Psychiatry 77(1) Spring 2014
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Olfaction Across the Schizophrenia Spectrum Auster et al.
Objective and Subjective Olfaction Across the Schizophrenia Spectrum Tracey L. Auster, Alex S. Cohen, Dallas A. Callaway, and Laura A. Brown
Much research indicates that patients with schizophrenia have impaired olfaction detection ability. However, studies of individuals with psychometrically defined schizotypy reveal mixed results—some document impairments while others do not. In addition to deficits in objective accuracy in olfaction for patients with schizophrenia, there has been an interest in subjective experience of olfaction. Unfortunately, methods of assessing accuracy and subjective hedonic olfactory evaluations in prior studies may not have been sensitive enough to detect group differences in this area. This study employed a measure of olfactory functioning featuring an expanded scoring system to assess both accuracy and subjective evaluations of pleasant and unpleasant experience. Data were collected for patients with schizophrenia, young adults with psychometrically defined schizotypy, psychiatric outpatients, and healthy controls. Results of this study indicate that both the schizophrenia and outpatient psychiatric groups showed similar levels of impaired olfaction ability; however, the schizotypy group was not impaired in olfaction detection. Interestingly, with regard to subjective hedonic evaluation, it was found that patients with schizophrenia did not differ from psychiatric outpatients, whereas individuals with schizotypy tended to rate smells as significantly less pleasant than healthy control participants. This suggests that subjective olfactory assessment is abnormal in some manner in schizotypy. It also suggests that accuracy of olfaction identification may be a characteristic of severe mental illness across severe mental illness diagnoses. The results are potentially important for understanding olfaction deficits across the mental illness spectrum. A relatively large literature suggests that patients with schizophrenia have impaired ability to identify and discriminate among various scents on the order of a full standard deviation (Brewer & Pantelis, 2010; Turetsky & Moberg, 2009; Wu et al., 1993). Given the magnitude of this deficit, it has been proposed that olfaction
deficits also reflect a vulnerability marker for schizophrenia-spectrum disorders. Related to this, there is a strong background of existing literature that links negative symptoms of schizophrenia to olfaction accuracy (Ishizuka et al., 2010). Often, negative symptoms are specifically linked to the first episode of psychosis (Corcoran et al., 2005). Given the
Tracey L. Auster, MA, Alex S. Cohen, PhD, Dallas A. Callaway, MA, and Laura A. Brown, MA, are affiliated with the Institute of Research, Department of Psychology, Louisiana State University, Baton Rouge, Louisiana. Address correspondence to Tracey L. Auster, Louisiana State University, Department of Psychology, 322 Audubon Hall, Baton Rouge, LA 70803. E-mail: [email protected] © 2014 Washington School of Psychiatry
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heterogeneous nature of schizophrenia (Cohen & Docherty, 2005), decoupling differences between symptoms and objective and subjective olfaction is a difficult feat, making it even more important to determine patterns in those at risk in order to guide early intervention. However, studies examining olfaction in individuals at elevated risk for schizophrenia-related illnesses have reported mixed results, some documenting impairment (Turetsky & Moberg, 2009; Turetsky, Moberg, Arnold, Doty, & Gur, 2003) and others finding no differences relative to controls (Compton & Chien, 2008; Kamath & Bedwell, 2008). Therefore, the first aim of the present study was to address the question of whether olfaction deficits reflect a vulnerability marker for those at putative risk for schizophrenia by directly comparing olfaction functions in stable outpatients with schizophrenia, psychiatric outpatients with serious mental illness other than schizophrenia, individuals with psychometrically defined schizotypy, and healthy controls. Considering the aforementioned inconsistency in findings in schizotypy across studies, it is important to consider whether previous research has used sensitive enough measures to assess olfaction. The University of Pennsylvania Smell Identification Test (UPSIT) had been the standard research measure of olfaction accuracy in both schizophrenia and schizotypy research (Cohen, Brown & Auster, 2012; Moberg et al., 1999). The UPSIT is a recognition-based test with a strong empirical backing for use in patient populations; to our knowledge, however its use in higher functioning populations is less clear. Consider that the recommended criteria denoting impairments is 87% correct (35 of 40 for women; 34 of 40 for men), suggesting that it is a relatively easy test even for patients with relatively severe impairments (see K. L. Minor, Wright, & Park, 2004). In this regard, it may lack sufficient discriminability for detecting differences in higher functioning populations. In the present study, we adapted a commonly used olfaction test (i.e., the “Sniffin’ Sticks” test; Hummel, Sekinger,
Auster et al.
