J Clin Periodontol 2015; 42: 900–907 doi: 10.1111/jcpe.12452

Alicia Morales1, Paola Carvajal1, Prevalence and predictors Hugo Romanelli2, Mariel Gomez 2, Cristina Loha3, Marıa E. Esper4, Graciela Musso4, Carlos M. Ardila5, for clinical attachment loss in Andres Duque6, Marco Medina7, Luis Bueno8, Ernesto Andrade8, Carolina Mendoza9 and Jorge Gamonal1 adolescents in Latin America: 1Laboratory of Periodontal Biology, Department of Conservative Dentistry, Faculty of Dentistry, Universidad de Chile, cross-sectional study Santiago, Chile; 2School of Dentistry, Universidad de Maimonides, Buenos Aires, Argentina; 3Faculty of Dentistry, Universidad Nacional de Cuyo, Mendoza, Argentina; Morales A, Carvajal P, Romanelli H, Gomez M, Loha C, Esper ME, Musso G, 4Faculty of Dentistry, Universidad Nacional Ardila CM, Duque A, Medina M, Bueno L, Andrade E, Mendoza C, Gamonal J. de Cordoba, Cordoba, Argentina; 5 Prevalence and predictors for clinical attachment loss in adolescents in Latin Department of , School of Dentistry, Universidad de Antioquia, Medellın, America: cross-sectional study. J Clin Periodontol 2015; 42: 900–907. doi: 6 10.1111/jcpe.12452 Colombia; Department of Periodontology, School of Dentistry, Universidad CES, Medellın, Colombia; 7Faculty of Dentistry, Abstract Universidad Central del Ecuador, Quito, Aim: To describe the prevalence, severity and extension of clinical attachment Ecuador; 8Department of Periodontology, loss (CAL) and to study the predictors in 15- to 19-year-old adolescents from Universidad de la Republica, Montevideo, high schools in the Latin America. Uruguay; 9Oral Health Department, Materials and Methods: A cross-sectional, epidemiological study was performed. DIPRECE, Ministerio de Salud, Santiago, The sample included 1070 high school adolescents 15–19 years of age from Chile Santiago de Chile (Chile), Buenos Aires, Cordoba, Mendoza (Argentina), Montevideo (Uruguay), Quito (Ecuador) and Medellın (Colombia). Calibrated examiners performed full mouth, six sites per tooth clinical examination. Results: There was a response rate of 100%. The prevalence of CAL ≥3 mm in ≥1 site was 32.6%, probing pocket depth ≥4 mm was 59.3% and (BoP) ≥25% was 28.6%. The logistic regression analysis adjusted for cities revealed that smoking (OR = 1.6), attending public school (OR = 2.3) and having Key words: adolescent; clinical attachment a BoP ≥25% (OR = 4.2) were positively associated with CAL ≥3 mm in ≥ 1 site. loss; predictor; probing depth Conclusion: Clinical attachment loss was prevalent in Latin America adolescents and it is associated with smoking, attendance public school and BoP. Accepted for publication 1 September 2015

Periodontal disease is a heteroge- described for this disease, are socioe- Latin America adults than in the neous group of conditions that affect conomic level, age, gender, and pla- USA and Europe (Oppermann et al. gum health and tooth supporting que and bleeding indices. Smoking 2015). The overall prevalence of structures. Some risk indicators, and diabetes mellitus are major risk CAL ≥5 mm was 62.6% among factors for adults in Porto Alegre, Brazil (Susin Conflict of interest and source of (Borrell & Crawford 2012, Genco & et al. 2004), and it was 58.3% and funding statement Borgnakke 2013). 81.4% among 35–44 and 55–74 year- The authors declare that there are no Surveys in adults performed in old- subjects in Chile (Gamonal conflicts of interest in this study. This Canada, USA and Australia showed et al. 2010). study was funded by the Federacion 15–30% of clinical attachment loss The prevalence of CAL ≥3 mm Iberopanamericana de Periodoncia, (CAL) ≥6 mm (Gilbert & Heft 1992, among adolescent population range Colgate-Palmolive and the Participat- Locker & Leake 1993, Slade et al. between 0% and 10.1% (Hoover ing Universities. 1993). CAL is more prevalent in et al. 1981, Albandar et al. 1997).

