Obsessive-compulsive symptom dimensions in a population-based, cross-sectional sample of school-aged...

7
Obsessive-compulsive symptom dimensions in a population-based, cross-sectional sample of school-aged children Pedro G. Alvarenga a, b, * , Raony C. Cesar a, 1 , James F. Leckman a, c, 1 , 3 , Tais S. Moriyama a, b, 1 , 2 , Albina R. Torres d, 4 , Michael H. Bloch c, 3 , Catherine G. Coughlin d, 4 , Marcelo Q. Hoexter a, b, 1 , 2 , Gisele G. Manfro b, e, 2, 5 , Guilherme V. Polanczyk a, b, 1 , 2 , Euripedes C. Miguel a, b, 1 , 2 , Maria C. do Rosario b, f, 2, 6 a Department & Institute of Psychiatry, University of Sao Paulo Medical School (USP), Rua Dr. Ovídio Pires de Campos, 785, S~ ao Paulo 01060-970, SP, Brazil b National Institute of Developmental Psychiatry for Children and Adolescents, CNPq, Rua. Dr. Ovídio Pires de Campos, S~ ao Paulo 01060-970, SP, Brazil c Child Study Center, Yale School of Medicine, 230, South Frontage Rd, New Haven, CT 06519, USA d Department of Neurology, Psychology and Psychiatry, Botucatu Medical School, S~ ao Paulo State University (UNESP), Av. Prof. Montenegro s/n, Botucatu 18618970, SP, Brazil e Hospital de Clinicas de Porto Alegre, Federal University of Rio Grande do Sul (UFRGS), Rua Ramiro Barcelos, 2350, Porto Alegre 90035-903, RS, Brazil f Child and Adolescent Psychiatry Unit (UPIA), Department of Psychiatry, Federal University of S~ ao Paulo (UNIFESP), Rua Pedro de Toledo, 590, S~ ao Paulo 04038-020, SP, Brazil article info Article history: Received 7 July 2014 Received in revised form 3 November 2014 Accepted 29 January 2015 Keywords: Epidemiology Family history Obsessive-compulsive disorder School children abstract Background: Obsessive-compulsive disorder can be expressed as four potentially overlapping obsessive- compulsive symptom (OCS) dimensions (OCSD) (symmetry/ordering, contamination/cleaning, aggressive/sexual/religiousand collecting/hoarding). In clinical samples, some dimensions are more familial and associated with increased psychiatric comorbidity and malfunctioning. However, data concerning OCS and OCSD are scarce in non-clinical samples, particularly among children. The present study aims to estimate: (1) the prevalence and sex/age distribution of OCS/OCSD in a community-based sample of schoolchildren; (2) the association between OCS and additional clinical factors; and (3) the degree of familial aggregation of OCS/OCSD. Methods: OCS and OCSD were evaluated in 9937 Brazilian school-children (6e12 years-old) and their biological relatives using the Family History Screen. Data analyses included gradient estimated equations and post-hoc tests. Results: We included data on 9937 index-children, 3305 siblings (13e18 years-old), and 16,218 parents. Biological mothers were the informants in 87.6% of the interviews. OCS were present in 14.7% of the index-children; 15.6% of their siblings; 34.6% of their mothers and 12.1% of their fathers. The prevalence of OCS and each of the OCSD gradually increased from ages 6 to 12 years. Overall, OCS in children were associated with the presence of other psychiatric symptoms, as well as behavioral/school impairment. OCS and each of the four OCSD aggregated signicantly within families. Conclusions: OCS are prevalent and associated with psychiatric symptoms and clinical impairment among school-aged children. OCSD aggregate within families in a dimension-specic fashion. These ndings suggest a natural continuum between OCS and OCD with regard to their dimensional character. © 2015 Elsevier Ltd. All rights reserved. * Corresponding author. Instituto de Psiquiatria, Rua Dr. Ovídeo Pires de Campos, 875, S~ ao Paulo 01060-970, SP, Brazil. Tel.: þ55 (11) 99861 6989, þ55 (11) 2661 6972, þ55 (11) 2661 7898. E-mail addresses: [email protected] (P.G. Alvarenga), [email protected] (A.R. Torres), [email protected] (C.G. Coughlin), [email protected] (G.G. Manfro), [email protected] (G.V. Polanczyk), [email protected] (M.C. do Rosario). 1 Tel.: þ55 (11) 2661 6972. 2 Tel.: þ55 (11) 2661 7898. 3 Tel.: þ1 203 785 2540. 4 Tel.: þ55 (14) 3880 1220. 5 Tel.: þ55 (51) 3359 8000. 6 Tel.: þ55 (11) 5576 4990. Contents lists available at ScienceDirect Journal of Psychiatric Research journal homepage: www.elsevier.com/locate/psychires http://dx.doi.org/10.1016/j.jpsychires.2015.01.018 0022-3956/© 2015 Elsevier Ltd. All rights reserved. Journal of Psychiatric Research 62 (2015) 108e114

Transcript of Obsessive-compulsive symptom dimensions in a population-based, cross-sectional sample of school-aged...

lable at ScienceDirect

Journal of Psychiatric Research 62 (2015) 108e114

Contents lists avai

Journal of Psychiatric Research

journal homepage: www.elsevier .com/locate/psychires

Obsessive-compulsive symptom dimensions in a population-based,cross-sectional sample of school-aged children

Pedro G. Alvarenga a, b, *, Raony C. Cesar a, 1, James F. Leckman a, c, 1, 3,Tais S. Moriyama a, b, 1, 2, Albina R. Torres d, 4, Michael H. Bloch c, 3,Catherine G. Coughlin d, 4, Marcelo Q. Hoexter a, b, 1, 2, Gisele G. Manfro b, e, 2, 5,Guilherme V. Polanczyk a, b, 1, 2, Euripedes C. Miguel a, b, 1, 2, Maria C. do Rosario b, f, 2, 6

a Department & Institute of Psychiatry, University of Sao Paulo Medical School (USP), Rua Dr. Ovídio Pires de Campos, 785, S~ao Paulo 01060-970, SP, Brazilb National Institute of Developmental Psychiatry for Children and Adolescents, CNPq, Rua. Dr. Ovídio Pires de Campos, S~ao Paulo 01060-970, SP, Brazilc Child Study Center, Yale School of Medicine, 230, South Frontage Rd, New Haven, CT 06519, USAd Department of Neurology, Psychology and Psychiatry, Botucatu Medical School, S~ao Paulo State University (UNESP), Av. Prof. Montenegro s/n, Botucatu18618970, SP, Brazile Hospital de Clinicas de Porto Alegre, Federal University of Rio Grande do Sul (UFRGS), Rua Ramiro Barcelos, 2350, Porto Alegre 90035-903, RS, Brazilf Child and Adolescent Psychiatry Unit (UPIA), Department of Psychiatry, Federal University of S~ao Paulo (UNIFESP), Rua Pedro de Toledo, 590, S~ao Paulo04038-020, SP, Brazil

a r t i c l e i n f o

Article history:Received 7 July 2014Received in revised form3 November 2014Accepted 29 January 2015

Keywords:EpidemiologyFamily historyObsessive-compulsive disorderSchool children

* Corresponding author. Instituto de Psiquiatria, Rua(11) 2661 7898.

