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Risk of Periodontitis in Adolescents with Attention Deficit Hyperactivity Disorder: A Cohort Study of 81,055 Participants

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Title: Risk of Periodontitis in Adolescents with Attention Deficit Hyperactivity Disorder: A Cohort Study of 81,055 Participants
Language: English
Authors: Ju-Wei Hsu, Li-Chi Chen, Kai-Lin Huang, Shih-Jen Tsai, Ya-Mei Bai, Tung-Ping Su, Tzeng-Ji Chen, Wen-Liang Lo, Mu-Hong Chen (ORCID 0000-0001-6516-1073)
Source: Journal of Attention Disorders. 2024 28(14):1726-1733.
Availability: SAGE Publications. 2455 Teller Road, Thousand Oaks, CA 91320. Tel: 800-818-7243; Tel: 805-499-9774; Fax: 800-583-2665; e-mail: journals@sagepub.com; Web site: https://sagepub.com
Peer Reviewed: Y
Page Count: 8
Publication Date: 2024
Document Type: Journal Articles
Reports - Research
Descriptors: Dental Health, Adolescents, Attention Deficit Hyperactivity Disorder, Hygiene, Drug Therapy, Foreign Countries, Comorbidity, Health Behavior
Geographic Terms: Taiwan
DOI: 10.1177/10870547241273093
ISSN: 1087-0547
1557-1246
Abstract: Objectives: Previous studies have demonstrated poor oral hygiene in children with attention deficit hyperactivity disorder (ADHD). However, the association between ADHD and periodontitis is still unclear. Methods: In all, 16,211 adolescents with ADHD and 162,110 age- and sex-matched controls participated in the study between 2001 and 2011. To identify the occurrence of periodontitis, the participants were followed up till the end of 2011. Confounding factors, including smoking, diabetes, and depressive disorder, were assessed and adjusted in the Cox regression models. Results: Adolescents with ADHD (HR: 2.29) were more likely to develop periodontitis later in life than controls. We additionally observed the beneficial effect of atomoxetine (HR: 0.42) on the periodontitis risk among adolescents with ADHD. However, this finding should be interpreted cautiously given the small sample (n = 290) of children taking atomoxetine in the present study. Conclusions: ADHD is an independent risk factor for subsequent periodontitis development. Oral health should be closely monitored in adolescents with ADHD. Future investigation of the shared pathomechanisms between periodontitis and ADHD is warranted.
Abstractor: As Provided
Entry Date: 2024
Accession Number: EJ1447284
Database: ERIC
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  Value: <anid>AN0180676626;gs001dec.24;2024Nov07.04:26;v2.2.500</anid> <title id="AN0180676626-1">Risk of Periodontitis in Adolescents With Attention Deficit Hyperactivity Disorder: A Cohort Study of 81,055 Participants </title> <p>Objectives: Previous studies have demonstrated poor oral hygiene in children with attention deficit hyperactivity disorder (ADHD). However, the association between ADHD and periodontitis is still unclear. Methods: In all, 16,211 adolescents with ADHD and 162,110 age- and sex-matched controls participated in the study between 2001 and 2011. To identify the occurrence of periodontitis, the participants were followed up till the end of 2011. Confounding factors, including smoking, diabetes, and depressive disorder, were assessed and adjusted in the Cox regression models. Results: Adolescents with ADHD (HR : 2.29) were more likely to develop periodontitis later in life than controls. We additionally observed the beneficial effect of atomoxetine (HR : 0.42) on the periodontitis risk among adolescents with ADHD. However, this finding should be interpreted cautiously given the small sample (n = 290) of children taking atomoxetine in the present study. Conclusions: ADHD is an independent risk factor for subsequent periodontitis development. Oral health should be closely monitored in adolescents with ADHD. Future investigation of the shared pathomechanisms between periodontitis and ADHD is warranted.</p> <p>Keywords: Taiwan National Health Insurance Research Database; epidemiology; oral health; ADHD medication; protective effect; risk</p> <hd id="AN0180676626-2">Clinical Significance</hd> <p>Adolescents with ADHD are at a higher risk of developing periodontitis than the controls without ADHD. Optimal intervention, particularly atomoxetine treatment, for ADHD may reduce this risk.</p> <hd id="AN0180676626-3">Introduction</hd> <p>Periodontitis leads to the destruction of the supporting structures of teeth, thereby causing tooth loss, and it may further contribute to systemic inflammation. It predominantly affects adults but is also common among adolescents ([<reflink idref="bib17" id="ref1">17</reflink>]; [<reflink idref="bib21" id="ref2">21</reflink>]; [<reflink idref="bib22" id="ref3">22</reflink>]). Studies have estimated the prevalence of periodontitis to be between 20% and 50%, which indicates that periodontitis is a public health concern ([<reflink idref="bib17" id="ref4">17</reflink>]; [<reflink idref="bib21" id="ref5">21</reflink>]; [<reflink idref="bib22" id="ref6">22</reflink>]). Multiple genetic and environmental factors (e.g., smoking and diabetes) act together to induce a susceptibility to periodontitis ([<reflink idref="bib17" id="ref7">17</reflink>]; [<reflink idref="bib21" id="ref8">21</reflink>]; [<reflink idref="bib22" id="ref9">22</reflink>]). In a 40-year follow-up study, the average tooth-loss number associated with periodontitis was 13 ([<reflink idref="bib22" id="ref10">22</reflink>]). Clinicians have highlighted the importance of the early treatment of periodontitis in individuals aged less than 30 ([<reflink idref="bib17" id="ref11">17</reflink>]; [<reflink idref="bib21" id="ref12">21</reflink>]; [<reflink idref="bib22" id="ref13">22</reflink>]).