Wolf, Pauli, & Kobal, 1997), to allow for free recall in addition to recognition, with the notion that this would expand the potential scoring range and provide a more sophisticated evaluation of olfaction deficits across the schizophrenia spectrum. In addition to accuracy deficits found in olfaction across the schizophrenia spectrum, there has been emerging interest in subjective experience of olfaction. While considerably less researched compared to olfaction deficits more generally, results from a handful of studies examining subjective ratings of hedonic experience of olfaction stimuli suggest that schizophrenia patients report smells as being less pleasant compared to controls (Kamath, Turetsky, & Moberg, 2011; Moberg et al., 2003). Related to this, Doop and Park (2006) reported that patients with schizophrenia have a more limited range of pleasant smells compared to controls. Findings for subjective experience of olfaction in individuals at risk for schizophrenia are even more limited, with one study failing to find differences in subjective experience between 13 biological family members of patients and 26 controls (Schneider et al., 2000). In this regard, a study directly comparing subjective experience of olfaction in patients with schizophrenia and in those at risk for schizophrenia would be a critical entry to this literature. Additionally, there is the question of whether olfaction deficits are specific to the schizophrenia spectrum or whether they reflect a symptom of severe mental illness more generally. Of note, olfaction deficits have been reported, albeit somewhat inconsistently, in patients with mood disorders compared to controls (Amsterdam, Settle, Doty, Abelman, & Winokur, 1987; Gross-Isseroff et al., 1994; Negoias et al., 2010; Pause, Miranda, Goder, Aldenhoff, & Ferstl, 2001). With respect to the subjective deficits, the findings have been more mixed, with some studies suggesting that patients with nonpsychotic affective disorders report more positive experiences with olfaction stimuli (Cumming, Matthews, & Park, 2010) and others indi-
Olfaction Across the Schizophrenia Spectrum 59
cate a less positive report (Negoias et al., 2010) compared to control groups. The final aim of our study was to explore how a psychiatric group, comprising stable outpatients with serious mental illness but not schizophrenia, compared to a schizophrenia group in olfaction deficits. The issue of how subjective olfaction ratings manifest in schizophrenia-spectrum disorders versus those with serious mental illness is a topic that, to our knowledge, has not yet been broached. This study examined the results of a measure of olfaction using an expanded scoring system in stable outpatients with and without schizophrenia, healthy controls, and individuals at elevated risk for developing schizophrenia-spectrum disorders, defined using validated psychometric procedures. The at-risk group was recruited from a university setting, which is advantageous in that use of a relatively healthy sample reflects a conservative test of the hypothesis that olfaction deficits are a vulnerability marker of schizophrenia pathology. In sum, our aims were to evaluate potential differences in detection of and subjective appraisal of olfaction for those with psychometrically defined schizotypy, those with schizophrenia, a healthy control group, and a psychiatric outpatient group. METHODS
Participants Four groups of participants were recruited for this study. Two groups were recruited from a community mental health center and were diagnosed with either schizophrenia (n = 31) or unipolar (n = 13) or bipolar (n = 12) affective disorders; they were diagnosed using the Structured Clinical Interview for DSM-IV (SCID; Lobbestael, Leurgans, & Arntz, 2011; Steiner, Tebes, Sledge, & Walker, 1995). Inclusion criteria included being 18–55 years of age, a Global Assessment of Functioning Scale (GAF) score
> 30, no current diagnosis of substance dependence (based on the SCID), and no neurological disease or head injury sufficient to cause overt neurocognitive deficits (based on patient records and self-report). The present data were included in a recent meta-analysis examining olfaction performance in schizophrenia and schizotypy (Cohen et al., 2012). Additionally, schizotypy and healthy adult control groups were recruited from a university setting. The Schizotypy Personality Questionnaire-Brief (SPQ-B; Raine & Benishay, 1995) was used to screen individuals. There is evidence that schizotypy accounts for 10% of the population (see Lenzenweger, 2006, for a conceptual review); we therefore used a strategy wherein the top 5% of scorers (1.65 standard deviations [SD] from the ethnicity and gender-determined means) on the SPQ-B subscales were contacted to participate in the laboratory segment of the study. Based on scores at the sex and ethnicity-derived 95th percentile or above on the positive, negative, or disorganized subscales, a schizotypy group was identified and recruited (n = 79). Additionally, a healthy control group (n = 34) was identified that had SPQ-B scores lower than the mean for each of the subscales (see Cohen, Callaway, Najolia, Larsen, & Strauss, 2011, for more details regarding recruitment). Selected participants were contacted via e-mail or phone by research assistants and asked to undergo an in-person testing session in our laboratory. All participants involved in the laboratory phase of the study were compensated $20. Measures Clinical Measures. The SCID for Axis I disorders (SCID-I; Steiner et al., 1995), the gold standard for clinical diagnosis, was used in this study. Diagnoses and symptom ratings were made using a consensus procedure led by Dr. Alex Cohen. In this manner, full interrater agreement was assured for each case. The Brief Psychiatric Rating Scale (BPRS; Lukoff, Nuechterlein, & Ventura, 1986)