E-mail addresses: [email protected] (P(G.G. Manfro), [email protected] (G.V. Polanczyk),

1 Tel.: þ55 (11) 2661 6972.2 Tel.: þ55 (11) 2661 7898.3 Tel.: þ1 203 785 2540.4 Tel.: þ55 (14) 3880 1220.5 Tel.: þ55 (51) 3359 8000.6 Tel.: þ55 (11) 5576 4990.

http://dx.doi.org/10.1016/j.jpsychires.2015.01.0180022-3956/© 2015 Elsevier Ltd. All rights reserved.

a b s t r a c t

Background: Obsessive-compulsive disorder can be expressed as four potentially overlapping obsessive-compulsive symptom (OCS) dimensions (OCSD) (“symmetry/ordering”, “contamination/cleaning”,“aggressive/sexual/religious” and “collecting/hoarding”). In clinical samples, some dimensions are morefamilial and associated with increased psychiatric comorbidity and malfunctioning. However, dataconcerning OCS and OCSD are scarce in non-clinical samples, particularly among children. The presentstudy aims to estimate: (1) the prevalence and sex/age distribution of OCS/OCSD in a community-basedsample of schoolchildren; (2) the association between OCS and additional clinical factors; and (3) thedegree of familial aggregation of OCS/OCSD.Methods: OCS and OCSD were evaluated in 9937 Brazilian school-children (6e12 years-old) and theirbiological relatives using the Family History Screen. Data analyses included gradient estimated equationsand post-hoc tests.Results: We included data on 9937 index-children, 3305 siblings (13e18 years-old), and 16,218 parents.Biological mothers were the informants in 87.6% of the interviews. OCS were present in 14.7% of theindex-children; 15.6% of their siblings; 34.6% of their mothers and 12.1% of their fathers. The prevalenceof OCS and each of the OCSD gradually increased from ages 6 to 12 years. Overall, OCS in children wereassociated with the presence of other psychiatric symptoms, as well as behavioral/school impairment.OCS and each of the four OCSD aggregated significantly within families.Conclusions: OCS are prevalent and associated with psychiatric symptoms and clinical impairmentamong school-aged children. OCSD aggregate within families in a dimension-specific fashion. Thesefindings suggest a natural continuum between OCS and OCD with regard to their dimensional character.

© 2015 Elsevier Ltd. All rights reserved.

Dr. Ovídeo Pires de Campos, 875, S~ao Paulo 01060-970, SP, Brazil. Tel.: þ55 (11) 99861 6989, þ55 (11) 2661 6972, þ55

.G. Alvarenga), [email protected] (A.R. Torres), [email protected] (C.G. Coughlin), [email protected]@gmail.com (M.C. do Rosario).

P.G. Alvarenga et al. / Journal of Psychiatric Research 62 (2015) 108e114 109

1. Introduction

Obsessive-compulsive disorder (OCD) is a chronic and poten-tially disabling psychiatric disorder with a lifetime prevalence of2e3% among adults (Fontenelle et al., 2006; Ruscio et al., 2010) anda prevalence of 0.5e2% in adolescent and pediatric populations(AACAP, 2012). Pediatric OCD is frequently under-diagnosed and upto 90% of affected children are not treated, especially mild andmoderate cases (AACAP, 2012).

There is limited evidence on the frequency and characteristics ofobsessive-compulsive symptoms (OCS) and subthreshold OCD innon-clinical populations. Most of these studies included adoles-cents (Apter et al., 1996; Essau et al., 2000; Flament, 1990; Shamset al., 2011; Valleni-Basile et al., 1994; Zohar et al., 1992) andadults (Fullana et al., 2010), and only a few have included schoolage-children (Canals et al., 2012; Voltas et al., 2014). These studiesare quite divergent regarding the prevalence of OCS, with reportedestimates varying from 2.0% (Flament, 1990) to 19.0% (Valleni-Basile et al., 1994; Vivan et al., 2014). Many studies have shownthat the presence of OCS, evenwithmild severity, is associated withan increased risk of co-occurring psychiatric disorders and varyingdegrees of functional impairment (Bruijn et al., 2010; Canals et al.,2012; Shams et al., 2011), as well as an increased risk for eventuallydeveloping full-blown OCD (Black and Gaffney, 2008; Fullana et al.,2009). Longitudinal studies have also demonstrated that OCS canpersist over years (Bruijn et al., 2010; Canals et al., 2012; Voltaset al., 2014).

Dissecting the OCD phenotype into multiple, overlapping andnon-exclusive obsessive-compulsive symptom dimensions (OCSD)has appeared to be a promising way to address the OCD hetero-geneity. At least four relatively independent OCSD have beenidentified by multiple factor-analyses: (1) “contamination/clean-ing”; (2) “aggressive/sexual/religious/checking”; (3) “symmetry/ordering/arranging”; and (4) “collecting/hoarding” (Bloch et al.,2008; Mataix-Cols et al., 2013; Stewart et al., 2008). Many studieshave demonstrated that these OCSD are temporally stable (Fullanaet al., 2009), associated with different comorbidity patterns (Hasleret al., 2007; Torres et al., 2012), have distinct neurobiological sub-strates (Alvarenga et al., 2012a, b; Van den Heuvel et al., 2009) andpatterns of treatment response (Bloch et al., 2014).