</p> <p>Evidence suggested an association between attention deficit hyperactivity disorder (ADHD) and poor oral hygiene ([<reflink idref="bib5" id="ref14">5</reflink>]; [<reflink idref="bib15" id="ref15">15</reflink>]). A small sample-size study of 21 young adolescents with ADHD and 79 healthy controls found that 48% and 48% in the ADHD group brushed their teeth every morning and evening compared with 75% and 82% in the control group, respectively ([<reflink idref="bib5" id="ref16">5</reflink>]). [<reflink idref="bib15" id="ref17">15</reflink>] demonstrated that the most frequent psychiatric complaints from parents of children aged 8 and 17 receiving orthodontic treatment were inattention (25%), opposition (14.8%), and hyperactivity (12.5%), which may suggest the potential roles of inattention (i.e., forgetfulness) and hyperactivity and impulsivity (i.e., rushing) symptoms on oral hygiene and related behaviors. Few studies have investigated the association between ADHD and periodontitis ([<reflink idref="bib1" id="ref18">1</reflink>]; [<reflink idref="bib2" id="ref19">2</reflink>]; [<reflink idref="bib3" id="ref20">3</reflink>]; [<reflink idref="bib5" id="ref21">5</reflink>], [<reflink idref="bib4" id="ref22">4</reflink>]). [<reflink idref="bib3" id="ref23">3</reflink>] assessed the dental records of 25 children with ADHD and 127 controls and discovered that the prevalence of toothache and bleeding gums in children with ADHD was statistically more significant than in controls. [<reflink idref="bib4" id="ref24">4</reflink>] reported that adolescents with ADHD are more likely to have caries and bleeding gums than those without ADHD. They further discovered that children with ADHD exhibited poorer oral health behaviors, such as not brushing teeth every morning, than those in the control group ([<reflink idref="bib5" id="ref25">5</reflink>]). Comparing the oral health conditions between 51 children and adolescents with ADHD and 50 without ADHD, [<reflink idref="bib2" id="ref26">2</reflink>] demonstrated that the individuals with ADHD exhibited worse oral health conditions and oral hygiene than the controls without ADHD. [<reflink idref="bib1" id="ref27">1</reflink>] examined oral health related behaviors in relation to depression and ADHD and demonstrated that depression and ADHD were associated with missing teeth and poor periodontal health. Surprisingly, they did not observe any association of ADHD and depression with decayed teeth or toothbrushing frequency ([<reflink idref="bib1" id="ref28">1</reflink>]). However, the aforementioned studies were limited by small sample sizes. Moreover, few studies have focused on the association between ADHD and periodontitis.</p> <p>In the current study, we investigated the risk of periodontitis in adolescents with ADHD using data from the Taiwan National Health Insurance Research Database (NHIRD); this study had a large sample size and a longitudinal follow-up design. Further, we clarified the effects of ADHD medications on the susceptibility to periodontitis. We hypothesized that adolescents with ADHD are more likely to develop periodontitis later in life than controls. In addition, we also hypothesized that ADHD medications may reduce the risk of periodontitis in adolescents with ADHD.</p> <hd id="AN0180676626-4">Methods</hd> <p></p> <hd id="AN0180676626-5">Data Source</hd> <p>Taiwan's National Health Insurance (NHI) is a mandatory universal health insurance program that is implemented in 1995 and offers comprehensive medical care coverage to all Taiwanese residents. The National Health Research Institute (NHRI) is in charge of the entire insurance claims database, namely the NHIRD, which consists of healthcare data from up to 99.7% of the entire Taiwan population (~28,000,000). The NHRI audits and releases the NHIRD for scientific and study purposes. The NHIRD can be accessed through a formal application that is regulated by the Health and Welfare Data Science Center of Ministry of Health and Welfare, Taiwan (https://<ulink href="http://www.apre.mohw.gov.tw/">www.apre.mohw.gov.tw/</ulink>). In current study, we linked two databases together for the analysis. The first is the specialized dataset of mental disorders, which include all medical (mental and non-mental) records of all insured individuals with mental disorders. The second is the Longitudinal Health Insurance Database, which includes all medical records of 3,000,000 insured individuals that are randomly selected from entire Taiwanese people (~28,000,000), and was used for the identification of control groups in current study. Those two databases contain comprehensive medical information about the insured patients, such as demographics (birthdate, sex, residential location), clinical visits (dates and diagnoses), and prescriptions. Individual medical records included in the NHIRD are anonymous to protect personal privacy. The diagnostic codes used were based on the International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM). The NHIRD has been used extensively in many epidemiologic studies in Taiwan ([<reflink idref="bib9" id="ref29">9</reflink>], [<reflink idref="bib8" id="ref30">8</reflink>]; [<reflink idref="bib10" id="ref31">10</reflink>]; [<reflink idref="bib18" id="ref32">18</reflink>]; [<reflink idref="bib26" id="ref33">26</reflink>]). Institutional review board of our Hospital approved the study protocol and waived the requirement for informed consent since this investigation used de-identified data and no human subjects contact was required.