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TABLE 1. Descriptive Statistics for the Demographic and Clinical Variables Across the Patient and Nonpatient Groups
% Women % Caucasian
Psychiatric Outpatient Group
Schizophrenia
Healthy Controls
Schizotypy
42
39
44
42
69
34
85
80
Age
45.96 ± 9.82
39.41 ± 10.80
19.89 ± 5.56
19.35± 1.67
Education
12.46 ± 2.67
11.47 ± 2.20
13.34 ± 0.59
13.66 ± 0..83
Mania/Excitement
10.0 ± 5.3
10.34 ±4.57
Negative
6.72 ± 2.92
8.53 ±3.65
Positive
7.8 ± 2.97
12.12 ± 5.27
BPRS Factor Scores
SPQ-B Scores Positive
–12.95 ± 3.63
2.85 ± 5.58
Negative
–13295 ± 2.88
4.24 ± 6.16
Disorganization
–10.74 ± 2.16
44.11 ± 4.39
is a standard assessment of 24 symptoms and was used to evaluate symptom severity across patient groups. Factor subscale scores reflecting positive (i.e., bizarre behavior, suspiciousness, unusual thought content, disorientation, and hallucinations items), negative (i.e., self-neglect, blunted affect, motor retardation, and emotional withdrawal items), depressive (i.e., depression, guilt, suicidality, and anxiety items), and mania/excitement (i.e., motor hyperactivity, elevated mood, excitement, distractibility, hostility, and grandiosity items) symptoms (defined in Ventura, Nuechterlein, Subotnik, Gutkind, & Gilbert, 2000) were employed here. Schizotypal Personality Questionnaire. The Schizotypal Personality Questionnaire-Brief (SPQ-B; Raine & Benishay, 1995) was used to identify individuals with psychometrically defined schizotypy. The SPQ-B is a 22-item instrument based on the original 74-item SPQ (Raine, 1991). The SPQ is one of the most commonly used measures for assessing schizotypy (Stefanis, Smyrnis, Avramopoulos, Ntzoufras, & Stefanis, 2004). Data reported here (see Table 1) display means
for participants broken down by those at the 95th percentile or above on the positive, negative, or disorganized subscales. We chose to administer the SPQ-B because of its brevity, as the SPQ-B has been shown to lead to fewer incomplete responses compared to the full SPQ (Cohen, Matthews, Najolia, & Brown, 2010). Olfaction Ability. The “Sniffin’ Sticks,” used in the present study, is an olfaction assessment measure developed in the 1990s to detect olfaction ability and discrimination (Hummel et al., 1997). The measure includes 12 different pens with a wide variety of smells (e.g., orange, leather). To expand the sensitivity of this measure to test our predictions, we modified the scoring protocol by adding a free recall phase before the recognition protocol. First, participants were asked to freely identify each smell. If the response was incorrect, participants were then provided a recognition response set that asked them to identify the smell from four options. Participants were awarded two points for a correct recall response and one point for a correct recognition response. To evaluate
Olfaction Across the Schizophrenia Spectrum 61
subjective experience of responses, participants were separately asked “How pleasant was this scent to you?” and “How unpleasant was this scent to you?” with answers for each question chosen from a diagram illustrating a 7-point Likert-type scale with anchors ranging from 1 (not at all) to 7 (extremely pleasant/unpleasant). The Sniffin’ Sticks measure has been used with patient and healthy control populations and has demonstrated adequate reliability and validity (Landis, Knecht, Huttenbrink, Lacroix, & Hummel, 2005; Negoias et al., 2010; Swiecicki et al., 2009). Analyses Analyses were conducted in four steps. First, we compared groups on age, sex, and ethnicity and compared BPRS and GAF scores to determine whether there were any potential demographic or clinical confounds that should be controlled for. Second, we compared the four groups on olfaction performance using an analysis of variance (ANOVA). Third, we compared the four groups on subjective experience of the olfaction stimuli using an ANOVA. For the second and third analyses, we predicted that, in line with the current literature, we would find deficits in accuracy and hedonic evaluation of olfaction for those with schizophrenia as compared to the psychiatric group without psychosis. We also hypothesized that we would see deficits in accuracy and hedonic evaluation for those with schizotypy compared to the healthy control group. The patient and nonpatient groups were also compared to each other, although a priori predictions were not made. Finally, we computed correlations between BPRS symptom factors and olfaction variables for the schizophrenia group and SPQ factors and the olfaction variables for the schizotypy group. This comparison evaluated whether olfaction deficits were associated with specific schizophrenia/schizotypy symptoms.