There is strong evidence that OCD is a familial disorder and thatthis familiality is largely explained by genetic factors (Mataix-Colset al., 2013). Nevertheless, familial studies assessing multipleOCSD are infrequent. For example, Alsobrook et al. (1999) reportedthat higher proband scores on the “symmetry/ordering” and the“aggression/sexual/religious/checking” dimensions were predictiveof higher risks of OCD in the first degree relatives (FDR). The familialcomponent of these OCSD have been replicated in family studies(Hanna et al., 2005; Hasler et al., 2007; Chacon et al., 2007), insegregation analyses (Leckman et al., 2003), and in molecular ge-netic studies (Kim et al., 2005; Zhang et al., 2002). However, almostall familial studies accessing OCSD have been with clinicallyreferred OCD populations. As OCS are prevalent, can be part ofnormal development, and are better observed as a dimensionalmeasure (rather than categorical), the study of non-clinical pop-ulations are better suited to understand these phenomena along ofcontinuum from normal to an abnormal obsessive-compulsivespectrum of behaviors (Abramowitz et al., 2014).

The present study examines obsessive-compulsive phenomenain a large population-based sample of children 6e12 years of ageand their biological relatives. In addition to documentingobsessive-compulsive phenomena presence in school-aged chil-dren, we also sought to estimate the familial aggregation of OCSand OCSD and to determine the degree to which OCS were asso-ciated with other psychiatric symptoms and clinical impairment.

2. Material and methods

2.1. Procedures

This study is drawn from a larger community cross-sectional,school-based study as published in the National Institute of Devel-opment Psychiatry (INPD) (Salum et al., 2014). A total of 57 publicelementary schools from two large Brazilian cities (22 schools inPorto Alegre and 35 schools in S~ao Paulo) were included. Thisinvestigation was carried out in accordance with the latest versionof the Declaration of Helsinki and was approved by the ethicscommittees from the universities in these two cities. Writtenconsents were obtained from all parents of participants.

2.2. Participants

We approached 12,500 eligible families with at least one 6e12year-old (index) child. 4488 families were excluded due to refusalor failure to complete the interview or the consent form (18.8%);biological parent unavailability (9.2%); invalid phone contacts/failed contact (5.3%); and other reasons (2.6%). The final samplecomprised 8012 families including: 9937 index-children, theirsiblings and their biological parents. Only biologically-related sib-lings up to the age of 18 years were included and adoptive childrenand siblings older than 18 years-old were excluded.

2.3. Data collection

Trained lay-interviewers conducted the interviews, assessing allinformation from the caregiver of the index-children (responderswere children's biological mothers in 87.6% of the families). INPDexpert clinicians taught sessions (to lay-interviewers) on majorpsychiatric symptoms and disorders, risk factors, confidentialityand ethical issues throughout the two-day procedure. Training alsoincluded videotaped interviews as well as simulation and role-playing exercises.

2.4. Instruments

Caregivers were interviewed with the (Psychiatric) Family His-tory Screen (FHS) (Weissman et al., 2000). The FHS is a valid briefscreen for collecting lifetime psychiatric history was designed toinvestigate the presence of psychiatric symptoms, previous mentalhealth treatments and other associated factors, such as schoolrefusal and/or withdrawal, delinquent behaviors, and overallfunctional impairment (Milne et al., 2009; Weissman et al., 2000).Psychiatric symptoms were grouped into: psychotic symptoms,anxiety symptoms, mood disorders symptoms, learning disorderssymptoms and functional impairment with regard to schoolrefusal/withdrawal, and delinquent behavior.

The OCS were ascertained using a short parent-report instru-ment adopted from the Dimensional Yale-Brown Obsessive-Compulsive Scale (DY-BOCS) (Rosario-Campos et al., 2006), whichassesses OCS according to four specific symptom dimensions:“symmetry/ordering/arranging”; “contamination/cleaning”;“aggressive/sexual/religious”; and “collecting/hoarding” (Table 1).For exploratory analyses, children with at least one OCS weregrouped together (OCS group).

2.5. Data analyses

The student t-test was used for normally distributed continuousvariables and the chi-square test for categorical variables. To mea-sure the association between the index-children symptomdimension and their first degree relative's OCSD, the Generalized

Table 1Dimensional obsessive-compulsive screening questionnaire.

Q1. Has anyone in your family been bothered by a need of things to be perfect orexact, or has had concerns with symmetry, or a need to do things repeatedlyuntil the objects are arranged or organized in a symmetrical or “just right”fashion?

Q1.1. [If “yes” to Q1] Has this person spent a lot of time with these rituals or“quirks” to arrange or organize things?

Q2. Has anyone in your family had intrusive worries about being physically sick?What about having a fear of being contaminated by dirt or bacteria?

Q2.1. [If “yes” to Q2] Has this person needed to wash or clean excessively, or in aritualized way, his own body or objects? Has he/she ever had an excessiveneed for cleanliness?

Q3. Has anyone in your family been bothered by worries or fears that somethingvery bad might happen (e.g.: accidents, the death of a relative)? What abouthaving thoughts containing improper violent, sexual or religious content?

Q3.1. [If “yes” to Q3] Has this person needed to do something repeatedly, such aspraying or confessing to avoid or dismiss these thoughts of violent, sexual orreligious content?

Q.4. Has anyone in your family needed to collect or store MANY things or uselessobjects?

This brief screening questionnaire was designed specifically for the purpose of thisstudy, consisting of seven questions (four main questions and three qualifiers toassess four obsessive-compulsive dimensions) adapted from DYBOCS (Ros�ario-Campos et al., 2006). Symmetry/ordering dimension was considered in the pres-ence of positive answers to both Q1 and Q1. (qualifier)1. Contamination/cleaningdimension in the presence of positive answers to both Q2 and Q2.1. Aggressive/sexual/religious” dimension in the presence of Q3 and Q3.1 and collecting/hoardingdimension in the presence of Q4.

P.G. Alvarenga et al. / Journal of Psychiatric Research 62 (2015) 108e114110

Estimating Equations (GEE) model (Liang and Zeger, 1986) was used.The GEE method allows the introduction of correlated individualsin a generalized linear model (McCullagh and Nelder, 1989). Weanalyzed all possible pairs (dyads) of all the index-children versuseach first degree relative (father, mother and first degree-sibling).Tukey test (Hsu, 1996) post-hoc correction was used. The Statisti-cal Package for Social Sciences (SPSS) version 14.0 and the R 3.0.2(www.r-project.org) were used for storage and analysis of data.

