evidence would indicate thatsmoking is a significant risk factor in inflammation of the marginalperiodontium (7, 41, 42), and therefore it might be hypothesizedthat it would have a similar effect on the apical periodontium.Kirkevang et al (14) have also reported that smoking is a statisticallysignificant risk factor for apical periodontitis when assessed separately(odds ratio, 1.9; 95% CI, 1.3–2.8) but had a reduced and nonsig-nificant effect on the risk of developing apical periodontitis when adjust-ing for age and reduced marginal bone level (odds ratio, 1.3; 95% CI,0.9–2.1). The authors claimed that the strong correlation betweensmoking and marginal periodontitis found in the studies cited previ-ously might at least partly explain why the association between smokingand periapical status was reduced when both smoking and marginalbone level were entered into the analysis.

Both the present study and the studies performed by Kirkevang andWenzel (9) and Kirkevang et al (14) only assessed the periapical condi-tion by radiographic methods, and there was no clinical examinationcarried out, and it is recognized that radiographic evaluation is nota perfect method of assessment because apical inflammation can bepresent in the absence of radiographic signs (8). This has been demon-strated in histologic evaluation of upper maxillary teeth (43). Kirkevangand Wenzel (9) discussed that in several orthopedic studies, bonyhealing was slower in smokers than in nonsmokers (44, 45),suggesting this delay in healing might result in an over-representationof disease in the smoking group in their study.

On the contrary, other investigations have not found any associa-tion (10, 11). Bergstr€om et al (10) in a cross-sectional study retrospec-tively examined 247 intraoral radiographs of smokers, nonsmokers,and former smokers and compared for incidence of apical disease.Although the mean number of periapical lesions was 6% in smokers,4% in former smokers, and 3% in nonsmokers, the association betweensmoking and periapical lesions was not significant after controlling forage. This study did not examine a random sample of a general popula-tion as had the initial study by Kirkevang and Wenzel (9), but rather itexamined a subpopulation of Swedish musicians, who might differ fromthe general population. As the authors themselves stated (10), the inves-tigation was cross-sectional in design, and the conclusion should beregarded as temporary until confirmed by long-term observations.Marending et al (11) have studied the impact of many patient-related

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factors with the outcome of root canal treatment and found that smokinghad negligible impact. Nevertheless, any conclusions from this studyare limited, owing to the small number of patients in each group,17 smokers and 31 nonsmokers.

The fact that in the present study smoking came out as a veryhigh risk factor for periapical disease (odds ratio, 32.4) indeed isstriking, particularly from the aspect that smoking hardly can be re-garded as a primary cause of root canal infection and apical perio-dontitis, whereas caries, restorative procedure, and dental traumaare. Therefore, it might be that the study design had not properlyconsidered all relevant confounding factors. Periodontal status,immune disorders, endocrine diseases, metabolic syndrome, bonediseases, and socioeconomic status have not been taken into accountas exclusion criteria. The wide odds ratio confidence interval, espe-cially in the multivariate analysis (95% CI, 11.7–89.8), could beexplained by this reason. Although the average number of teeth wasequal between the 2 groups, this cannot be regarded as sufficient esti-mate of identical risk exposure for pulpal disease, root canal infec-tion, and subsequent apical periodontitis. Additional studies mustbe developed that match the cases with well-known risk factors forapical periodontitis such as caries, quality of coronal restorations,and history of trauma.

To our knowledge, at present all the studies conducted to in-vestigate the association between smoking and periapical status werecross-sectional studies. It is difficult to control for confounding factorsin cross-sectional studies, particularly when any influence on apical pe-riodontitis is likely to be multifactorial (15). This is the first studyanalyzing the association between periapical status and tobaccosmoking by using a case-control study design and taking into accountconfounding factors such as number of teeth, number of root-filledteeth, number of root-filled teeth with unsatisfactory root filling,diabetes, and oral health status.

Although it is not the purpose of this investigation, some consid-erations can be made with respect to the mechanism by which periap-ical status could be affected by smoking. Tobacco smoking exacerbatesbone loss in the systemic skeleton (46) and oral cavity (6) and impairsthe body’s responses to infection (47). Although the counts of periph-eral leukocyte are higher in smokers than in nonsmokers (48, 49),the functions of polymorphonuclear leukocytes, macrophages, T-celllymphocytes, antibodies, and immunoglobulins A, G, and M aresuppressed in smokers (50). Smoking also induces a chronic systemicinflammatory response increasing C-reactive protein levels in serum(46, 49, 51). These observations suggest that once bacterial infectionbegins in the pulp and surrounding tissues, smokers are less likelythan nonsmokers to be able to limit the destruction (12). Anothercontributory explanation for the results of this study is decreasedoxygen delivery and damage to the pulpal circulatory system. Smokingdecreases the blood’s oxygen-carrying capacity (52), increasing thelevels of carboxyhemoglobin in the blood. Moreover, smoking causesvascular dysfunction, impaired microvascular function, and endothelialcell injury in blood vessels, possibly because of free radicals found intobacco smoke (52, 53). Because components in cigarette smokeinduce stress (54) and reduce blood flow volume, vessels that servethe tooth root are likely to show signs of vascular dysfunction thatrestrict nutrient supply and impede cellular repair. This suggests thatsmoking could contribute to early tissue death within the pulp cavity.Any one of these pathophysiologic pathways can potentially affect thehealth of the tooth pulp and surrounding bone tissues and result ina higher frequency of radiographic periapical lesions in smokersthan in nonsmokers (12).

In conclusion, the results of the present study show that afteradjusting for age, gender, number of teeth, endodontic status, quality

Smoking and Periapical Status 587

Clinical Research

of root filling, and diabetic status as covariates, tobacco smokingis strongly associated to the presence of radiographically diagnosedperiapical lesions.

AcknowledgmentsThe authors deny any conflicts of interest related to this study.

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JOE — Volume 38, Number 5, May 2012