RESULTS
Demographic Variables Table 1 contains demographic and clinical information. Within the total sample, age was significantly different across groups, F(3, 173) = 156.2, p < .01. Age was significantly higher for the patient groups compared to the schizotypy and healthy control groups (ps < .05). Education levels were significantly different across groups, F(3, 173) = 17.63, p < .01. These education levels were significantly higher for the healthy control and schizotypy groups compared to the patient groups (ps < .05). The schizophrenia versus patient control group had significantly more severe BPRS negative and positive symptoms (ts[55] = 2.03 and 3.67, ps < .05), but the groups were not statistically dissimilar with respect to other BPRS symptom factors (ps > .10). Smoking status, sex, age, and education were not significantly related to any of the dependent measures in this study. There were no statistically significant differences on subjective or objective olfaction ratings between unipolar and bipolar patients and the psychiatric outpatient group. Olfactory Accuracy Variables Across Groups A one-way ANOVA comparing the four groups revealed a significant difference between groups in olfaction accuracy, F(3, 175) = 36.02, p < 01. The post hoc t tests revealed that the psychiatric outpatient group and the schizophrenia group were impaired in olfaction ability compared to the schizotypy and healthy control groups (ps < .05), but the groups did not differ from each other (ps > .05) (see Figure 1).
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FIGURE 1. Average accuracy means. Higher means represent higher accuracy. Brackets denote which groups were significantly different from each other.
Subjective Olfaction Variables Across Groups A one-way ANOVA comparing the four groups also revealed a significant difference between groups on subjective rating of smells, F(3, 165) = 2.10, p < .05. The results of post hoc comparisons indicated that both patient groups (psychiatric outpatient and schizophrenia) showed similar levels of subjective olfactory evaluation (see Table 1). The schizotypy group was associated with less pleasant ratings compared to the healthy control participants (ps < .05) (see Figure 2). Bivariate Correlations Between Olfaction Ratings and Symptom Ratings Negative BPRS factor scores and negative SPQ scores were correlated with subjective smell ratings, suggesting that negative symptoms were related to negative evaluation of smell. This suggests that the greater the negative symptoms, the poorer the participants rated hedonic experience of smell. See Table 2 for additional correlations between BPRS symptoms and SPQ symptoms and objective and subjective olfaction rat-
ings. Olfaction scores, both objective and subjective, were not significantly associated with any other symptoms or trait scores. DISCUSSION
The present study was designed to address inconsistency in the literature regarding whether olfaction deficits reflect a vulnerability marker of the schizophrenia spectrum. This study is the first to our knowledge to evaluate olfaction both in patients with schizophrenia and in individuals with psychometrically defined schizotypy. There were three major findings from this study. First, individuals with psychometrically defined schizotypy showed no objective olfaction deficits compared to the healthy control group, and these groups were significantly more accurate in objective smell ratings compared with both outpatient groups. This finding argues against claims that deficits in olfaction identification reflect a vulnerability marker of those with psychometric schizotypy. While it may be true that olfaction inaccuracy is a marker for those at ultrahigh risk, it is unlikely that the lack of group differences reflects a sensitivity issue for this population on the schizophrenia spectrum,
Olfaction Across the Schizophrenia Spectrum 63
FIGURE 2. Average pleasant ratings across groups. Higher means represent higher pleasant rating of smell. Brackets denote which groups were significantly different from each other.
because the measure of olfaction employed in this study was probably more sensitive than those used in prior studies. In support of this conclusion, note that the healthy controls received, on average, less than half of the potential points for the identification trials. In contrast, the demarcation for poor performance on the UPSIT is approximately 87% correct (Minor et al., 2004). Second, there was a distinct pattern for subjective in-the-moment hedonic experience of olfaction stimuli for those with schizotypy compared to matched controls. The schizotypy group reported smells as subjectively less pleasant than controls, indicating that there is a difference for the at-risk group in comparative emotional experience. Interestingly, and consistent with prior studies (see Minor & Cohen, 2010, for a review), patients with schizophrenia do not generally show reduced hedonic experience of olfactory stimuli in the laboratory (Berenbaum, 1992). Thus, there appears to be a discrepancy regarding experience in patients with schizophrenia and those with psychometrically defined schizotypy. That is, university students with psychometrically defined schizotypy are more pathological compared to older chronic patients with schizophrenia with regard to hedonic olfactory experience. The resolution to this discrepancy is not im-
mediately clear, although it is worth noting that individuals with schizotypy have reported less pleasant experience in reaction to in-the-moment evaluation of visual images in another study from our laboratory (Cohen et al., 2011). Further research regarding this discrepancy seems an important endeavor. Third, as supported by the previous research, we found that individuals with schizophrenia are impaired in olfaction identification. Interestingly, the psychiatric outpatient group, comprising individuals with mood disorders, revealed a similar impairment consistent with the literature, which raises questions about the specificity of olfaction deficits in schizophrenia. Previous research indicates impairment of objective olfaction in those with mood disorders (Pause et al., 2001). The similarities in these heterogeneous groups provide credence to the theory that olfactory impairment may be a symptom of general serious mental illness, not just a schizophrenia-specific phenomenon. Limitations of these results must be noted based on inequitable sample sizes, with the schizotypy group being much larger than all other groups. We were unable to control for some factors that may affect smell, including specific allergies, smoking, or perfumes, due to lack of comprehensive
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TABLE 2. Bivariate Correlations Between Schizophrenia Spectrum Symptoms and Objective Olfaction Ratings Olfaction Accuracy
Olfaction Subjective Pleasant Rating
.08
.11
BPRS Negative
–.37**
–.37**
BPRS Positive
–.02
–.07
BPRS Depression
.14
–.64
Schizophrenia Group and Psychiatric Outpatient Group (n = 59) BPRS Mania
Schizotypy and Healthy Controls (n = 117) SPQ-B Positive
–.05
–.16
SPQ-B Negative
–.04
–.28**
SPQ-B Disorganized
.06
–.21
Note. **Correlation is significant at .01 levels (two-tailed).
