Conditional associations between childhood cat ownership and psychotic experiences in adulthood: A retrospective study

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Abstract

Ownership of cats in childhood has been inconsistently associated with psychosis in adulthood. Parasitic exposure, the putative mechanism of this association, may be more common with rodent-hunting cats, and its association with psychosis may depend on other environmental exposures. We examined the conditional associations between childhood cat ownership and the frequency of psychotic experiences in adulthood. Adults (n = 2206) were recruited in downtown Montreal to complete a survey about childhood cat ownership (non-hunting or rodent-hunting), winter birth, residential moves in childhood, head trauma history, and tobacco smoking. The frequency of psychotic experiences (PE) was measured with the 15-item positive subscale of the Community Assessment of Psychic Experiences. Associations between exposures and PE were examined in linear regressions adjusted for age and sex. Interactions among variables were explored using a conditional inference tree. Rodent-hunting cat ownership was associated with higher PE scores in male participants (vs. non-hunting or no cat ownership: SMD = 0.57; 95% CI: 0.27, 0.86), but not in female participants (SMD = 0.10; 95% CI: −0.18, 0.38). In the conditional inference tree, the highest mean PE score was in the class comprised of non-smokers with >1 residential move, head trauma history, and rodent-hunting cat ownership (n = 22; mean standard score = 0.96). The interaction between rodent-hunting cat ownership and head trauma history was supported by a post-hoc linear regression model. Our findings suggest childhood cat ownership has conditional associations with psychotic experiences in adulthood.

Introduction

Toxoplasma gondii is a candidate causal risk factor for psychosis. This protozoan parasite is typically transmitted to humans by domestic cats (Dubey, 1998). A seminal case-control study by Torrey and Yolken (1995) showed an association between cat ownership during childhood and the risk for severe mental illness in adulthood. Subsequently, it was found that seropositivity for T. gondii is associated with a greater number of psychotic experiences in the general population (Lindgren et al., 2018), and with a higher risk for schizophrenia (Sutterland et al., 2015). Additional evidence comes from animal research showing, for example, that T. gondii infection is associated with activated microglia and synaptic loss (Carrillo et al., 2020), two mechanisms that are thought to be involved in the pathogenesis of schizophrenia in humans (Howes and McCutcheon, 2017). Other studies, however, could not demonstrate an association between cat ownership and psychotic experiences in humans (e.g., Bedwell et al., 2020).

The association between cat ownership and psychotic experiences may be conditional on other factors. Domestic cats generally become infected with the parasite by feeding on rodents, and will only be contagious during the days or weeks that follow (Dubey, 1998). Hence, specifying whether the cat was known to hunt rodents might provide a better proxy for probable exposure to T. gondii compared to cat ownership alone. Another consideration is that the association between cat ownership and psychotic experiences may be sexually dimorphic: studies in humans have identified male-specific associations between T. gondii infection and behavior or physiology (Flegr et al., 2008, 2011). Further, as suggested by the multi-hit model of schizophrenia (Davis et al., 2016; Howes and McCutcheon, 2017), the presence or absence of other environmental risk factors may influence the association between cat ownership and psychosis expression.

Identifying interactions among environmental exposures is an analytical challenge. Environmental risk factors for psychosis are largely interconnected (Guloksuz et al., 2018; Paquin et al., 2020). The ability of common statistical models, such as linear regressions, to detect interactions will depend on the data analyst's decisions of which covariables to include, and which interactions to test for (Guloksuz et al., 2018; Venkatasubramaniam et al., 2017). Decision tree learning is a statistical approach that allows data-driven exploration of interactions among predictor variables, which are selected by means of an algorithm. This approach generates tree-shaped models of the outcome's distribution according to the status of selected predictor variables (Hothorn et al., 2006; Venkatasubramaniam et al., 2017). This simple approach to machine learning can uncover potential interactions among predictors and identify subgroups of participants who share homogeneous exposure profiles and symptom levels.

Using retrospective assessments of environmental exposures in a community sample, we first aimed to examine the association between rodent-hunting cat ownership in childhood and psychotic experiences in adulthood. Second, we evaluated whether this association was sexually dimorphic. Third, using decision tree learning, we explored potential interactions between cat ownership and other risk factors for psychotic experiences.

Section snippets

Participants

This retrospective study was conducted as part of the EnviroGen project, the aim of which was to characterize environmental and genetic risk factors for psychosis (King et al., 2005). Adults were approached in public places in downtown Montreal, Canada to complete a questionnaire about “unusual psychic experiences”. Participants were required to be between 18 and 40 years of age and to live in the greater Montreal area. Participants were offered a 1:25 chance of winning $50 if they provided

Descriptive statistics and correlations

Of 3208 participants deemed eligible, 2470 agreed to complete the questionnaire (77.0% acceptance), and of those, 2206 were confirmed to be eligible. In the total sample (n = 2206), there was no missing data on PE but 7–26% missing data on the exposure variables. Participants included in primary analyses were those with complete data (n = 1986; 90.0% of the sample).

Descriptive analyses are presented in Table 1. The mean PE score was 1.46 (SD = 0.30). Based on the descriptive statistics and

Discussion

Cat ownership in childhood was associated with greater psychosis expression in adulthood, but only in presence of certain factors. Rodent-hunting cat ownership was associated with higher PE scores compared to non-hunting or no cat ownership, which is consistent with our hypothesis based on the life cycle of T. gondii as the putative mechanism of this association. By using a more granular proxy for parasitic exposure, our study brings a new perspective on previously mixed associations between

Data access

The data that support the findings of this study are available on request from the corresponding author, S.K. The data are not publicly available due to their containing information that could compromise the privacy of research participants.

Funding

This project was funded by grants to S.K., R.J. and N.S. from the Fonds de recherche en santé du Québec (Quebec Health Research Fund, FRQS). The funding source had no involvement in the study design, nor in the collection, analysis and interpretation of data.

Author statement

V.P. and S.K. formulated the research questions. S.K. designed the study and carried it out. V.P. analysed the data and drafted the manuscript. G.E. and A.C. oversaw the analyses. All authors revised and approved the final version of the manuscript.

Declaration of competing interest

The authors have no conflict of interest to declare.

Acknowledgements

The authors thank Patrice Grondin for the initial idea of considering the rodent-hunting behavior of cats in the context of psychosis risk. We also thank the research assistants who collected the data from Montrealers: Anna Fukuda, Jessica Diamond, Michelle Goudreau, Amélie Barras, Sylvain Lemieux, Sherry Abadie, Pascale Le Hir, Luc Valiquette, and Eric Chetrit. Nicole Pawliuk did initial entry and cleaning of the data.

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