900 © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Clinical attachment loss in adolescents 901

Latin America adolescents presented Buenos Aires, Cordoba, Mendoza Sampling – stage 3 a prevalence of CAL ≥3 mm of (Argentina), Montevideo (Uruguay), The subjects were selected according 4.5% in Santiago de Chile, Chile Quito (Ecuador) and Medellın to gender and age, using a random- (Lopez et al. 2001), 4% in Santo (Colombia), according to data ization table. The number of individ- Domingo, Dominican Republic obtained from the Statistics Institute uals to be included in each stratum (Collins et al. 2005), 22.3% in Porto of each country. This age group was is derived by proportionate stratifica- Alegre, Brazil (Susin et al. 2011) and selected based on recommendation tion. Subjects undergoing fixed 100% in Cajaiba, Brazil (Corraini from World Health Organization for orthodontic treatments at the time et al. 2008). oral health surveys (Petersen & of clinical examination or with any However, there is a considerable Ogawa 2005). The five countries condition that required antibiotic lack of methodological consistency included in this study, were selected premedication prior to the periodon- in periodontal epidemiology. Some after accepting the invitation from tal examination were excluded from of methodological aspects consider the Federacion Iberopanamericana the study. the use of different periodontal de Periodoncia and then several protocols and periodontal probes, Universities of these countries were missing or insufficient examiner invited to organize the present Data collection techniques calibration, assessment of different study. Clinical evaluation was carried out clinical variables, and large varia- in schools, under room light. The tions in the definition of periodonti- Sampling and sample size examiner was properly sitting down tis (Savage et al. 2009, Holtfreter and the subject was lying down on a et al. 2014). Prevalence studies on The sample size was calculated con- clinical stretcher. Periodontal clinical periodontal disease in Latin America sidering the rate of 4.5% of CAL parameters were evaluated at six adolescents are marginal (Botero ≥3 mm in ≥1 sites in adolescents sites in all teeth, excluding third et al. 2015), difficult to compare described by Lopez et al. (2001), molars. These parameters included (Mendoza et al. 2006), and they used with 95% confidence interval and probing pocket depth (PPD), partial recording protocol, which 1.6% range of error. Thus, the study dichotomous mesio-buccal, mid- tended to underestimate the CAL required a sample of 1032 subjects, buccal, disto-buccal, disto-lingual, prevalence (Peres et al. 2012). To plus an oversampling to allow better mid-lingual and mesio-lingual mea- overcome these limitations, some precision in estimates. According to surements of supragingival plaque authors suggested some principles the Statistics Institute of each accumulation (plaque index [PI]), such as: definition of case as a per- country, this study included adoles- and bleeding on probing (BoP) at son with CAL (Lopez & Baelum cents from cities mentioned above, the base of the crevice. Clinical 2003), examiner calibration, full representing the total adolescents attachment loss was determined mouth assessment (Savage et al. population in the five countries. The using the distance from the cement- 2009) and standardized principles for sampling units were schools and unit enamel junction (CEJ) to the free reporting prevalence and severity of of analysis was the adolescent. (FGM) and the dis- periodontal diseases (Holtfreter et al. Sampling – stage 1 tance from the FGM to the bottom 2015). of the pocket/sulcus. From these two Taking these factors into consid- The number of subjects in each city measurements, the clinical attach- eration, CAL was measured in 15- is derived by proportionate stratifica- ment level (distance from the CEJ to to 19-year-old secondary school tion, according to data from the the bottom of pocket/sulcus) was adolescents from Santiago de Chile Statistics Institute of each country. calculated. The assessment of the (Chile), Buenos Aires (Argentina), In this study, only urban adolescents periodontal supporting tissue status Cordoba (Argentina), Mendoza were sampled. was made with a first generation (Argentina), Montevideo (Uruguay), Sampling – stage 2 manual (UNC-15; Quito (Ecuador) and Medellın Hu Friedy Mfg. Co. Inc., Chicago, (Colombia) to determine the preva- A stratified, random sample was IL USA). At the time of recording lence, severity and extension CAL generated using information on the depths, if necessary, measurements and to study the predictors. governmental support to high were approximated to the nearest schools to form two strata, one of whole millimetre. The interdentally the high schools receiving partial or Material and Methods measures were probed parallel in total support from the government relation to the tooth axis. Finally, (n = 57), and the other high schools Study design the subjects were asked to fill a short not receiving support (n = 47). questionnaire giving details about A cross-sectional, epidemiological Within each stratum, schools were their demographic information study was conducted between 2010 selected using a randomization table. (name, gender, age) and smoking and 2012. The target population for All schools were contacted to obtain habits. this cross-sectional screening study information of the number of stu- was defined as students the last four dents in the last four grades. How- Reproducibility of the measurements grades that cover adolescence in the ever, 16 schools do not respond and high schools. The study included 15- four schools declined to participate, All examiners in the survey group to 19-year-old high school adoles- leaving 84 schools available for the received theoretical classes, clinical cents from Santiago de Chile (Chile), study. training and calibration in