3. Results

The study comprised information on 8012 families, 9937 index-children, 8019 biological mothers, 8198 biological fathers, and 3305biological siblings. 1627 families had more than one index-childand 1262 families had at least one half-sibling. The total samplecomprised 29,459 individuals. OCS were present in 19.4% of thetotal sample, including 14.7% of index-children, 16.5% of their sib-lings and 12.1% of their fathers. Therewas a fairly similar prevalenceof OCS among the index-children, siblings, and fathers, but motherspresented a higher rate (34.0%). Regarding the OCSD, the “collect-ing/hoarding” dimension was the most prevalent among childrenand adolescents (index-children and their siblings) and biologicalfathers. Among biological mothers, the “symmetry/ordering” and

Table 2Sociodemographic data and prevalence of obsessive-compulsive symptom dimensions in

Index-children (6e12 years)(n ¼ 9937)

Older sibli(n ¼ 3305

Sex (male) 52.41% 50.35%Age, mean (SD) 8.87 (1.90) 15.20 (1.66OCS (at least one) 14.70% 16.50%Symmetry/ordering/arranging 2.18% 2.60%Contamination/cleaning 3.78% 4.30%Aggressive/sexual/religious 2.43% 3.18%Collecting/hoarding 9.27% 9.68%

OCS: obsessive-compulsive symptoms; SD: standard deviation. As the sample unit in thisfamily. If the index-children from the same family are half-siblings, there may be more

“aggressive/sexual/religious” dimensions were the most prevalent(Table 2).

Exploratory analyses in the index-children group (6e12 years-old) revealed the presence of at least one OCS and of the fourOCSD dimensions to be associated with an increase in age(p < .001). The presence of at least one OCS and the collecting-hoarding dimension was related to male gender (p < .001)(Table 3). In boys, the prevalence of OCS and of the four OCSD tendsto peak earlier compared to girls, and decreases after the age of 11,when prevalence in girls starts to increase (Fig. 1).

A comparison of index-children with or without OCS revealedthat the OCS group also presented higher rates of mood, anxiety,and psychotic symptoms, previous mental health treatments andfunctional impairment in comparison to non-OCS children(Table 4).

Familial aggregation of OCS and OCSD were obtained from theGEE model. Of all 8012 families, 38.4% of those without OCS index-children (n ¼ 6694) have at least one first degree relative with OCS.63% of families with at least one OCS index-child (n ¼ 1318) have atleast one other first-degree relative with OCS (p ¼ .0001). Signifi-cant associations were obtained for all the four OCSD. “Contami-nation/cleaning” was the most familial dimension, with an oddsratio (OR) of 1.44 (CI 95% 1.23e1.67) (Table 3).

4. Discussion

This is the first study to estimate the prevalence and distributionof OCS and OCSD in a large population-based sample of school-agechildren (6e12 year-olds) and their biological relatives. This pedi-atric sample is larger than those of previous Brazilian (Fleitlich-Bilyk and Goodman, 2004; Vivan et al., 2014) and internationalepidemiological studies (Canals et al., 2012; Voltas et al., 2014).

The overall prevalence of (at least one) OCS in the total sample(n¼ 29,459) was 19.4%, similar to that described in previous studiesincluding adolescents and young adults (Apter et al., 1996; Fullanaet al., 2009; Mahfouz et al., 2009; Shams et al., 2011; Valleni-Basileet al., 1994, 1996; Vivan et al., 2014). Very few studies, though, haveestimated the prevalence of OCS and/or OCD in prepubertal chil-dren (Canals et al., 2012; Fleitlich-Bilyk and Goodman, 2004;Heyman et al., 2001; Voltas et al., 2014). These studies are quitedivergent regarding the prevalence of OCD, with reported esti-mates varying from 0.1% (Fleitlich-Bilyk and Goodman, 2004) to1.8% (Canals et al., 2012). Moreover, one recent study reports that30.4% of children exhibit mild OCD symptoms (OCS) (Voltas et al.,2014) and another reports a school-aged children OCS prevalenceof 10.3%, considering both mild OCS plus sublinical OCD (Canalset al., 2012). In the present study, we detected a prevalence of14.7% for one or more OCS among 6e12 year old children, which isfairly high and similar to the prevalence reported in their adoles-cent siblings (15.6%). In a recent Brazilian study, the past-monthprevalence of OCS among high school adolescents was 18.3%

school-aged children and their biological relatives.

ngs (13e18 years))

Fathers(n ¼ 8198)

Mothers(n ¼ 8019)

All(n ¼ 29,459)

100% 0 51.16%) 38.73 (8.38) 35.19 (7.09) 19.95 (13.27)

12.10% 34.04% 19.44%3.0% 15.51% 6.08%2.76% 11.09% 5.54%2.73% 15.29% 6.10%5.83% 9.36% 8.11%

study is the family (n ¼ 8012 families), there may be more than one index-child perthan one biological parent per family.

Table 3Familial aggregation of overall obsessive-compulsive symptoms and specific symptom dimensions and its association with children's sex and age.

GEE estimation Standard error Or CI 95% (lower) CI 95% (higher) P value (Tukey)

(Overall) Obsessive-compulsive symptomsSex (male) 0.08 1.3 1.12 0.08 1.52 0.001Age 0.02 1.15 1.11 0.02 1.19 <0.001OCS in FDR 0.02 1.16 1.12 0.02 1.20 <0.001Symmetry/ordering dimensionSex (male) 0.01 0.23 1.01 0.64 1.58 0.976Age 0.199 0.06 1.22 1.09 1.36 0.001Symmetry/ordering in FDR 0.18 0.08 1.19 1.01 1.40 0.036Aggressive/sexual/religious dimensionSex (male) 0.08 0.17 1.08 0.78 1.52 0.638Age 0.16 0.04 1.17 1.08 1.27 <0.001Aggressive/sexual/religious in FDR 0.22 0.07 1.24 1.09 1.42 0.001Contamination/cleaning dimensionSex (male) 0.10 0.13 1.10 0.86 1.43 0.455Age 0.09 0.04 1.09 1.02 1.17 0.014Contamination/cleaning in FDR 0.36 0.08 1.44 1.23 1.67 <0.001Collecting/hoarding dimensionSex (male) 0.36 0.09 1.43 1.20 1.71 <0.001Age 0.16 0.02 1.18 1.13 1.23 <0.001Collecting/hoarding in FDR 0.12 0.04 1.13 1.04 1.22 0.002

OR: odds ratio, CI: confidence interval, FDR: first-degree relative, OCS: obsessive-compulsive symptoms.

