Abnormal involuntary movements are linked to psychosis-risk in children and adolescents: Results of a population-based study
Introduction
Psychoses have repeatedly been shown to lead to enormous disability and cost. The lifetime prevalence rate of all psychoses is estimated at 3–3.5% with a peak of first onset between the ages of 20 to 25, and an annual incidence of 0.035% (Kirkbride et al., 2006, Perala et al., 2007); 10 to 15% have an onset before the age of 18. Currently, early detection of and intervention in persons with initial signs of emerging psychosis is regarded as a promising strategy to reduce the burden of this disease (WHO, 2004). To this aim, two complementary sets of clinical high risk (CHR) criteria were developed on predominately adult samples: (1) “ultra-high risk” criteria (UHR) (McGlashan et al., 2010, Yung et al., 1996, Yung et al., 1998) including attenuated and brief intermittent psychotic symptoms and a combination of genetic risk factors and a recent significant functional decline; and (2) the basic symptom criteria (BS) “cognitive-perceptive basic symptoms” (COPER) (Klosterkotter et al., 2001) and “cognitive disturbances” (COGDIS) (Schultze-Lutter and Koch, 2010, Schultze-Lutter et al., 2012). Yet, recent studies indicate that CHR criteria may be less predictive of psychosis conversion in children and adolescents (Cornblatt et al., 2015, Schimmelmann et al., 2015, Schultze-Lutter et al., 2015), thus making the search for additional predictors to improve prognostic accuracy even more imperative in children and adolescents.
Altered motor behavior has consistently been reported in the schizophrenia literature (Bleuler, 1911, Kahlbaum, 1874, Kraepelin, 1899), including a wide range of motor symptoms. These comprehensive clinical descriptions were later neglected when scientific attention shifted to antipsychotic-related motor symptoms. The importance of motor symptoms has recently been rediscovered as symptoms were found in never-medicated patients (Cunningham Owens and Johnstone, 1980, Fenton et al., 1994, Walther and Strik, 2012) and first episode psychosis (Walther et al., 2014b). Movement patterns were predictive of the severity of positive symptoms, disorganization, and agitation in schizophrenia (Walther et al., 2014a). Furthermore, neuroimaging data demonstrated alterations in the human motor system in schizophrenia (Bracht et al., 2013, Walther et al., 2011). Among schizophrenia-related motor symptoms, abnormal involuntary movements have frequently been investigated (Pappa and Dazzan, 2009, Whitty et al., 2009). When these motor abnormalities occur prior to antipsychotic exposure, they are considered “Spontaneous Movement Abnormalities”, including dyskinesia and Parkinsonism (Pappa and Dazzan, 2009); presently we will use the term “Abnormal Involuntary Movements” (AIM). AIM comprise abnormal, involuntary, repetitive movements of the orofacial, limb, trunk, and respiratory musculature (Waddington, 1989) and have been detected in healthy relatives of patients with schizophrenia (Koning et al., 2010, Mittal et al., 2007b), as well as in help-seeking adolescents fulfilling UHR criteria (Mittal et al., 2008). In fact, several studies on UHR adolescents suggested that AIM were predictive of conversion (Callaway et al., 2014, Mittal et al., 2007a). Furthermore, in retrospective studies of schizophrenia patients, motor abnormalities could be traced into childhood (Walker et al., 1994), and in young offspring of schizophrenia patients, deficits in gross motor skills were reported to be predictive of schizophrenia-related psychoses in adulthood (Erlenmeyer-Kimling et al., 2000). Recent studies indicated that AIM in CHR reflect striatal pathology (Dean and Mittal, 2015) and are associated with poorer psychosocial (Mittal et al., 2011) and cognitive functioning (Howes et al., 2009, Mittal et al., 2010).
However, the association of abnormal involuntary movements and CHR in psychosis has not been investigated in population-based samples of children and adolescents from the community. With respect to both CHR and AIM status, selected samples of help-seeking persons must be assumed a non-representative minority of the CHR/AIM population. In contrast, population based epidemiological studies additionally provide information on non-help-seeking individuals, which might be of particular value for the development of effective preventive strategies.
Therefore, we tested whether the frequency of AIM differs in children and adolescents from the community with and without CHR to develop psychosis. Moreover, we investigated whether AIM were associated with disturbances in social functioning, cognition or psychopathology beyond the CHR state.
Section snippets
Sample
The sample was part of the Binational Evaluation of At-Risk Symptoms in Children and Adolescents, BEARS-Kid study (Schimmelmann et al., 2015). Stratified sampling by sex (1:1) was used to randomly select potential participants aged 8–17 years from approximately 384,000 persons of this age group included in the obligatory population register of Canton Bern, Switzerland. The local ethics committee approved the study. Written informed assent/consent was provided by participants and their parents.
Sample
Of the 102 participants (age range from 8.6 to 17.9 years), 11 (10.8%) fulfilled CHR criteria (no BIPS, 6 APS only, 3 COPER only, 2 COPER and COGDIS), 13 (12.7%) fulfilled criteria of increased AIM (AIMS ≥ 2; see Table 1). The distribution of AIMS scores is shown in Fig. S1. While the CHR group contained only females, there was no effect of gender on AIMS total scores (p = 0.7, z = − 0.41), or on presence of AIM (see Table 1). There were no differences in other demographic variables.
CHR state and AIM
Total AIMS scores
Discussion
This is the first study investigating the prevalence of spontaneous Abnormal Involuntary Movements (AIM) in children and adolescents from the general population. Our study gives initial support to the notion that an increased risk of psychosis risk in children and adolescents is associated with movement abnormalities, not only in clinical or genetic high-risk samples but also in children and adolescents randomly selected from the community. Individuals at CHR showed both increased total AIMS
Ethical standards
The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008.
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