CAL, © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 902 Morales et al. which were administered by a senior (Lang & Tonetti 2003, Leininger statistical package for Mac (Stata- member of the Periodontal Depart- et al. 2010). Corp, College Station, TX, USA). ment of the Faculty of Dentistry, The type of school as public or University of Chile (Jorge Gamo- private was considered (public Results nal). CAL was used to record the school received governmental sup- periodontal condition of the individ- port, and private school did not). A total of 1234 subjects were invited uals. Nine dentists performed the This variable was used as a proxy and examined, and 1070 of those 15- clinical evaluations. Calibration for socioeconomic position (Lopez & to 19-year-old adolescents complied training was performed within Baelum 2007). Subjects were defined with the criteria (Table 1). The successive days. All examinations by their smoking habits as either reasons for non-eligibility were: were repeated until acceptable con- never- smokers or smokers (current undergoing orthodontic treatment sistency was achieved. A > 93% of or former smokers). (76), requirement for antibiotics (19) intra-examiner agreement was and being under the age of 15 (35). obtained for CAL ≥1 mm, with an Non-participation due to refusal to Ethical considerations average maximum difference for be examined (34). The final sample each subject of 0.3 mm, correspond- The Ethics Committee of each centre included 555 (51.87%) female and ing to kappa value of 0.88. A > 91% revised and approved the protocol 515 (48.13%) male. The mean age of inter-examiner agreement was for this study. An informed consent was 16.4 1.5 years. 27.5% of sub- obtained for the site with document was handed to every sub- jects wereÆ smokers and 52.2% of CAL ≥1 mm, with an average maxi- ject who had agreed to participate them attended a public school mum difference for each subject of for their guardians to revise and (Table 1). The distribution according 0.8 mm, corresponding to kappa sign. All subjects were informed of to centre in Table 1. value of 0.95. The reliability of the their oral health status via written Overall in each subject, in total examiners was in a range considered communication if so required. Sub- 164.9 6.6 sites were examined in good to excellent. jects with oral pathologies were duly 27.5 Æ1.1 teeth. The mean CAL Validity and reliability examina- informed, and a written derivation wasÆ 0.5 0.6 mm, the mean tions were performed during the field to a specialist was provided. PPD wasÆ 1.9 0.5 mm, the mean period at the beginning of the study BoP was 19.9Æ 24.1%, and the Æ (Mendoza, Argentina) and then Statistical analysis mean PI was 48.1 30.1%. Females when 50% of the subjects had been had a significantlyÆ higher means examined (Santiago de Chile) (Lan- Univariable and multivariable analy- PPD (1.9 mm versus 1.8 mm), BoP dis & Koch 1977). ses were used to compare CAL, (50.0% versus 46.1%) and PI (22.9% PPD, BoP and PI measures and versus 16.8%) (Table 2 and 3). tooth count between males and Subjects attended public school pre- Variable definitions females. Also, mean CAL, PPD, sented significantly higher mean Clinical attachment loss and PPD BoP, PI and prevalence of CAL CAL (0.5 mm versus 0.4 mm), PPD were presented as mean ( standard ≥3 mm in ≥1 site were compared (2.0 mm versus 1.8 mm), BoP error). According to standardsÆ for between females- males, adolescents (25.3% versus 14.1%) and PI (52.9% reporting attending private- public school, versus 43.0%). Smokers had a signif- prevalence and severity in epidemio- smokers and no smokers, subjects icantly higher mean CAL (0.6 mm logical studies (Holtfreter et al. who had BoP <25% and ≥25% or versus 0.5 mm) and PPD (1.9 mm 2015), the prevalence of CAL was PI <30% or ≥30%. versus 1.8 mm), and they had signifi- defined as the percentage of subjects Logistic regression analyses were cantly lower mean BoP (18.4% who had ≥1 site with CAL ≥1 mm, used to assess the influence of the versus 20.5%). Subjects with a BoP ≥3 mm and ≥5 mm. The extent of predictors age, gender, attending ≥25% presented significantly CAL was defined as the percentage public or private school, smoking higher mean CAL (0.8 mm versus of sites/teeth, which had CAL status (smoker or no smoker), BoP 0.4 mm), PPD (2.3 mm versus ≥1 mm, ≥3 mm and ≥5 mm. The (<25% or ≥25%), PI (<30% or 1.7 mm) and PI (75.7% versus prevalence of PPD was defined as ≥30%) and cities on the occurrence 37.1%). Adolescents with PI ≥30% the percentage of subjects who had of at least one site with CAL had significantly higher mean CAL ≥1 site with PPD ≥4 mm. The extent ≥3 mm. First, an analysis using uni- (0.6 mm versus 0.3 mm), PPD of PPD was defined as the percent- variate models was performed. (2.0 mm versus 1.6 mm) and BoP age of sites/teeth, which had PPD Later, a multivariate analysis model (64.5% versus 14.1%) (Table 3). ≥4 mm. was constructed and only exposures Overall, 88.5% of the students Bleeding on probing and PI were showing in the univariable analyses examined had at least one site with presented as mean ( standard devia- associations with p ≤ 0.25 were CAL ≥1 mm. CAL ≥3 mm was seen tion). Also, PI wasÆ divided into included (Hosmer & Lemeshow in 32.6% and CAL ≥5 mm was <30% and ≥30%, the BoP into 2000). found in 4.5%. 34.3% of sites and <25% and ≥25%. Those thresholds A 95% level of confidence was 57.7% of teeth were affected by were selected because patients with considered as representing statistical CAL ≥1 mm. The percentage of sites mean PI ≥30% and BoP ≥25% significance (p < 0.05). The statistical that had CAL ≥3 mm was 3.1% and should be considered to be at high analysis was performed using Micro- the percentage of teeth was 9.1%. Ò Ò risk for periodontal breakdown soft Excel 2011 and the Stata 11 The extent of CAL ≥5 mm was © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Clinical attachment loss in adolescents 903