P.G. Alvarenga et al. / Journal of Psychiatric Research 62 (2015) 108e114 111

(Vivan et al., 2014). These differences in the prevalence of OCD andOCS across the literature may be justified by the variation in in-struments employed, ability of the interviewers, and populationsstudied in each analysis.

OCS in index-children were significantly more commonlyendorsed by males, which is consistent with some previous studies(Flament et al., 1998; Mahfous et al., 2009; Vivan et al., 2014) butcontrasts with others (Canals et al., 2012; Fullana et al., 2009) thatreported similar frequencies between sexes. Actually, the preva-lence of OCS and of the four OCSD tends to peak earlier in boyscompared to girls and decreases after the age of 11. The prevalenceof OCS and OCSD in girls starts to peak later (around 11 years of age)and increases toward adolescence. In fact, the distribution of OCS inthis study is similar to OCD distribution in the general population,with higher rates in males in childhood and higher rates in femalesfrom adolescence (Flament, 1990; Ruscio et al., 2010). As expected,the prevalence of OCS and of the four OCSD in children increasedprogressively with age, confirming the results of several commu-nity studies with pediatric samples (Essau et al., 2000; Fullana et al.,2010; Heyman et al., 2001; Valleni-Basile et al., 1996). However, wedid not report data for children above 12 years, which limits thisanalysis.

In this study, the “collecting/hoarding” dimension was the mostprevalent dimension among children. In previous studies accessingOCS in children, aggressive and checking symptoms were the mostprevalent (Fullana et al., 2010; Valleni-Basile et al., 1994, 1996).Collecting/hoarding symptoms were also frequent in some studies(Valleni-Basile et al., 1994) but not investigated in others (Fullanaet al., 2009, 2010). Since our sample was composed of youngersubjects, compared to previous reports (Apter et al., 1996; Flament,1990; Fullana et al., 2010; Valleni-Basile et al., 1994; Vivan et al.,2014; Zohar et al., 1992), the presence of collecting/hoardingsymptoms may, at least in part, reflect normal developmentalpatterns of behavior in young children (Evans et al., 1999; Leckmanand Evans, 2006). Furthermore, collecting/hoarding symptomsmaybe present in several mental disorders (Torres et al., 2012) andHoarding Disorder is now listed as a separate disorder in the DSM-5as a disorder “related” to OCD (APA, 2013).

Among adults (parents) in our sample, there was a higher fre-quency of OCS in biological mothers, compared to biological fa-thers, especially in the “symmetry/ordering” and “aggressive/sexual/religious” dimensions. The higher frequency of symmetry/

ordering symptoms in adults is consistent with the results of a largeand multicenter clinical study including 1001 Brazilian patientswith OCD (de Mathis et al., 2013). Particularly among women, thesebehaviors, along with contamination/cleaning, may represent acontinuum from normal to psychopathological manifestations thatare influenced by socio-cultural aspects. Moreover, the “aggressive/sexual/religious” dimension has been associated with femalegender in treatment-seeking adults (Torresan et al., 2013). How-ever, the high disproportion of OCS between genders in the presentstudy may in part represent information bias, since there are noreports of such OCS gender-based imbalances in the adult popu-lation. It is important to consider that, in the present study, mothersgave information about all family members in 87.6% of the cases.Given the potential biases associated with self- and parental-reports, some mothers may have enhanced their complaints inorder to obtain referrals to treatment. Alternatively, some mothersmay have underestimated the other family members' symptoms,since many OCS are not openly shared even with close familymembers, due to preserved insight and embarrassment (Alvarengaet al., 2012a, b; Rosario-Campos et al., 2008).

Regarding clinical severity, our results are consistent with pre-vious studies assessing juvenile samples that demonstrated thepresence of OCS in children is associated with increased levels ofpsychiatric symptom comorbidity and clinical impairment (Apteret al., 1996; Blom et al., 2011; Canals et al., 2012; Vivan et al.,2014; Voltas et al., 2014). Therefore, we agree with authors whosuggest that threshold obsessive compulsive phenomena should bemore actively and systematically investigated by primary care andmental health professionals (Fullana et al., 2009). In addition, theresults emphasize the need for future follow up-studies investi-gating the predictive value of these symptoms for the developmentof the full-blown OCD.

Finally, a novel finding of this study is that OCSD aggregatewithin families in a dimension-specific fashion. This is similar towhat has been reported for adults in clinically referred cases of OCDand Tourette's disorder (Alsobrook et al., 1999; Hanna et al., 2005;Leckman et al., 2003) and in other non-clinical OCS samples (vanGrootheest et al., 2008; Iervolino et al., 2011; Taberner et al.,2009). This finding provides additional evidence that a dimen-sional approach to OCD has scientific merit. The “contamination/cleaning” dimension showed the strongest familial patterncompared to the other OCSD, which contrasts with several previous

Fig. 1. Percentile of obsessive-compulsive symptoms (OCS) (axis y) in 9937 index-children from 6 to 12 years-old (axis x) stratified by age and gender. In boys, the prevalence of atleast one OCS and of the four OCS dimensions tends to peak earlier and decrease from the age of 11, when prevalence of OCS in girls starts to increase. OCS and the four dimensionsare associated with increasing age (p < .001). OCS and the collecting-hoarding dimension are associated with male gender (p < .001).

Table 4Psychiatric symptoms and associated clinical factors in index-children with and without obsessive-compulsive symptoms.

Index children (6-12 years-old) With OCS (n ¼ 1459) Without OCS (n ¼ 8478) (Total) (n ¼ 9937)

Sex (male) M: 52.12%* M: 50.9%* 50.75%Age (SD) 9.2 (1.81)* 8.82 (1.9)* 8,9 (1,9)Mood disorders symptoms 36.1%* 16.24%* 19.2%Anxiety symptoms 68.9%* 41.9%* 45.8%Psychotic symptoms 12.47%* 3.64%* 4.94%Disruptive behaviors 45.1%* 28.10%* 30.59%Learning disorder symptoms 41.6%* 27.46%* 29.54%Previous mental health treatment (�) 22.76%* 12.05%* 13.63%Functional impairment (��) 13.57%* 5.41%* 6.61%

*p < .001(Chi-square); (�) previous inpatient or outpatient mental health treatment; (��): overall functional impairment, school refusal/withdraw or delinquent behavior; OCS:obsessive-compulsive symptoms. Note that Family History Screen (Milne et al., 2009) does not stipulate psychiatric diagnoses, but only the presence of psychiatric symptoms.