</p> <hd id="AN0180676626-6">Study and Control Groups</hd> <p>Adolescents aged 12 to 19 years who had a psychiatrist-diagnosed ADHD (ICD-9-CM codes: 314) and had no prior history of any periodontitis (ICD-9-CM codes: 523.3, 523.4, 523.5) were identified between 2001 and 2011 as the ADHD group. Furthermore, ADHD presentations were classified based on ICD-9-CM codes: combined presentation (314.01), predominantly inattentive presentation (314.00), and predominantly hyperactive presentation (314.1, 314.2, 314.8, and 314.9). The time of ADHD diagnosis was defined as the time of enrollment. Exact matching was used to match this cohort in a 1:4 fashion to controls without diagnoses of neither ADHD nor periodontitis prior to the enrollment on the bases of age (±1 year)-, sex-, enrollment time, family income-, residence (a proxy for healthcare availability in Taiwan), and comorbidities (obesity, diabetes mellitus, smoking, bipolar disorder, major depressive disorder, and alcohol and substance use disorders) ([<reflink idref="bib19" id="ref34">19</reflink>]).</p> <hd id="AN0180676626-7">Outcome and Confounder Assessment</hd> <p>Diagnosis of periodontitis given by board-certified dentists was identified during the follow-up (from enrollment to December 31 2011 or to the death). In order to improve the diagnostic validity of periodontitis, Taiwanese procedure codes of periodontitis-related treatment were used, including scaling (91003C, 91004C, 91005C, 91006C, 91017C, 91089C, 91090C, 91103C, 91104C), root planing (91006C, 91007C, 91008C, 91008CB, P35912, P35913, P35914), and flap surgery and others (91001C, 91002C, 91009B, 91010B, 91014C, 91015C, 91016C, 91018C, 91019C, 91021C, 91022C, 91023C, 91114C, P35911, P4001C, P4002C, P4003C). Medical and mental comorbidities, including gingivitis, obesity, diabetes mellitus, smoking, autism spectrum disorder (ASD), bipolar disorder, major depressive disorder, and alcohol and substance use disorders, were assessed as the confounding factors in our study. Additionally, Charlson Comorbidity Index (CCI) and all-cause clinical visits were examined for the ADHD and the matched-control cohorts. CCI consisting of 22 physical conditions was also assessed to determine the systemic health conditions of all enrolled subjects ([<reflink idref="bib6" id="ref35">6</reflink>]). In order to avoid the double adjustment of diabetes mellitus in the CCI, diabetes mellitus was not counted in the CCI in present study. All-cause clinical visits (the numbers of clinical visits per year) were included as a variable to account for potential detection bias. Furthermore, the use of ADHD medications (methylphenidate and atomoxetine) during the follow-up was also examined, and divided into three subgroups: non-users (cumulative defined daily dose [cDDD] during the follow-up <30), short-term users (cDDD = 30–364), and long-term users (cDDD ≥ 365). Income level (levels 1–3 per month: ≤19,000 NTD [New Taiwanese Dollars], 19,001 to 42,000 NTD and ≥42,001 NTD) and urbanization level of residence (levels 1–5, most to least urbanized) were regarded as the proxies for healthcare availability in Taiwan ([<reflink idref="bib19" id="ref36">19</reflink>]).</p> <hd id="AN0180676626-8">Statistical Analysis</hd> <p>Regarding between-group comparisons, the <emph>F</emph> test was used for continuous variables and Pearson's X<sups>2</sups> test for nominal variables, where appropriate. Cox regression models were used to investigate the hazard ratio (HR) with a 95% confidence interval (CI) of developing periodontitis during the follow-up after adjusting for demographic data (age, sex, level of urbanization, and income), medical and mental comorbidities (gingivitis, obesity, diabetes mellitus, smoking, ASD, bipolar disorder, major depressive disorder, and alcohol and substance use disorders), all-cause clinical visits and CCI scores between groups. Subanalyses stratified by sex and income were also assessed for the relationship between ADHD and periodontitis risk. Finally, we examined the relationship between ADHD medications and the periodontitis risk in adolescents with ADHD. A two-tailed <emph>p</emph>-value of less than.05 was considered statistically significant. All data processing and statistical analyses were performed with Statistical Package for Social Science (SPSS) version 17 software (SPSS Inc.) and Statistical Analysis Software (SAS) version 9.1 (SAS Institute, Cary, NC).</p> <hd id="AN0180676626-9">Data Availability Statement</hd> <p>The NHIRD was released and audited by the Department of Health and Bureau of the NHI Program for the purpose of scientific research (https://nhird.nhri.org.tw/). NHIRD can be obtained through the formal application that is regulated by Department of Health and Bureau of the NHI Program.</p> <hd id="AN0180676626-10">Results</hd> <p>A total of 16,211 adolescents with ADHD and 162,110 age- and sex-matched controls participated in the present study, with a male predominance (80.9% vs. 19.1%) and a mean age of 13 years (Table 1). The incidence of periodontitis later in life was higher in the adolescents with ADHD than in the controls (15.0% vs. 7.9%, <emph>p</emph> <.001), with an earlier periodontitis onset (16.39 ± 2.39 vs. 21.50 ± 2.86 years, <emph>p</emph> <.001; Table 1).</p> <p>Table 1. Demographic Characteristics and Incidence of Periodontitis Between Adolescents With ADHD and Control Group.