0.08% of sites and 0.4% of teeth.

1.5 1.1 Females had a significantly higher

Æ Æ prevalence of CAL ≥3 mm (35.8% versus 29.1%) and ≥5 mm (5.7% versus 3.1%), extent of CAL ≥3 mm (4.0% versus 2.0% sites; 11.3% versus 6.8% teeth affected) and

1.6 16.4 1.2 27.5 ≥5 mm (0.1% versus 0.03% sites;

Æ Æ 0.5% versus 0.2% teeth affected) Quito,

Ecuador (Table 2). The prevalence of PPD ≥4 mm was 59.3%. Four point one percent of sites and 11.0% of teeth were ın, 

1.1 16.5 1.1 27.5 affected by PPD ≥4 mm (Table 2).

Æ Æ The prevalence of BoP ≥25% was

Medell 28.6%, and it was higher in females Colombia (34.1% versus 22.7%) (Table 2). The prevalence of PI ≥30% was 67.6%, and it was higher in females (69.2%

1.4 16.1 1.2 27.6 versus 65.8%) (Table 2).

Æ Æ Clinical attachment loss ≥3 mm Chile

Santiago, in ≥1 sites was significantly more prevalent in women (35.8% versus 29.1%), in public high school students (35.9% versus 28.9%), in smokers (40% versus 29.8%), in 0.9 16.9 1.4 27.3

Æ Æ those with a BoP ≥25% (57.8%

Uruguay versus 22.5%), a PI ≥30% (39.4%

Montevideo, versus 18.4%) (Table 4). City, Country Total The adjusted logistic regression analysis revealed that smoking (OR = 1.6), attending public school 1.5 16.3 1.0 27.1

Æ Æ (OR = 2.3), having a BoP ≥25% (OR = 4.2) and living in Santiago de Mendoza, Argentina Chile, Chile (OR = 9.5), Buenos Aires, Argentina (OR = 3.3) and in Quito, Ecuador (OR = 520.2) were statistically significantly positively 1.6 16.2 0.7 27.6 associated with having at least one Æ Æ  ordoba, site with CAL ≥3 mm (Table 5). The C Argentina validity of final model was 0.000 and the goodness was 0.3489. standard deviations (SD). Discussion Æ 1.1 15.6 1.2 27.9

Æ Æ The prevalence of CAL in 15- to 19-

Argentina year-old high school from Latin Buenos Aires, America is consistent with other studies. In this study, the prevalence of CAL ≥1 mm was 88.5%, CAL ≥3 mm was 32.6% and CAL ≥5 mm was 4.5%. The prevalence of CAL ≥1 mm was 69.2% in Santiago de Chile, Chile and 49.5% in Santo Domingo, Dominican Republic. The prevalence of CAL ≥3 mm was 4.5% in adolescents in Santiago de Chile, Chile, 4% in Santo Domingo, Dominican Republic, 22.3% in

Characteristics of study subjects with Porto Alegre, Brazil and 100% in Cajaiba, Brazil. The prevalence of CAL ≥5 mm was 7.4% in Porto Ale- Sample sizeNumber of subjects invitedNet to sample participate sizeAge, yearsMale gender 139Current smokersSubjects attend public schoolTooth count* 173 128 73 (12.4%) (57.0%) 128 (12.0%) 117 169 26 (16.4%) 16.3 (20.3%) 57 97 169 (44.5%) (57.4%) (15.8%) 113 (10.9%) 27.4 113 99 25 (10.6%) (87.6%) (14.8%) 75 (44.4%) 42 42 (4.1%) 42 (4%) 10 24 (23.8%) (21.2%) 63 (55.8%) 294 (28.5%) 5 78 (11.9%) (23.5%) 332 19 (31.0%) (45.2%) 430 142 (13.8%) 127 142 (89.4%) (13.3%) 159 167 (47.9%) (50.3%) 144 (14.0%) 75 144 (52.1%) (13.5%) 17 84 (12.0%) (59.1%) 1032 (100%) 189 1070 (100%) 559 (52.2%) 38 50 (26.4%) (34.7%) 294 515 (27.5%) (48.1%) 144 1234 Table 1. Data are presented as*Excluding numbers third (percentages) molars. or means gre, Brazil and 7.7% in Cajaiba, © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 904 Morales et al.