P.G. Alvarenga et al. / Journal of Psychiatric Research 62 (2015) 108e114112

studies that have reported the “symmetry/ordering” and the“aggression/checking” rituals as the most common familial symp-toms (Alsobrook et al., 1999; Hanna et al., 2005; Leckman et al.,2003). However, our finding is consistent with a sib-pair studyusing the full version of DY-BOCS, which reported the “contami-nation/washing” dimension as the most familial (Chacon et al.,2007) and with a recent twin study that found evidence for spe-cific genetic and environmental factors underlying the “contami-nation/washing” dimension (van Grootheest et al., 2008).

5. Limitations

The results of the present study should be considered in light ofseveral limitations, particularly related to possible collection andinformation bias. First, all interviews were conducted by trained,but lay, interviewers, and many of them (60%) were conducted bytelephone. Interviews conducted by lay interviewers can over-estimate the presence of OCD (Stein et al., 1997). Second, the OCSquestions were adapted from another instrument (the DY-BOCS) to

P.G. Alvarenga et al. / Journal of Psychiatric Research 62 (2015) 108e114 113

be a brief screening measure of OCSD and they have not beenvigorously validated. Third, the FHS is a screening instrument thatdoes not allow clinicians to make mental disorder diagnoses. Theproperties of FHS substantially improve when two informants areused (Weissman et al., 2000), which was not possible in our study.Fourth, most informants were mothers of the index-children, whomay have over-reported their own OCS and underestimated theoccurrence of OCS in other family members, due to the secret na-ture of some symptoms. Fifth, despite the large sample size, someassociated clinical factors had to be grouped, since they wererelatively infrequent in the pediatric sample. Finally, this study islimited in its inability to generalize behaviors beyond those ofchildren attending public elementary schools in Brazil.

6. Conclusions

This is the first study to investigate the presence of specificOCSD in a large community sample of school-aged (6e12 years old)children and their biological relatives. The results indicate that OCSand OCSD are present in a substantial number of children, adoles-cents and their parents. The presence of OCS (and not necessarilythe full-blown disorder) in children was associated with increasedrates of psychiatric symptom comorbidity, clinical referrals andfunctional impairment. Specific OCSD were found to aggregatewithin families mostly in a dimension-specific fashion, which mayhave implications for future genetic and neuroimaging studies. Ourfindings have potentially relevant clinical implications for OCDunderstanding and prevention, which need to be further exploredin longitudinal population-based studies.

Ethics

The authors assert that all procedures contributing to this workcomply with the ethical standards of the relevant national andinstitutional committees on human experimentation, with theethical principles of psychologists and code of conduct (AmericanPsychiatric Association, 2013) and with the Helsinki Declaration(1975, as revised in 2008). All Brazilian authors had full access tothe database and take responsibility for the integrity and the ac-curacy of the data analysis.

Role of funding sources

This study was supported by the National Council of Techno-logical and Scientific Development (CNPQ) (grant: 573974/2008-0)and Foundation for Research in the State of Sao Paulo (FAPESP)(grant: 08/57896-8).

Contributors

Pedro G. Alvarenga, MD PhD, is the first author of the manu-script, has materially participated in both the research design,execution and article preparation

Raony C. Cesar, statistician, has materially participated in theresearch design, data analysis.

James F. Leckman, MD PHD, child psychiatrist, has materiallyparticipated in research design, data analysis and articlepreparation.

Tais S. Moriyama, MD, child psychiatrist, has materially partic-ipated in research design, data analysis (psychiatric diagnosis) andarticle preparation.

Albina R. Torres, MD PhD, epidemiologist, has materiallyparticipated in research design and article preparation.

Michael H. Bloch, MD, child and adult psychiatrist, has materi-ally participated in research design and article preparation.

Catherine G. Coughlin, BS, research assistant has materiallyparticipated in article preparation and review.

Marcelo Q. Hoexter, MD PhD, adult psychiatrist has materiallyparticipated in research design and article preparation.

Gisele G. Manfro, MD PhD, child psychiatrist, has materiallyparticipated in research design, data analysis (psychiatric diag-nosis) and article preparation.

Guilherme V. Polanczyk, MD PhD, child psychiatrist, has mate-rially participated in research design, data analysis (psychiatricdiagnosis) and article preparation.

Euripedes C. Miguel, MD PhD, adult and child psychiatrist, hasmaterially participated in research design, data analysis (psychi-atric diagnosis) and article preparation.

Maria C. do Rosario, MD PhD, child psychiatrist, last (senior)author. Has materially participated in research design, mentorshipactivities, data analysis and article preparation.

Conflicts of interest

Guilherme Polanczyk has served as a speaker and/or consultantto Eli-Lilly, Novartis, Janssen-Cilag, and Shire Pharmaceuticals,developed educational material for Janssen-Cilag, and receivesunrestricted research support from Novartis; Michael H. Bloch hasreceived support from the National Institutes of Health (salary andresearch funding), Tourette Syndrome Association (research fund-ing), Patterson Trust Foundation (research funding) and the Rem-brandt Foundation (research funding); James F. Leckman, MD, PhD,has received support from the National Institutes of Health (salaryand research funding), Tourette Syndrome Association (researchfunding), Grifols, LLC (research funding), Klingenstein Third Gen-eration Foundation (medical student fellowship program), JohnWiley and Sons (book royalties), McGraw Hill (book royalties), andOxford University Press (book royalties). All authors materiallyparticipated in the research and/or article preparation and haveapproved the final manuscript.

Acknowledgments

The authors thank Luis Augusto Rohde, Giovanni Salum, JilianMulqueen and Marcos Mercadante (in memoriam) and MonicaRudner for previous contributions and for help in preparing themanuscript.

References

American Academy of Child and Adolescent Psychiatry (AACAP). Practice parame-ters for the assessment and treatment of children and adolescents withobsessive. J Am Acad Child Adolesc Psychiatry 2012;51(1):98e113.

Abramowitz JS, Fabricant LE, Taylor S, Deacon BJ, McKay D, Storch EA. The relevanceof analogue studies for understanding obsessions and compulsions. Clin Psy-chol Rev 2014;34(3):206e17.