</p> <p>Graph</p> <p> <ephtml> <table><colgroup><col align="left" /><col align="char" char="." /><col align="char" char="." /><col align="char" char="." /></colgroup><thead><tr><th /><th align="center">Adolescents with ADHD (<italic>n</italic> = 16,211)</th><th align="center">Control group (<italic>n</italic> = 64,844)</th><th align="center"><italic>p</italic>-value</th></tr></thead><tbody><tr><td>Age at enrollment (years, <italic>SD</italic>)</td><td>13.83 (1.56)</td><td>13.76 (2.39)</td><td>.627</td></tr><tr><td>Male (<italic>n</italic>, %)</td><td>13,121 (80.9)</td><td>52,484 (80.9)</td><td>>.999</td></tr><tr><td colspan="4">ADHD subtypes (<italic>n</italic>, %)</td></tr><tr><td> Combined presentation</td><td>7,673 (47.3)</td><td /><td /></tr><tr><td> Predominantly inattentive presentation</td><td>5,417 (33.4)</td><td /><td /></tr><tr><td> Predominantly hyperactive presentation</td><td>3,121 (19.3)</td><td /><td /></tr><tr><td colspan="4">Use of ADHD medications (<italic>n</italic>, %)</td></tr><tr><td> Non-user</td><td>6,415 (39.6)</td><td /><td /></tr><tr><td> Short-term user</td><td>7,441 (45.9)</td><td /><td /></tr><tr><td> Long-term user</td><td>2,355 (14.5)</td><td /><td /></tr><tr><td colspan="4">Use of methylphenidate (<italic>n</italic>, %)</td></tr><tr><td> Non-user</td><td>6,543 (40.4)</td><td /><td /></tr><tr><td> Short-term user</td><td>7,348 (45.3)</td><td /><td /></tr><tr><td> Long-term user</td><td>2,320 (14.3)</td><td /><td /></tr><tr><td colspan="4">Use of atomoxetin (<italic>n</italic>, %)</td></tr><tr><td> Non-user</td><td>15,921 (98.2)</td><td /><td /></tr><tr><td> Short-term user</td><td>276 (1.7)</td><td /><td /></tr><tr><td> Long-term user</td><td>14 (0.1)</td><td /><td /></tr><tr><td>ASD comorbidity (<italic>n</italic>, %)</td><td>916 (5.7)</td><td>105 (0.1)</td><td><.001</td></tr><tr><td colspan="4">Medical and mental comorbidities (<italic>n</italic>, %)</td></tr><tr><td> Diabetes mellitus</td><td>21 (0.1)</td><td>84 (0.1)</td><td>.991</td></tr><tr><td> Obesity</td><td>243 (1.5)</td><td>972 (1.5)</td><td>.997</td></tr><tr><td> Smoking</td><td>49 (0.3)</td><td>196 (0.3)</td><td>.994</td></tr><tr><td> Bipolar disorder</td><td>41 (0.3)</td><td>164 (0.3)</td><td>.993</td></tr><tr><td> Major depressive disorder</td><td>103 (0.6)</td><td>412 (0.6)</td><td>.996</td></tr><tr><td> Alcohol use disorder</td><td>38 (0.2)</td><td>152 (0.2)</td><td>.993</td></tr><tr><td> Substance use disorder</td><td>67 (0.4)</td><td>268 (0.4)</td><td>.995</td></tr><tr><td>Comorbidity of gingivitis (<italic>n</italic>, %)</td><td>4,447 (27.4)</td><td>9,785 (15.1)</td><td><.001</td></tr><tr><td>CCI score (<italic>SD</italic>)</td><td>0.43 (0.69)</td><td>0.33 (0.59)</td><td><.001</td></tr><tr><td>Incidence of periodontitis (<italic>n</italic>, %)</td><td>2,428 (15.0)</td><td>5,133 (7.9)</td><td><.001</td></tr><tr><td> Age at periodontitis diagnosis (years, <italic>SD</italic>)</td><td>16.39 (2.39)</td><td>21.50 (2.86)</td><td><.001</td></tr><tr><td> Duration between enrollment and diagnosis (years, <italic>SD</italic>)</td><td>2.33 (1.93)</td><td>5.25 (2.73)</td><td><.001</td></tr><tr><td>Level of urbanization (<italic>n</italic>, %)</td><td /><td /><td>>.999</td></tr><tr><td> 1 (most urbanized)</td><td>2,924 (18.0)</td><td>11,696 (18.0)</td><td /></tr><tr><td> 2</td><td>5,096 (31.4)</td><td>20,384 (31.4)</td><td /></tr><tr><td> 3</td><td>1,475 (9.1)</td><td>5,900 (9.1)</td><td /></tr><tr><td> 4</td><td>1,182 (7.3)</td><td>4,728 (7.3)</td><td /></tr><tr><td> 5 (most rural)</td><td>5,534 (34.2)</td><td>22,136 (34.2)</td><td /></tr><tr><td>Income-related insured amount (<italic>n</italic>, %)</td><td /><td /><td>>.999</td></tr><tr><td> ≤19,100 NTD/month</td><td>2,823 (17.4)</td><td>11,292 (17.4)</td><td /></tr><tr><td> 19,001–42,000 NTD/month</td><td>5,764 (35.6)</td><td>23,056 (35.6)</td><td /></tr><tr><td> >42,000 NTD/month</td><td>7,624 (47.0)</td><td>30,496 (47.0)</td><td /></tr><tr><td>All-cause clinical visits per year (<italic>SD</italic>)</td><td>19.55 (27.15)</td><td>13.57 (20.69)</td><td><.001</td></tr></tbody></table> </ephtml> </p> <p>1 <emph>Note</emph>. ADHD = Attention-deficit hyperactivity disorder; ASD = autism spectrum disorder; NTD = new Taiwan dollar; SD = standard deviation; CCI = Charlson Comorbidity Index.</p> <p>The Kaplan–Meier survival curve indicated that during follow-up, the adolescents with ADHD were at a significantly higher risk of developing periodontitis than the controls (<emph>p</emph> <.001; Figure 1). The Cox regression models adjusted for the demographic data and medical and mental comorbidities of the participants displayed that the adolescents with ADHD (<emph>HR</emph>: 2.29, 95% CI [2.17, 2.41]), including boys (<emph>HR</emph>: 2.29, 95% CI [2.16, 2.43]) and girls (<emph>HR</emph>: 2.11, 95% CI [1.90, 2.34]), were more likely to develop periodontitis during the follow-up than the controls (Table 2). Increased risk of periodontitis was noted across three ADHD presentation subtypes: combined presentation (<emph>HR</emph>: 2.69, 95% CI [2.52, 2.89]), predominantly inattentive presentation (<emph>HR</emph>: 2.23, 95% CI [2.05, 2.42]), and predominantly hyperactive presentation (<emph>HR</emph>: 2.07, 95% CI [1.90, 2.26]; Table 2). Income-stratified Cox regression models showed consistent findings that ADHD was associated with an elevated risk of developing periodontitis during the follow-up (Table 2). In addition, we found no associations of the exposure to overall ADHD medications and the exposure to methylphenidate with the risk of periodontitis in adolescents with ADHD (all <emph>p</emph> >.05; Table 3). Interestingly, we identified a beneficial effect of atomoxetine treatment (short-term use: <emph>HR</emph>: 0.42, 95% CI [0.35, 0.70]) on the periodontitis risk despite only about 2% of adolescents with ADHD who were treated with atomoxetine (Table 3). The mean cDDD of atomoxetine was 109.03 ± 78.26 in the short-term use group.</p> <p>Graph: Figure 1. The periodontitis risk between adolescents with ADHD and control group. Note. ADHD = Attention-deficit hyperactivity disorder.</p> <p>Table 2. Cox Regression Analyses of the Periodontitis Risk Between Adolescents With ADHD and Control Group.