detail on these variables. These data suggest an overall accuracy deficit among those with serious mental illness and also a subjective difference in olfaction experiences for those at risk for schizophrenia. In the future, it may be important to consider these variables as potential confounds. Future research should explore this distinct difference for those with schizotypy and elaborate how subjective ex-
perience of olfaction directly relates to psychiatric risk and vulnerability. This research may inform identification of illness susceptibility, and therefore be important to consider in early intervention. The present data highlight the need to explore whether olfaction accuracy deficits are distinct to those withschizophrenia or are characteristic of those with psychiatric illness generally.
REFERENCES Amsterdam, J. D., Settle, R. G., Doty, R. L., Abelman, E., & Winokur, A. (1987). Taste and smell perception in depression. Biological Psychiatry, 22(12), 1481–1485. Berenbaum, H. (1992). Posed facial expressions of emotion in schizophrenia and depression. Psychological Medicine, 22(4), 929–937. Brewer, W. J., & Pantelis, C. (2010). Olfactory sensitivity: Functioning in schizophrenia and implications for understanding the nature and progression of psychosis. Vitamins and Hormones, 83, 305–329. doi:10.1016/S0083-6729(10)83013-4 Cohen, A. S., Brown, L. A., & Auster, T. L. (2012). Olfaction, “olfiction,” and the schizophrenia spectrum: An updated meta-analysis on identification and acuity. Schizophrenia Research, 135(1– 3), 152–157. doi:10.1016/j.schres.2011.12.005 Cohen, A. S., Callaway, D. A., Najolia, G. M., Larsen, J. T., & Strauss, G. P. (2011). On “risk” and reward: Investigating state anhedonia in psychometrically defined schizotypy and schizophre-
nia. Journal of Abnormal Psychology, 121(2), 407–415. doi:10.1037/a0026155 Cohen, A. S., Dinzeo, T. J., Nienow, T. M., Smith, D. A., Singer, B., & Docherty, N. M. (2005). Diminished emotionality and social functioning in schizophrenia. Journal of Nervous and Mental Disorders, 193(12), 796–802. doi:10.1037/ a0026155 Cohen, A. S., & Docherty, N. M. (2005). Symptom-oriented versus syndrome approaches to resolving heterogeneity of neuropsychological functioning in schizophrenia. Journal of Clinical Psychology, 17(3), 384–390. doi:10.1176/appi. pn.2013.4b2 Cohen, A. S., Matthews, R. A., Najolia, G. S., & Brown, L. A. (2010). Toward a more psychometrically sound brief measure of schizotypal traits: Introducing the SPQ Brief Revised. Journal of Personality Disorders, 24(4), 516–537. doi:10.1521/pedi.2010.24.4.516 Compton, M. T., & Chien, V. H. (2008). No association between psychometrically-determined
Olfaction Across the Schizophrenia Spectrum 65
schizotypy and olfactory identification ability in first-degree relatives of patients with schizophrenia and non-psychiatric controls. Schizophrenia Research, 100(13), 216–223. doi: 10.1016/j. schres.2007.11.021
Landis, B. N., Knecht, M., Huttenbrink, K. B., Lacroix, J. S., & Hummel, T. (2005). Clinical aspects of dysosmia and presentation of European Olfactory Test of “Sniffin Sticks”: A review. Journal of Otolaryngology, 34(2), 86–92.
Corcoran, C., Whitaker, A., Coleman, E., Fried, J., Feldman, J., Goudsmit, N., & Malaspina, D. (2005). Olfactory deficits, cognition and negative symptoms in early onset psychosis. Schizophrenia Research, 80(2–3), 283–293.
Lenzenweger, M. F. (2006). Schizotaxia, schizotypy, and schizophrenia: Paul E. Meehl’s blueprint for the experimental psychopathology and genetics of schizophrenia. Journal of Abnormal Child Psychology, 115, 195–220.