Table 2. Prevalence of at least one affected site and extent (proportion) of affected sites et al., which tended to underestimate and teeth per mouth by degree of CAL (cut-offs ≥1, ≥3 and ≥5 mm), PPD (cut-off ≥4 mm), the CAL prevalence rates in both BoP (cut-off ≥25%), PI (cut-off ≥30%) and mean in total, gingival biotype and tooth count adolescents and adults (Susin et al. according to gender 2005, Peres et al. 2012). Addition- Age groups (15–19 years) ally, the studies performed in Porto Alegre (Brazil) and Santiago (Chile) Female Male Total rounded measurements to the next- (n = 555) (n = 515) (n = 1070) lowest millimetre, contrary with our study, where the closest millimetre CAL measures Prevalence CAL ≥ 1 mm 87.2 (0.01) 89.9 (0.01) 88.5 (0.009) was considered during rounding. In Prevalence CAL ≥ 3 mm 35.8 (0.02)* 29.1 (0.02)* 32.6 (0.01) Cajaiba (Brazil), the study consisted Prevalence CAL ≥ 5 mm 5.7 (0.009)† 3.1 (0.007)† 4.5 (0.006) of a rural population; in contrast, Proportion of sites/mouth CAL ≥ 1 mm (%) 36.5 (1.4) 31.9 (1.4) 34.3 (1.0) ours was based on an urban popula- Proportion of sites/mouth CAL ≥ 3 mm (%) 4.0 (0.5)† 2.0 (0.3)† 3.1 (0.3) tion. Proportion of sites/mouth CAL ≥ 5 mm (%) 0.1 (0.05)† 0.03 (0.01)† 0.08 (0.02) As described in the literature, Proportion of teeth/mouth CAL ≥ 1 mm (%) 59.1 (1.7) 56.3 (1.7) 57.7 (1.2) adults men have a higher probability Proportion of teeth/mouth CAL ≥ 3 mm (%) 11.3 (1.0)† 6.8 (0.8)† 9.1 (0.6) † † of CAL (Kocher et al. 2005, Shiau Proportion of teeth/mouth CAL ≥ 5 mm (%) 0.5 (0.1) 0.2 (0.07) 0.4 (0.08) & Reynolds 2010). The literature is Mean CAL (mm) 0.5 (0.03) 0.4 (0.02) 0.5 (0.02) inconclusive regarding data in ado- PPD measures Prevalence PPD ≥ 4 mm 58.9 (0.02) 59.6 (0.02) 59.3 (0.02) lescents (Botero et al. 2015). In this Proportion of sites/mouth PPD ≥ 4 mm (%) 4.6 (0.4) 3.5 (0.3) 4.1 (0.4) study, we observed that females had Proportion of teeth/mouth PPD ≥ 4 mm (%) 15.1 (0.9) 11.9 (0.9) 13.6 (0.6) higher means PPD, BoP and PI. Mean PPD (mm) 1.9 (0.02)† 1.8 (0.02)† 1.9 (0.01) Also, they had a higher prevalence BoP measures and extent of CAL ≥3 and ≥5 mm, Prevalence BoP ≥ 25% 189 (34.1)‡ 117 (22.7)‡ 306 (28.6) prevalence of BoP ≥25% and PI Mean BoP (%) 22.9 (24.7)† 16.8 (22.9)† 19.9 (24.1) ≥30%. Hormonal, genetic and envi- PI measures ronmental factors may contribute to Prevalence PI ≥ 30% 384 (69.2) 339 (65.8) 723 (67.6) this difference (Ghazeeri et al. 2011). Mean PI (%) 50.0 (30.7)† 46.1 (29.3)† 48.1 (30.1) Tooth count 27.4 (1.1) 27.5 (1.1) 27.5 (1.1) Socioeconomic status has been proposed as a CAL risk indicator BoP, Bleeding on probing; CAL, Clinical attachment loss; PI, plaque index; PPD, pocket (Lopez et al. 2006, Borrell & Craw- probing depth. CAL measures and PPD measures are presented as percentage (standard