</p> <p>Graph</p> <p> <ephtml> <table><colgroup><col align="left" /><col align="char" char="." /><col align="char" char="." /></colgroup><thead><tr><th /><th align="center">Events (<italic>n</italic>, %)</th><th align="center">HR [95% CI]<xref ref-type="table-fn" rid="tfn3">a</xref></th></tr></thead><tbody><tr><td colspan="3">All sample</td></tr><tr><td> Control group</td><td>5,133 (7.9)</td><td>1 (ref)</td></tr><tr><td> Adolescents with ADHD</td><td>2,428 (15.0)</td><td><bold>2.29 [2.17, 2.41]</bold></td></tr><tr><td> Combined presentation</td><td>1,113 (14.5)</td><td><bold>2.69 [2.52, 2.89]</bold></td></tr><tr><td> Predominantly inattentive presentation</td><td>696 (12.8)</td><td><bold>2.23 [2.05, 2.42]</bold></td></tr><tr><td> Predominantly hyperactive presentation</td><td>619 (19.8)</td><td><bold>2.07 [1.90, 2.26]</bold></td></tr><tr><td colspan="3">Male sample</td></tr><tr><td> Control group</td><td>3,865 (7.4)</td><td>1 (ref)</td></tr><tr><td> Adolescents with ADHD</td><td>1,842 (14.0)</td><td><bold>2.29 [2.16, 2.43]</bold></td></tr><tr><td colspan="3">Female sample</td></tr><tr><td> Control group</td><td>1,268 (10.3)</td><td>1 (ref)</td></tr><tr><td> Adolescents with ADHD</td><td>586 (19.0)</td><td><bold>2.11 [1.90, 2.34]</bold></td></tr><tr><td colspan="3">Low-income sample</td></tr><tr><td> Control group</td><td>707 (6.3)</td><td>1 (ref)</td></tr><tr><td> Adolescents with ADHD</td><td>358 (12.7)</td><td><bold>2.22 [1.94, 2.55]</bold></td></tr><tr><td colspan="3">Middle-income sample</td></tr><tr><td> Control group</td><td>1,394 (6.0)</td><td>1 (ref)</td></tr><tr><td> Adolescents with ADHD</td><td>721 (12.5)</td><td><bold>2.36 [2.14, 2.59]</bold></td></tr><tr><td colspan="3">High-income sample</td></tr><tr><td> Control group</td><td>3,032 (9.9)</td><td>1 (ref)</td></tr><tr><td> Adolescents with ADHD</td><td>1,349 (17.7)</td><td><bold>2.12 [2.06, 2.31]</bold></td></tr></tbody></table> </ephtml> </p> <ulist> <item>2 <emph>Note</emph>. <bold>Bold</bold> type means the statistical significance. HR = Hazard ratio; CI = confidence interval; ADHD = Attention-deficit hyperactivity disorder.</item> <item>3 Adjusted for demographic data, comorbidities, all-cause clinical visits and CCI score.</item> </ulist> <p>Table 3. ADHD Medications and the Periodontitis Risk Among Adolescents With ADHD.</p> <p>Graph</p> <p> <ephtml> <table><colgroup><col align="left" /><col align="char" char="." /><col align="char" char="." /></colgroup><thead><tr><th /><th align="center">Events (<italic>n</italic>, %)</th><th align="center">HR [95% CI]<xref ref-type="table-fn" rid="tfn5">a</xref></th></tr></thead><tbody><tr><td colspan="3">ADHD medications</td></tr><tr><td> Non-use</td><td>993 (15.5)</td><td>1 (ref)</td></tr><tr><td> Short-term use</td><td>1,052 (14.1)</td><td>0.97 [0.89, 1.06]</td></tr><tr><td> Long-term use</td><td>383 (16.3)</td><td>0.99 [0.88, 1.12]</td></tr><tr><td colspan="3">Methylphenidate</td></tr><tr><td> Non-user</td><td>995 (15.2)</td><td>1 (ref)</td></tr><tr><td> Short-term user</td><td>1,052 (14.3)</td><td>1.00 [0.91, 1.09]</td></tr><tr><td> Long-term user</td><td>381 (16.4)</td><td>1.02 [0.90, 1.15]</td></tr><tr><td colspan="3">Atomoxetine</td></tr><tr><td> Non-user</td><td>2,412 (15.1)</td><td>1 (ref)</td></tr><tr><td> Short-term user</td><td>15 (5.4)</td><td><bold>0.42 [0.35, 0.70]</bold></td></tr><tr><td> Long-term user</td><td>1 (7.1)</td><td>0.29 [0.04, 2.07]</td></tr></tbody></table> </ephtml> </p> <ulist> <item>4 <emph>Note</emph>. <bold>Bold</bold> type means the statistical significance. HR = Hazard ratio; CI = confidence interval; ADHD = Attention-deficit hyperactivity disorder.</item> <item>5 Adjusted for demographic data, comorbidities, all-cause clinical visits and CCI score.</item> </ulist> <hd id="AN0180676626-11">Discussion</hd> <p>The results of this study partially support the hypotheses that during follow-up, the adolescents with ADHD are at a higher risk of developing periodontitis than the controls without ADHD after adjusting for modifiable risk factors, such as gingivitis, smoking, and diabetes. Increased periodontitis risk occurred across three ADHD presentation subgroups. Furthermore, we found that the use of atomoxetine, but not methylphenidate, may be associated with a reduced risk of developing periodontitis during the follow-up in the adolescents with ADHD.</p> <p>As discussed earlier in the text, poor oral hygiene and oral health behaviors may be the reason for the increased periodontitis risk in adolescents with ADHD, although previous results are inconsistent ([<reflink idref="bib1" id="ref37">1</reflink>]; [<reflink idref="bib2" id="ref38">2</reflink>]; [<reflink idref="bib3" id="ref39">3</reflink>]; [<reflink idref="bib5" id="ref40">5</reflink>], [<reflink idref="bib4" id="ref41">4</reflink>]). A study involving 25 children with ADHD and 127 non-ADHD controls did not report any differences in oral hygiene compliance, plaque accumulation, and gingival inflammation between the groups ([<reflink idref="bib3" id="ref42">3</reflink>]). A study involving 364 participants who were assessed for ADHD symptoms and oral health related behaviors reported no association between ADHD and decayed teeth or toothbrushing frequency ([<reflink idref="bib1" id="ref43">1</reflink>]). However, [<reflink idref="bib1" id="ref44">1</reflink>] suggested that the periodontal status of adolescents with ADHD was poorer than that of controls. A meta-analysis was performed with 27 studies that investigated oral health in children with ADHD; the results revealed that children with ADHD exhibit a tendency toward higher levels of gingival inflammation ([<reflink idref="bib7" id="ref45">7</reflink>]). Contrastingly, [<reflink idref="bib24" id="ref46">24</reflink>] evaluated the oral health condition according to the plaque index and the decayed, missing, and filled teeth index and reported that oral health was poorer in children with ADHD undergoing methylphenidate therapy than in those undergoing neuro-feedback therapy. The present study discovered that the risk of developing periodontitis during the follow-up period was higher in the adolescents with ADHD than in the controls without ADHD.