Cumming, A. G., Matthews, N. L., & Park, S. (2010). Olfactory identification and preference in bipolar disorder and schizophrenia. European Archives of Psychiatry and Clinical Neurosciences, 261(4), 251–259 .doi:10.1007/s00406 010-01457
Lobbestael, J., Leurgans, M., & Arntz, A. (2011). Inter-rater reliability of the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID I) and Axis II Disorders (SCID II). Clinical Psychology & Psychotherapy, 18(1), 75–79. doi:10.1002/ cpp.693
Doop, M. L., & Park, S. (2006). On knowing and judging smells: Identification and hedonic judgment of odors in schizophrenia. Schizophrenia Research, 81(2–3), 317–319. doi:10.1016/j. schres.2005.08.006
Lukoff, D., Nuechterlein, K. H., & Ventura, J. (1986). Manual for the expanded Brief Psychiatric Rating Scale (BPRS). Schizophrenia Bulletin, 12, 594–602.
Gross-Isseroff, R., Luca-Haimovici, K., Sasson, Y., Kindler, S., Kotler, M., & Zohar, J. (1994). Olfactory sensitivity in major depressive disorder and obsessive compulsive disorder. Biological Psychiatry, 35(10), 798–802. doi: 10.1016/00063223(94)91142-8 Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., & Kobal, G. (1997). ‘Sniffin’ Sticks’: Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chemical Senses, 22(1), 39–52. Ishizuka, K., Tajinda, K., Colantuoni, C., Morita, M., Winicki, J., Le, C., . . . Cascella, N. G. (2010). Negative symptoms of schizophrenia correlate with impairment on the University of Pennsylvania smell identification test. Neuroscience, 66(1), 106–110. doi:10.1016/j.neures.2009.10.001 Kamath, V., & Bedwell, J. S. (2008). Olfactory identification performance in individuals with psychometrically defined schizotypy. Schizophria Research, 100(1–3), 212–215. doi:10.1016/j. schres.2007.10.008 Kamath, V., Turetsky, B. I., & Moberg, P. J. (2011). Identification of pleasant, neutral, and unpleasant odors in schizophrenia. Psychiatry Research, 187(1–2), 30–35. doi:10.1016/j.psychres.2010.12.011
Minor, K. L., Wright, B. D., & Park, S. (2004). The Smell Identification Test as a measure of olfactory identification ability in schizophrenia and healthy populations: A Rasch psychometric study. Journal of Abnormal Psychology, 113(2), 207– 216. doi:10.1037/0021-843X.113.2.207 Minor, K. S., & Cohen, A. S. (2010). Affective reactivity of speech disturbances in schizotypy. Journal Psychiatry Research, 44(2), 99–105. doi:10.1016/j.jpsychires.2009.06.005 Moberg, P. J., Agrin, R., Gur, R. E., Gur, R. C., Turetsky, B. I., & Doty, R. L. (1999). Olfactory dysfunction in schizophrenia: A qualitative and quantitative review. Neuropsychopharmacology, 21(3), 325–340. doi:10.1016/S0893133X(99)00019-6 Moberg, P. J., Arnold, S. E., Doty, R. L., Kohler, C., Kanes, S., Seigel, S., . . . Turetsky, B. I. (2003). Impairment of odor hedonics in men with schizophrenia: Comparative study. American Journal of Psychiatry, 160(10), 1784–1789. Negoias, S., Croy, I., Gerber, J., Puschmann, S., Petrowski, K., Joraschky, P., & Hummel, T. (2010). Reduced olfactory bulb volume and olfactory sensitivity in patients with acute major depression. Neuroscience, 169(1), 415–421. doi:10.1016/j.neuroscience.2010.05.012
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Overall, J. E., & Gorham, D. R. (1962). The Brief Psychiatric Rating Scale. Psychological Reports, 10, 799–812. Pause, B. M., Miranda, A., Goder, R., Aldenhoff, J. B., & Ferstl, R. (2001). Reduced olfactory performance in patients with major depression. Journal of Psychiatry Reseach, 35(5), 271–277. doi:10.1016/S0022-3956(01)00029-2 Raine, A. (1991). The SPQ: A scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophrenia Bulletin, 17, 555–564. Raine, A., & Benishay, D. (1995). The SPQ-B: A brief screening instrument for schizotypal personality disorder. Journal of Personality Disorders, 9, 346–355. Schneider, F., Habel, U., Reske, M., Toni, I., Falkai, P., & Shah, N. J. (2000). Neural substrates of olfactory processing in schizophrenia patients and their healthy relatives. Psychiatry Research: Neuroimaging, 155(2), 103–112. doi:10.1016/j. pscychresns.2006.12.004 Stefanis, N. C., Smyrnis, N., Avramopoulos, D., Evdokimidis, I., Ntzoufras, I., & Stefanis, C. N. (2004). Factorial composition of self-rated schizotypal traits among young males undergoing military training. Schizophrenia Bulletin, 30, 335–350. Steiner, J. L., Tebes, J. K., Sledge, W. H., & Walker, M. L. (1995). A comparison of the Structured Clinical Interview for DSM-III-R and clinical diagnoses. Journal of Nervous and Mental Disorders, 183(6), 365–369.
Auster et al.