Alsobrook II JP, Leckman JF, Goodman WK, Rasmussen SA, Pauls DL. Segregationanalysis of obsessive-compulsive disorder using symptom-based factor scores.Am J Med Genet 1999;88(6):669e75.

Alvarenga PG, de Mathis MA, Dominguez Alves AC, do Ros�ario MC, Fossaluza V,Hounie AG, et al. Clinical features of tic-related obsessive-compulsive disorder:results from a large multicenter study. CNS Spectr 2012a;17(2):87e93.

Alvarenga PG, do Ros�ario MC, Batistuzzo MC, Diniz JB, Shavitt RG, Duran SL, et al.Obsessive-compulsive symptom dimensions correlate to specific gray mattervolumes in treatment-naïve patients. J Psychiatr Res 2012b;46(12):1635e42.

American Psychiatric Association. Diagnostic and statistical manual of mental dis-orders. 5th ed. Washington (DC): APA; 2013.

Apter A, Pauls DL, Bleich A, Zohar AH, Kron S, Ratzoni G, et al. An epidemiologicstudy of Gilles de la Tourette's syndrome in Israel. Arch Gen Psychiatry 1996;50:734e8.

Black DW, Gaffney GR. Subclinical obsessive-compulsive disorder in children andadolescents: additional results from a “high-risk” study. CNS Spectr 2008;13:54e61.

Bloch MH, Landeros-Weisenberger A, Rosario MC, Pittenger C, Leckman JF. Meta-analysis of the symptom structure of obsessive-compulsive disorder. Am JPsychiatry 2008;165(12):1532e42.

P.G. Alvarenga et al. / Journal of Psychiatric Research 62 (2015) 108e114114

Bloch MH, Bartley CA, Zipperer L, Jakubovski E, Landeros-Weisenberger A,Pittenger C, et al. Meta-analysis: hoarding symptoms associated with poortreatment outcome in obsessive-compulsive disorder. Mol Psychiatry 2014Sep;19(9):1025e30.

Blom RM, de Bruijn C, de Graaf R, ten Have M, Denys DA. Obsessions in normalityand psychopathology. Depress Anxiety 2011;28(10):870e5.

Bruijn C, Beun S, de Graaf R, ten Have M, Denys D. Subthreshold symptoms andobsessive-compulsive disorder: evaluating the diagnostic threshold. PsycholMed 2010;40(6):989e97.

Canals J, Hern�andez-Martínez C, Cosi S, Voltas N. The epidemiology of obsessive-compulsive disorder in Spanish school children. J Anxiety Disord 2012;26(7):746e52.

Chacon P, Rosario-Campos MC, Pauls DL, Hounie AG, Curi M, Akkerman F, et al.Obsessive-compulsive symptoms in sibling pairs concordant for obsessive-compulsive disorder. Am J Med Genet 2007;144(4):551e5.

De Mathis MA, Diniz JB, Hounie AG, Shavitt RG, Fossaluza V, Ferr~ao Y, et al. Tra-jectory in obsessive-compulsive disorder comorbidities. Eur Neuro-psychopharmacol 2013;23(7):594e601.

Essau CA, Conradt J, Petermann F. Frequency, comorbidity, and psychosocialimpairment of anxiety disorders in German adolescents. J Anxiety Disord2000;14(3):263e79.

Evans D, Gray F, Leckman J. The rituals, fears and phobias of young children: in-sights from development, psychopathology and neurobiology. Child PsychiatryHum Dev 1999;29(4):261e76.

Flament M. Epidemiology of obsessive-compulsive disorder in children and ado-lescents. Encephale 1990;16:311e6.

Flament MF, Whitaker A, Rapoport JL, Davies M, Berg CZ, Kalikow K, et al. Obsessivecompulsive disorder in adolescence: an epidemiological study. J Am Acad ChildAdolesc Psychiatry 1998;27(6):764e71.

Fleitlich-Bilyk B, Goodman R. Prevalence of child and adolescent psychiatric dis-orders in southeast Brazil. J Am Acad Child Adolesc Psychiatry 2004;43(6):727e34.

Fontenelle LF, Mendlowicz MV, Versiani M. The descriptive epidemiology ofobsessive-compulsive disorder. Prog Neuropsychopharmacol Biol Psychiatry2006;30(3):327e37.

Fullana MA, Mataix-Cols D, Caspi A, Harrington H, Grisham JR, Moffitt TE, et al.Obsessions and compulsions in the community: prevalence, interference, help-seeking, developmental stability, and co-occurring psychiatric conditions. Am JPsychiatry 2009;166(3):329e36.

Fullana MA, Vilagut G, Rojas-Farreras S, Mataix-Cols D, de Graaf R, Demyttenaere K,et al. Obsessive-compulsive symptom dimensions in the general population:results from an epidemiological study in six European countries. J Affect Disord2010;124(3):291e9.

Hanna GL, Himle JA, Curtis GC, Gillespie BW. A family study of obsessive-compulsive disorder with pediatric probands. Am J Med Genet 2005;134(1):13e9.

Hasler G, Pinto A, Greenberg BD, Samuels J, Fyer AJ, Pauls D, et al. Familiality offactor analysis-derived YBOCS dimensions in OCD-affected sibling pairs fromthe OCD Collaborative Genetics Study. Biol Psychiatry 2007;61(5):617e25.

Heyman I, Fombonne E, Simmons H, Ford T, Meltzer H, Goodman R. Prevalence ofobsessive-compulsive disorder in the British nationwide survey of child mentalhealth. Br J Psychiatry 2001;179:324e9.

Hsu JC. Multiple comparisons: theory and methods. 1st ed. London (UK): Chapman& Hall/CRC; 1996.

Iervolino AC, Rijsdijk FV, Cherkas L, Fullana MA, Mataix-Cols D. A multivariate twinstudy of obsessive-compulsive symptom dimensions. Arch Gen Psychiatry2011;68(6):637e44.

Kim SJ, Lee HS, Kim CH. Obsessive-compulsive disorder, factor-analyzed symptomdimensions and serotonin transporter polymorphism. Neuropsychobiology2005;52(4):176e82.

Leckman JF, Evans EW. Origins of OCD: developmental and evolutionary perspec-tive. In: Cicchetti D, Cohen DJ, editors. Developmental Psychopathology. 2nd ed.New Jersey: John Wiley & Sons; 2006.