</p> <p>It is possible that the finding of an association between atomoxetine and periodontitis risk represents a spurious finding owing to the small sample size of individuals with ADHD who were exposed to atomoxetine, so it should be interpreted cautiously. The pharmacodynamics and pharmacokinetics differed between psychostimulants (i.e., methylphenidate) and non-psychostimulants (i.e., atomoxetine), which may explain the different effects of methylphenidate and atomoxetine on the periodontitis risk ([<reflink idref="bib11" id="ref47">11</reflink>]). The medication effect of psychostimulants disappears in the evening and night and in the early morning, but the medication effect of non-psychostimulants still lasts in such time periods ([<reflink idref="bib25" id="ref48">25</reflink>]). Kelsey et al measured specific morning or evening activities, including settling at bedtime and getting ready in the morning among 197 children with ADHD, and found that the parent-rated evening and morning behaviors scored significantly higher in the atomoxetine group than in the control group ([<reflink idref="bib25" id="ref49">25</reflink>]). [<reflink idref="bib13" id="ref50">13</reflink>] reported that tooth brushing frequency was found to be significantly lower in children with externalizing symptoms, such as hyperactivity, impulsivity, and opposition, compared with the control peers. Those findings may suggest that the therapeutic effects of psychostimulants are not sustained long enough to maintain good oral health behaviors among children with ADHD. However, the therapeutic effects of non-psychostimulants persist throughout the day, which may improve the evening and morning behaviors, including tooth-brushing ([<reflink idref="bib13" id="ref51">13</reflink>]; [<reflink idref="bib25" id="ref52">25</reflink>]).</p> <p>Shared hyperinflammatory states, such as elevated levels of interleukin (IL)-6 and tumor necrosis factor (TNF)-α, may contribute to the comorbidity of ADHD and periodontitis ([<reflink idref="bib12" id="ref53">12</reflink>]; [<reflink idref="bib14" id="ref54">14</reflink>]; [<reflink idref="bib16" id="ref55">16</reflink>]; [<reflink idref="bib20" id="ref56">20</reflink>]; [<reflink idref="bib23" id="ref57">23</reflink>]). [<reflink idref="bib14" id="ref58">14</reflink>] measured the levels of serum IL-6 and TNF-α in 80 children with ADHD and reported that children with ADHD exhibited higher levels of serum IL-6 than controls. [<reflink idref="bib12" id="ref59">12</reflink>] demonstrated that drug-naïve children with ADHD exhibited higher IL-6 and IL-10 levels than controls. A meta-analysis was performed with 11 studies that assessed the levels of proinflammatory cytokines in patients with periodontitis; the results revealed increased concentrations of IL-6 and matrix metalloproteinase-8 in patients with periodontitis compared with those in controls ([<reflink idref="bib16" id="ref60">16</reflink>]). [<reflink idref="bib23" id="ref61">23</reflink>] suggested that the TNF-α rs1800629 polymorphism is related to the risk of periodontitis, particularly in individuals of Asian descent. However, the hypothesis on the influence of shared hyperinflammatory states did not explain any causal relationship between ADHD and periodontitis; this relationship requires further investigation.</p> <p>The limitations of this study are similar to those of other registry-based analyses. First, the prevalence of periodontitis may have been underestimated because only adolescents who sought dental consultation and treatment were included in the database. While board-certified dentists and psychiatrists made all diagnoses, it may be possible that errors in the diagnoses of periodontitis and ADHD remained. These errors could have led to differential misclassification of either periodontitis by ADHD status (or vice versa). Second, the present study was only conducted among the Taiwanese population, which may limit the generalization of our findings to other races and ethnicities. Third, the sample of our study was predominantly male (about 80% male). Despite the smaller number of females in the present study, the pattern of an association between ADHD and periodontitis risk was still consistent. Fourth, information regarding the lifestyle of the participants, for example, self-care, oral hygiene, diet, and family history, was unavailable in the database; thus, the effects of those factors could not be investigated. Third, despite findings emphasizing the strong unidirectional association between ADHD and subsequent periodontitis development, a causal relationship could not be inferred. Finally and importantly, the sample size of relevance for the atomoxetine effect on periodontitis risk is really small, which may bias our finding. A further study with a large sample of patients exposed to atomoxetine would be required to elucidate whether the protective effect of atomoxetine on periodontitis risk was real or spurious.</p> <p>In conclusion, the adolescents with ADHD exhibited an elevated risk of developing periodontitis later in life than the controls without ADHD after adjustment for periodontitis-related risk factors, including smoking, diabetes, and depressive disorder. ADHD is an independent risk factor for subsequent periodontitis development. If ADHD was to be demonstrated as a risk factor of periodontitis and ADHD medications may be a potential preventative approach against the periodontitis risk, it would have broad public health significance given the prevalence of ADHD. Future studies would be necessary to more carefully understand the role of ADHD and its treatments in the development of periodontitis.</p> <p>The authors thank Mr I-Fan Hu, MA (Courtauld Institute of Art, University of London; National Taiwan University) for his friendship and support. Mr Hu declares no conflicts of interest.