Swiecicki, L., Zatorski, P., Bzinkowska, D., Sienkiewicz-Jarosz, H., Szyndler, J., & Scinska, A. (2009). Gustatory and olfactory function in patients with unipolar and bipolar depression. Progress in Neuropsychopharmacology and Biological Psychiatry, 33(5), 827–834. doi:10.1016/j. pnpbp.2009.03.030 Turetsky, B. I., & Moberg, P. J. (2009). An odorspecific threshold deficit implicates abnormal intracellular cyclic AMP signaling in schizophrenia. American Journal of Psychiatry, 166(2), 226–233. doi:10.1176/appi.ajp.2008.07071210 Turetsky, B. I., Moberg, P. J., Arnold, S. E., Doty, R. L., & Gur, R. E. (2003). Low olfactory bulb volume in first-degree relatives of patients with schizophrenia. American Journal of Psychiatry, 160(4), 703–708. Ventura, J., Nuechterlein, K. H., Subotnik, K. L., Gutkind, D., & Gilbert, E. A. (2000). Symptom dimensions in recent-onset schizophrenia and mania: A principal components analysis of the 24-item Brief Psychiatric Rating Scale. Psychiatry Research, 97(2–3), 129–135. doi:10.1016/S01651781(00)00228-6 Wu, J., Buchsbaum, M. S., Moy, K., Denlea, N., Kesslak, P., Tseng, H., . . . Cotman, C. (1993). Olfactory memory in unmedicated schizophrenics. Schizophrenia Research, 9(1),41–47.
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Olfaction Across the Schizophrenia Spectrum Auster et al.
Objective and Subjective Olfaction Across the Schizophrenia Spectrum Tracey L. Auster, Alex S. Cohen, Dallas A. Callaway, and Laura A. Brown
Much research indicates that patients with schizophrenia have impaired olfaction detection ability. However, studies of individuals with psychometrically defined schizotypy reveal mixed results—some document impairments while others do not. In addition to deficits in objective accuracy in olfaction for patients with schizophrenia, there has been an interest in subjective experience of olfaction. Unfortunately, methods of assessing accuracy and subjective hedonic olfactory evaluations in prior studies may not have been sensitive enough to detect group differences in this area. This study employed a measure of olfactory functioning featuring an expanded scoring system to assess both accuracy and subjective evaluations of pleasant and unpleasant experience. Data were collected for patients with schizophrenia, young adults with psychometrically defined schizotypy, psychiatric outpatients, and healthy controls. Results of this study indicate that both the schizophrenia and outpatient psychiatric groups showed similar levels of impaired olfaction ability; however, the schizotypy group was not impaired in olfaction detection. Interestingly, with regard to subjective hedonic evaluation, it was found that patients with schizophrenia did not differ from psychiatric outpatients, whereas individuals with schizotypy tended to rate smells as significantly less pleasant than healthy control participants. This suggests that subjective olfactory assessment is abnormal in some manner in schizotypy. It also suggests that accuracy of olfaction identification may be a characteristic of severe mental illness across severe mental illness diagnoses. The results are potentially important for understanding olfaction deficits across the mental illness spectrum. A relatively large literature suggests that patients with schizophrenia have impaired ability to identify and discriminate among various scents on the order of a full standard deviation (Brewer & Pantelis, 2010; Turetsky & Moberg, 2009; Wu et al., 1993). Given the magnitude of this deficit, it has been proposed that olfaction
deficits also reflect a vulnerability marker for schizophrenia-spectrum disorders. Related to this, there is a strong background of existing literature that links negative symptoms of schizophrenia to olfaction accuracy (Ishizuka et al., 2010). Often, negative symptoms are specifically linked to the first episode of psychosis (Corcoran et al., 2005). Given the
Tracey L. Auster, MA, Alex S. Cohen, PhD, Dallas A. Callaway, MA, and Laura A. Brown, MA, are affiliated with the Institute of Research, Department of Psychology, Louisiana State University, Baton Rouge, Louisiana. Address correspondence to Tracey L. Auster, Louisiana State University, Department of Psychology, 322 Audubon Hall, Baton Rouge, LA 70803. E-mail: [email protected] © 2014 Washington School of Psychiatry
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heterogeneous nature of schizophrenia (Cohen & Docherty, 2005), decoupling differences between symptoms and objective and subjective olfaction is a difficult feat, making it even more important to determine patterns in those at risk in order to guide early intervention. However, studies examining olfaction in individuals at elevated risk for schizophrenia-related illnesses have reported mixed results, some documenting impairment (Turetsky & Moberg, 2009; Turetsky, Moberg, Arnold, Doty, & Gur, 2003) and others finding no differences relative to controls (Compton & Chien, 2008; Kamath & Bedwell, 2008). Therefore, the first aim of the present study was to address the question of whether olfaction deficits reflect a vulnerability marker for those at putative risk for schizophrenia by directly comparing olfaction functions in stable outpatients with schizophrenia, psychiatric outpatients with serious mental illness other than schizophrenia, individuals with psychometrically defined schizotypy, and healthy controls. Considering the aforementioned inconsistency in findings in schizotypy across studies, it is important to consider whether previous research has used sensitive enough measures to assess olfaction. The University of Pennsylvania Smell Identification Test (UPSIT) had been the standard research measure of olfaction accuracy in both schizophrenia and schizotypy research (Cohen, Brown & Auster, 2012; Moberg et al., 1999). The UPSIT is a recognition-based test with a strong empirical backing for use in patient populations; to our knowledge, however its use in higher functioning populations is less clear. Consider that the recommended criteria denoting impairments is 87% correct (35 of 40 for women; 34 of 40 for men), suggesting that it is a relatively easy test even for patients with relatively severe impairments (see K. L. Minor, Wright, & Park, 2004). In this regard, it may lack sufficient discriminability for detecting differences in higher functioning populations. In the present study, we adapted a commonly used olfaction test (i.e., the “Sniffin’ Sticks” test; Hummel, Sekinger,
Auster et al.