Leckman JF, Pauls DL, Zhang H, Rosario-Campos MC, Katsovich L, Kidd KK, et al.Obsessive-compulsive symptom dimensions in affected sibling pairs diagnosedwith Gilles de la Tourette syndrome. Am J Med Genet 2003;116B(1):60e8.

Liang K, Zeger SL. Longitudinal data analysis using generalized linear models. Bio-metrika 1986;73(1):13e22.

Mahfouz AA, Al-Gelban KS, Al Amri H, Khan MY, Abdelmoneim I, Daffalla AA, et al.Adolescents' mental health in Abha city, southwestern Saudi Arabia. Int J Psy-chiatry Med 2009;39(2):169e77.

Mataix-Cols D, Boman M, Monzani B, Rück C, Serlachius E, Långstr€om N, et al.Population-based, multigenerational family clustering study of obsessive-compulsive disorder. JAMA Psychiatry 2013;70(7):709e17.

McCullagh P, Nelder JA. Generalized linear models. 2nd ed. London UK: Chapman &Hall/CRC; 1989.

Milne BJ, Caspi A, Crump R, Poulton R, Rutter MR, Sears MR, et al. The validity of thefamily history screen for assessing family history of mental disorders. Am J MedGenet 2009;150(1):41e9.

Ros�ario-Campos MC, Miguel EC, Quatrano S, Chacon P, Ferrao Y, Findley D, et al. TheDimensional Yale-Brown Obsessive-Compulsive Scale (DY-BOCS): an instru-ment for assessing obsessive-compulsive symptom dimensions. Mol Psychiatry2006;11(5):495e504.

Ros�ario-Campos MC, Alvarenga PG, de Mathis A, Leckman JF. Obsessive-compulsivedisorder in childhood. In: Banaschewski T, Rohde LA, editors. Biological childpsychiatry. Recent trends and developments. Advances in biological psychiatry.1st ed. Basel: Karger; 2008.

Ruscio AM, Stein DJ, Chiu WT, Kessler RC. The epidemiology of obsessive-compulsive disorder in the National Comorbidity Survey Replication. MolPsychiatry 2010;15(1):53e63.

Salum GA, Gadelha A, Pan P, Moriyama TS, Graeff-Martins AS, Tamanaha AC, et al.High risk Cohort study for psychiatric disorders in childhood: rationale, design,methods and preliminary results. Int J Methods Psychiatr Res 2014 Dec 3.http://dx.doi.org/10.1002/mpr.1459.

Shams G, Foroughi E, Esmaili Y, Amini H, Ebrahimkhani N, Sheehan D, et al. Prev-alence rates of obsessive-compulsive symptoms and psychiatric comorbidityamong adolescents in Iran. Acta Med Iran 2011;49(10):680e7.

Stein MB, Forde DR, Anderson G, Walker JR. Obsessive-compulsive disorder in thecommunity: an epidemiologic survey with clinical reappraisal. Am J Psychiatry1997 Aug;154(8):1120e6.

Stewart SE, Rosario MC, Baer L, Carter AS, Brown TA, Scharf JM, et al. Four-factorstructure of obsessive-compulsive disorder symptoms in children, adolescents,and adults. J Am Acad Child Adolesc Psychiatry 2008;47(7):763e72.

Taberner J, Fullana MA, Caseras X, Pertusa A, Bados A, van den Bree M, et al. Areobsessive-compulsive symptom dimensions familial in nonclinical individuals?Depress Anxiety 2009;26(10):902e8.

Torres AR, Fontenelle LF, Ferr~ao YA, do Ros�ario MC, Torresan RC, Miguel EC, et al.Clinical features of obsessive-compulsive disorder with hoarding symptoms: amulticenter study. Psychiatry Res 2012;46(6):724e32.

Torresan RC, Ramos-Cerqueira AT, Shavitt RG, do Ros�ario MC, de Mathis MA,Miguel EC, et al. Symptom dimensions, clinical course and comorbidity in menand women with obsessive-compulsive disorder. Psychiatry Res 2013;209(2):186e95.

Valleni-Basile LA, Garrison CZ, Jackson KL, Waller JL, McKeown RE, Addy CL. Fre-quency of obsessive-compulsive disorder in a community sample of youngadolescents. J Am Acad Child Adolesc Psychiatry 1994;33(6):782e91.

Valleni-Basile LA, Garrison CZ, Waller JL, Addy CL, McKeown RE, Jackson KL, et al.Incidence of obsessive-compulsive disorder in a community sample of youngadolescents. J Am Acad Child Adolesc Psychiatry 1996;35(7):898e906.

Van den Heuvel OA, Remijnse PL, Mataix-Cols D, Vrenken H, Groenewegen HJ,Uylings HB, et al. The major symptom dimensions of obsessive-compulsivedisorder are mediated by partially distinct neural systems. Brain 2009;132(4):853e68.

van Grootheest DS, Boomsma DI, Hettema JM, Kendler KS. Heritability of obsessive-compulsive symptom dimensions. Am J Med Genet B Neuropsychiatr Genet2008;147B(4):473e8.

Vivan AD, Rodrigues L, Wendt G, Bicca MG, Braga DT, Cordioli AV. Obsessive-compulsive symptoms and obsessive-compulsive disorder in adolescents: apopulation-based study. Rev Bras Psiquiatr 2014;36(2):111e8.

Voltas N, Hern�andez-Martínez C, Arija V, Aparicio E, Canals J. A prospective study ofpaediatric obsessive-compulsive symptomatology in a Spanish communitysample. Child Psychiatry Hum Dev 2014;45(4):377e87.

Weissman MM, Wickramaratne P, Adams P, Wolk S, Verdeli H, Olfson M. Briefscreening for family psychiatric history: the family history screen. Arch GenPsychiatry 2000;57(7):675e82.

Zhang H, Leckman JF, Pauls DL, Tsai CP, Kidd KK, Campos MR. Genomewide scan ofhoarding in sib pairs in which both sibs have Gilles de la Tourette syndrome.Am J Hum Genet 2002;70(4):896e904.

Zohar AH, Ratzoni G, Pauls DL, Apter A, Bleich A, Kron S, et al. An epidemiologicalstudy of obsessive-compulsive disorder and related disorders in Israeli ado-lescents. J Am Acad Child Adolesc Psychiatry 1992;31(6):1057e61.