</p> <ref id="AN0180676626-12"> <title> Footnotes </title> <blist> <bibl id="bib1" idref="ref18" type="bt">1</bibl> <bibtext> MHC, JWH, WLL, and LCC designed the study. LCC and MHC analyzed the data and drafted the first version of the manuscript. WLL critically reviewed the manuscript. SJT, YMB, KLH, TPS, and TJC performed literature search and reviewed the manuscript. All authors contributed substantially to the manuscript, and approved the final manuscript for submission. All authors are responsible for the integrity, accuracy and presentation of the data.</bibtext> </blist> <blist> <bibl id="bib2" idref="ref19" type="bt">2</bibl> <bibtext> The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.</bibtext> </blist> <blist> <bibl id="bib3" idref="ref20" type="bt">3</bibl> <bibtext> The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The study was supported by grant from Taipei Veterans General Hospital (V111C-010, V111C-040, V111C-029, V112C-033, V113C-010, V113C-011, V113C-039), Yen Tjing Ling Medical Foundation (CI-109-21, CI-109-22, CI-110-30, CI-113-30, CI-113-31, CI-113-32), Ministry of Science and Technology, Taiwan (MOST110-2314-B-075-026, MOST110-2314-B-075-024 -MY3, MOST 109-2314-B-010-050-MY3, MOST111-2314-B-075-014-MY2, MOST 111-2314-B-075 -013, NSTC111-2314-B-A49-089-MY2), Taipei, Taichung, Kaohsiung Veterans General Hospital, Tri-Service General Hospital, Academia Sinica Joint Research Program (VTA112-V1-6-1, VTA113-V1-5-1) and Veterans General Hospitals and University System of Taiwan Joint Research Program (VGHUST112-G1-8-1, VGHUST113-G1-8-1). 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Gut, 70(1), 85–91.</bibtext> </blist> </ref> <aug> <p>By Ju-Wei Hsu; Li-Chi Chen; Kai-Lin Huang; Shih-Jen Tsai; Ya-Mei Bai; Tung-Ping Su; Tzeng-Ji Chen; Wen-Liang Lo and Mu-Hong Chen</p> <p>Reported by Author; Author; Author; Author; Author; Author; Author; Author; Author</p> <p></p> <p>Ju-Wei Hsu is a child and adolescent psychiatrist in the Taipei Veterans General Hospital, Taiwan and an assistant professor in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Li-Chi Chen is a child and adolescent psychiatrist in the General Cheng Hsin Hospital, Taiwan and a lecturer in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Kai-Lin Huang is a child and adolescent psychiatrist in the Taipei Veterans General Hospital, Taiwan and an assistant professor in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Shih-Jen Tsai is an adult psychiatrist in the Taipei Veterans General Hospital, Taiwan and a full professor in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Ya-Mei Bai is an adult psychiatrist in the Taipei Veterans General Hospital, Taiwan and a full professor in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Tung-Ping Su is an adult psychiatrist in the General Cheng Hsin Hospital, Taiwan and an Emeritus professor in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Tzeng-Ji Chen is a Superintendent in the Taipei Veterans General Hospital, Hsinchu Branch, Taiwan and a full professor in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Wen-Liang Lo is a dentist and an oral surgeon in the Taipei Veterans General Hospital, Taiwan and a full professor in the National Yang Ming Chiao Tung University, Taiwan.</p> <p>Mu-Hong Chen is a child and adolescent psychiatrist in the Taipei Veterans General Hospital, Taiwan and an associate professor in the National Yang Ming Chiao Tung University, Taiwan.</p> </aug> <nolink nlid="nl1" bibid="bib17" firstref="ref1"></nolink> <nolink nlid="nl2" bibid="bib21" firstref="ref2"></nolink> <nolink nlid="nl3" bibid="bib22" firstref="ref3"></nolink> <nolink nlid="nl4" bibid="bib15" firstref="ref15"></nolink> <nolink nlid="nl5" bibid="bib10" firstref="ref31"></nolink> <nolink nlid="nl6" bibid="bib18" firstref="ref32"></nolink> <nolink nlid="nl7" bibid="bib26" firstref="ref33"></nolink> <nolink nlid="nl8" bibid="bib19" firstref="ref34"></nolink> <nolink nlid="nl9" bibid="bib24" firstref="ref46"></nolink> <nolink nlid="nl10" bibid="bib11" firstref="ref47"></nolink> <nolink nlid="nl11" bibid="bib25" firstref="ref48"></nolink> <nolink nlid="nl12" bibid="bib13" firstref="ref50"></nolink> <nolink nlid="nl13" bibid="bib12" firstref="ref53"></nolink> <nolink nlid="nl14" bibid="bib14" firstref="ref54"></nolink> <nolink nlid="nl15" bibid="bib16" firstref="ref55"></nolink> <nolink nlid="nl16" bibid="bib20" firstref="ref56"></nolink> <nolink nlid="nl17" bibid="bib23" firstref="ref57"></nolink>
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  Data: Risk of Periodontitis in Adolescents with Attention Deficit Hyperactivity Disorder: A Cohort Study of 81,055 Participants
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  Data: <searchLink fieldCode="AR" term="%22Ju-Wei+Hsu%22">Ju-Wei Hsu</searchLink><br /><searchLink fieldCode="AR" term="%22Li-Chi+Chen%22">Li-Chi Chen</searchLink><br /><searchLink fieldCode="AR" term="%22Kai-Lin+Huang%22">Kai-Lin Huang</searchLink><br /><searchLink fieldCode="AR" term="%22Shih-Jen+Tsai%22">Shih-Jen Tsai</searchLink><br /><searchLink fieldCode="AR" term="%22Ya-Mei+Bai%22">Ya-Mei Bai</searchLink><br /><searchLink fieldCode="AR" term="%22Tung-Ping+Su%22">Tung-Ping Su</searchLink><br /><searchLink fieldCode="AR" term="%22Tzeng-Ji+Chen%22">Tzeng-Ji Chen</searchLink><br /><searchLink fieldCode="AR" term="%22Wen-Liang+Lo%22">Wen-Liang Lo</searchLink><br /><searchLink fieldCode="AR" term="%22Mu-Hong+Chen%22">Mu-Hong Chen</searchLink> (ORCID <externalLink term="https://orcid.org/0000-0001-6516-1073">0000-0001-6516-1073</externalLink>)
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  Data: <searchLink fieldCode="SO" term="%22Journal+of+Attention+Disorders%22"><i>Journal of Attention Disorders</i></searchLink>. 2024 28(14):1726-1733.