ford 2012). School was used as a error [SE]) or means (SE). BoP measures, PI measures are presented as number of subjects proxy for socioeconomic position (percentage) or mean (standard deviation [SD]). Tooth count (excluding third molars) is (Lopez & Baelum 2007). In this presented as mean (SD). study, adolescents from public high *Student test. †Mann–Whitney U-test. schools had a higher mean CAL, ‡Fisher’s exact test, p < 0.05. PPD, BoP and PI. Also, they pre- sented a higher prevalence of CAL ≥3 mm compared to private high school students (35.9% versus Table 3. Clinical characteristics of study subjects with periodontal examination according 28.9%). These results are consistent to the demographics, school, behavioural and clinical variables with the literature. In Santiago de Variables Categories Mean CAL Mean PPD Mean BoP Mean Chile, Chile, the prevalence of CAL (mm) (mm) (%) PI (%) ≥3 mm was higher in adolescents in public schools than in private Gender Female 0.5 (0.03) 1.9 (0.02)* 22.9 (24.7)* 50.0 (30.7)* schools (5.1% versus 3.3%) (Lopez Male 0.4 (0.02) 1.8 (0.02)* 16.8 (22.9)* 46.1 (29.3)* et al. 2001). In Porto Alegre (Brazil), School Private 0.5 (0.02)* 1.8 (0.02)* 14.1 (18.0)* 43.0 (26.5)* adolescents from a low socioeco- Public 0.4 (0.03)* 2.0 (0.02)* 25.3 (27.5)* 52.9 (32.3)* Smoking No 0.5 (0.02)* 1.9 (0.02)* 20.5 (24.3)* 48.7 (30.9) nomic level had a higher prevalence Yes 0.6 (0.02)* 1.8 (0.03)* 18.4 (23.5)* 46.6 (27.7) of CAL ≥3 mm in interproximal BoP <25% sites 0.4 (0.02)* 1.7 (0.01)* 7.3 (6.8)* 37.1 (26.1)* sites of ≥2 teeth compared with those ≥25% sites 0.8 (0.04)* 2.3 (0.03)* 51.6 (22.5)* 75.7 (20.1)* from middle and upper socioeco- PI <30% sites 0.3 (0.02)* 1.6 (0.02)* 4.8 (6.6)* 14.1 (9.0)* nomic levels (56.7% versus 34.7%) ≥30% sites 0.6 (0.03)* 2.0 (0.02)* 27.2 (25.9)* 64.5 (21.9)* (Susin et al. 2011). In the same pop- Total 0.5 (0.02) 1.9 (0.01) 19.9 (24.1) 48.1 (30.1) ulation, adolescents from low socioe- BoP, Bleeding on probing; CAL, Clinical attachment loss; PPD, pocket probing depth; PI, conomic levels had a higher plaque index. CAL measures and PPD measures are presented as means (standard eror prevalence of CAL ≥4 mm in ≥4 [SE]). BoP measures, PI measures are presented as mean (standard deviation [SD]). teeth in 14- to 19-year-old adoles- *Mann–Whitney U-test, p < 0.05 cents and CAL ≥5 mm in ≥ 4 teeth in 20- to 29-year-old young adults Brazil (Lopez et al. 2001, Collins between studies might be due to par- when compared with middle and et al. 2005, Corraini et al. 2008, tial recording protocols used in the high socioeconomic levels (9.4% Susin et al. 2011). The differences studies of Lopez et al. and Collins versus 2.8%) (Susin & Albandar © 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Clinical attachment loss in adolescents 905