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  Data: SAGE Publications. 2455 Teller Road, Thousand Oaks, CA 91320. Tel: 800-818-7243; Tel: 805-499-9774; Fax: 800-583-2665; e-mail: journals@sagepub.com; Web site: https://sagepub.com
– Name: PeerReviewed
  Label: Peer Reviewed
  Group: SrcInfo
  Data: Y
– Name: Pages
  Label: Page Count
  Group: Src
  Data: 8
– Name: DatePubCY
  Label: Publication Date
  Group: Date
  Data: 2024
– Name: TypeDocument
  Label: Document Type
  Group: TypDoc
  Data: Journal Articles<br />Reports - Research
– Name: Subject
  Label: Descriptors
  Group: Su
  Data: <searchLink fieldCode="DE" term="%22Dental+Health%22">Dental Health</searchLink><br /><searchLink fieldCode="DE" term="%22Adolescents%22">Adolescents</searchLink><br /><searchLink fieldCode="DE" term="%22Attention+Deficit+Hyperactivity+Disorder%22">Attention Deficit Hyperactivity Disorder</searchLink><br /><searchLink fieldCode="DE" term="%22Hygiene%22">Hygiene</searchLink><br /><searchLink fieldCode="DE" term="%22Drug+Therapy%22">Drug Therapy</searchLink><br /><searchLink fieldCode="DE" term="%22Foreign+Countries%22">Foreign Countries</searchLink><br /><searchLink fieldCode="DE" term="%22Comorbidity%22">Comorbidity</searchLink><br /><searchLink fieldCode="DE" term="%22Health+Behavior%22">Health Behavior</searchLink>
– Name: Subject
  Label: Geographic Terms
  Group: Su
  Data: <searchLink fieldCode="DE" term="%22Taiwan%22">Taiwan</searchLink>
– Name: DOI
  Label: DOI
  Group: ID
  Data: 10.1177/10870547241273093
– Name: ISSN
  Label: ISSN
  Group: ISSN
  Data: 1087-0547<br />1557-1246
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Objectives: Previous studies have demonstrated poor oral hygiene in children with attention deficit hyperactivity disorder (ADHD). However, the association between ADHD and periodontitis is still unclear. Methods: In all, 16,211 adolescents with ADHD and 162,110 age- and sex-matched controls participated in the study between 2001 and 2011. To identify the occurrence of periodontitis, the participants were followed up till the end of 2011. Confounding factors, including smoking, diabetes, and depressive disorder, were assessed and adjusted in the Cox regression models. Results: Adolescents with ADHD (HR: 2.29) were more likely to develop periodontitis later in life than controls. We additionally observed the beneficial effect of atomoxetine (HR: 0.42) on the periodontitis risk among adolescents with ADHD. However, this finding should be interpreted cautiously given the small sample (n = 290) of children taking atomoxetine in the present study. Conclusions: ADHD is an independent risk factor for subsequent periodontitis development. Oral health should be closely monitored in adolescents with ADHD. Future investigation of the shared pathomechanisms between periodontitis and ADHD is warranted.
– Name: AbstractInfo
  Label: Abstractor
  Group: Ab
  Data: As Provided
– Name: DateEntry
  Label: Entry Date
  Group: Date
  Data: 2024
– Name: AN
  Label: Accession Number
  Group: ID
  Data: EJ1447284
PLink https://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=eric&AN=EJ1447284
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  BibEntity:
    Identifiers:
      – Type: doi
        Value: 10.1177/10870547241273093
    Languages:
      – Text: English
    PhysicalDescription:
      Pagination:
        PageCount: 8
        StartPage: 1726
    Subjects:
      – SubjectFull: Dental Health
        Type: general
      – SubjectFull: Adolescents
        Type: general
      – SubjectFull: Attention Deficit Hyperactivity Disorder
        Type: general
      – SubjectFull: Hygiene
        Type: general
      – SubjectFull: Drug Therapy
        Type: general
      – SubjectFull: Foreign Countries
        Type: general
      – SubjectFull: Comorbidity
        Type: general
      – SubjectFull: Health Behavior
        Type: general
      – SubjectFull: Taiwan
        Type: general
    Titles:
      – TitleFull: Risk of Periodontitis in Adolescents with Attention Deficit Hyperactivity Disorder: A Cohort Study of 81,055 Participants
        Type: main
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            NameFull: Ju-Wei Hsu
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            NameFull: Li-Chi Chen
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            NameFull: Kai-Lin Huang
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            NameFull: Shih-Jen Tsai
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            NameFull: Tzeng-Ji Chen
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            NameFull: Wen-Liang Lo
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            NameFull: Mu-Hong Chen
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            – D: 01
              M: 12
              Type: published
              Y: 2024
          Identifiers:
            – Type: issn-print
              Value: 1087-0547
            – Type: issn-electronic
              Value: 1557-1246
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            – Type: volume
              Value: 28
            – Type: issue
              Value: 14
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            – TitleFull: Journal of Attention Disorders
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