2005). In the study from Lopez et al. Chile: 72.3% versus 22.8%; Porto opment of periodontal disease (Loe (2006) performed with adolescents Alegre: 30.4% versus 24.5%) (Lopez et al. 1965). A PI between 20% and from Santiago de Chile, a possible et al. 2001, Susin et al. 2011). The 40% can be tolerated in a majority explanation for the impact of socioe- absence of BoP is an excellent pre- of subjects (Lang & Tonetti 2003). conomic variables for CAL may be dictor for periodontal stability (Lang Plaque has been associated with a related to a higher education among et al. 1990, Griffiths et al. 2001), higher risk of CAL in adolescents parents which either reduce exposure with a score of <25% considered a and adults in some longitudinal to harmful factors and/or reinforce good predictor of a stable condition studies (Albandar et al. 1998, Tim- protective health behaviours (Lopez (Lang & Tonetti 2003). The results merman et al. 2000, Schatzle et al. et al. 2006). of this study are consistent with lit- 2003). In Cajaiba, Brazil a 73.2% Bleeding on probing is an indica- erature showing less periodontal prevalence of CAL ≥5 mm in ≥1 tor for gingival inflammation that destruction in adolescents with lower sites was observed when presenting suggests its pivotal role in CAL initi- BoP. Thus, adolescents with BoP PI ≥75% (Corraini et al. 2008). In ation in adolescents and adults <25% showed a lower mean CAL, Porto Alegre, Brazil there was a (Suda et al. 2000, Schatzle et al. PPD and PI. The prevalence of CAL higher prevalence of CAL ≥3 mm in 2003). The adolescents of Santiago ≥3 mm was lower (22.5% versus interproximal sites of ≥2 sites in sub- de Chile and Porto Alegre, Brazil, 57.8%). jects with PI ≥10% (55.5% versus with CAL ≥3 mm in ≥2 teeth had Bacterial plaque is considered the 28.6%) (Susin et al. 2011). In this more sites with BoP (Santiago de main etiological factor in the devel- study, PI ≥30% was associated with higher mean CAL, PPD and BoP and with a higher prevalence of CAL ≥3 mm in ≥1 sites (39.4% ver- Table 4. Prevalence of CAL ≥ 3 mm in at least 1 site according to the demographics, sus 18.4%) when compared to PI school, behavioural and clinical variables <30%. Variables Categories Prevalence CAL ≥ 3 mm ≥ 1 site The adjusted logistic regression analysis revealed that smoking n % p-Value (OR = 1.6), attending public school (OR = 2.3), having a BoP Gender Female 199 35.8 0.022* Male 150 29.1 ≥25% (OR = 4.2) and living in San- School Private 148 28.9 0.016* tiago de Chile, Chile (OR = 9.5), Public 201 35.9 Buenos Aires, Argentina (OR = 3.3) Smoking No 233 29.8 0.002* and in Quito, Ecuador (OR = 520.2) Yes 116 40 were significantly positively associ- Bleeding on probing <25% sites 172 22.5 0.001* ated with at least one site with CAL ≥25% sites 177 57.8 ≥3 mm. The results of this study are Plaque index <30% sites 64 18.4 0.001* consistent with literature. The role of ≥30% sites 285 39.4 smoking as a risk factor for peri- Total 349 32.6 odontitis in adults is well established CAL, clinical attachment loss. (Genco & Borgnakke 2013), how- *Fisher’s exact test, p < 0.05. ever, limited data are available for

Table 5. Univariable and multivariate logistic regression analysis of the effect of demographics, school, behavioural factor and clinical vari- ables on the prescence of CAL ≥ 3 mm in at least 1 site (n = 349) Variable Categories Univariable Multivariable analysis analysis Full model Reduced final model

OR p-Value OR p-Value OR p-Value

Gender (reference = Female) Male 0.7 0.019 1 0.965 –– Age (years) 1.1 0.002 1.1 0.388 –– Smoking (reference = No) Yes 1.6 0.002 1.6 0.017 1.6 0.009 School (reference = Private) 1.4 0.015 2.3 0.001 2.3 0.001 BOP (reference =<25%) ≥25% 4.7 0.001 4.4 0.001 4.2 0.001 PI (reference =<30%) ≥30% 2.9 0.001 0.9 0.743 –– Santiago de Chile, Chile (reference = Mendoza, Argentina) 4.3 0.001 9.4 0.001 9.5 0.001 Buenos Aires, Argentina (reference = Mendoza, Argentina) 3.9 0.001 3.3 0.002 3.3 0.003 Cordoba, Argentina (reference = Mendoza, Argentina) 1.2 0.581 –– –– Medellın, Colombia (reference = Mendoza, Argentina) 2.1 0.057 –– –– Montevideo, Uruguay (reference = Mendoza, Argentina) 1.9 0.236 –– –– Quito, Ecuador (reference = Mendoza, Argentina) 435.8 0.001 531.5 0.001 520.2 0.001

BoP, bleeding on probing; CAL, clinical attachment loss; PI, plaque index; OR, Odds ratio.

© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 906 Morales et al. adolescents. In Chile, there was no Acknowledgements of the current literature. Current Oral Health association between CAL and smok- Reports 1, 251–261. We thank the University leadership Hoover, J. N., Ellegaard, B. & Attstrom, R. ing (Lopez et al. 2001). In Porto and educational institutions for their (1981) Periodontal status of 14-16 year-old Alegre, Brazil, smoking was posi- support of this study. Danish schoolchildren. Scandinavian Journal of tively associated with CAL ≥3 mm Dental Research 89, 175–179. in ≥2 teeth (OR = 1.7) (Susin et al. Hosmer, D. W. & Lemeshow, S. J. (2000) Applied Logistic Regression, 2nd edition, pp. 260–287. 2011) and with CAL ≥4 mm in ≥4 References New York: John Wiley & Sons. teeth (OR = 3.1) (Susin & Albandar Kocher, T., Schwahn, C., Gesch, D., Bernhardt, 2005). As mentioned above, socioe- Albandar, J. M., Brown, L. J. & Loe, H. 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Clinical Relevance Principal findings: Periodontal Practical implications: Health pro- Scientific rationale for the study: destruction was prevalent in Latin motion and prevention programs Few studies have been performed America adolescents and is associ- in the Latin America must focus in Latin America adolescents on ated to smoking, socioeconomic on adolescents and reducing risk prevalence and risk indicators, and level, bleeding on probing index factors, thus preventing future peri- those existing are difficult to com- where adolescent is from. odontal destruction. pare.

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