Wolf, Pauli, & Kobal, 1997), to allow for free recall in addition to recognition, with the notion that this would expand the potential scoring range and provide a more sophisticated evaluation of olfaction deficits across the schizophrenia spectrum. In addition to accuracy deficits found in olfaction across the schizophrenia spectrum, there has been emerging interest in subjective experience of olfaction. While considerably less researched compared to olfaction deficits more generally, results from a handful of studies examining subjective ratings of hedonic experience of olfaction stimuli suggest that schizophrenia patients report smells as being less pleasant compared to controls (Kamath, Turetsky, & Moberg, 2011; Moberg et al., 2003). Related to this, Doop and Park (2006) reported that patients with schizophrenia have a more limited range of pleasant smells compared to controls. Findings for subjective experience of olfaction in individuals at risk for schizophrenia are even more limited, with one study failing to find differences in subjective experience between 13 biological family members of patients and 26 controls (Schneider et al., 2000). In this regard, a study directly comparing subjective experience of olfaction in patients with schizophrenia and in those at risk for schizophrenia would be a critical entry to this literature. Additionally, there is the question of whether olfaction deficits are specific to the schizophrenia spectrum or whether they reflect a symptom of severe mental illness more generally. Of note, olfaction deficits have been reported, albeit somewhat inconsistently, in patients with mood disorders compared to controls (Amsterdam, Settle, Doty, Abelman, & Winokur, 1987; Gross-Isseroff et al., 1994; Negoias et al., 2010; Pause, Miranda, Goder, Aldenhoff, & Ferstl, 2001). With respect to the subjective deficits, the findings have been more mixed, with some studies suggesting that patients with nonpsychotic affective disorders report more positive experiences with olfaction stimuli (Cumming, Matthews, & Park, 2010) and others indi-
Olfaction Across the Schizophrenia Spectrum 59
cate a less positive report (Negoias et al., 2010) compared to control groups. The final aim of our study was to explore how a psychiatric group, comprising stable outpatients with serious mental illness but not schizophrenia, compared to a schizophrenia group in olfaction deficits. The issue of how subjective olfaction ratings manifest in schizophrenia-spectrum disorders versus those with serious mental illness is a topic that, to our knowledge, has not yet been broached. This study examined the results of a measure of olfaction using an expanded scoring system in stable outpatients with and without schizophrenia, healthy controls, and individuals at elevated risk for developing schizophrenia-spectrum disorders, defined using validated psychometric procedures. The at-risk group was recruited from a university setting, which is advantageous in that use of a relatively healthy sample reflects a conservative test of the hypothesis that olfaction deficits are a vulnerability marker of schizophrenia pathology. In sum, our aims were to evaluate potential differences in detection of and subjective appraisal of olfaction for those with psychometrically defined schizotypy, those with schizophrenia, a healthy control group, and a psychiatric outpatient group. METHODS
Participants Four groups of participants were recruited for this study. Two groups were recruited from a community mental health center and were diagnosed with either schizophrenia (n = 31) or unipolar (n = 13) or bipolar (n = 12) affective disorders; they were diagnosed using the Structured Clinical Interview for DSM-IV (SCID; Lobbestael, Leurgans, & Arntz, 2011; Steiner, Tebes, Sledge, & Walker, 1995). Inclusion criteria included being 18–55 years of age, a Global Assessment of Functioning Scale (GAF) score
> 30, no current diagnosis of substance dependence (based on the SCID), and no neurological disease or head injury sufficient to cause overt neurocognitive deficits (based on patient records and self-report). The present data were included in a recent meta-analysis examining olfaction performance in schizophrenia and schizotypy (Cohen et al., 2012). Additionally, schizotypy and healthy adult control groups were recruited from a university setting. The Schizotypy Personality Questionnaire-Brief (SPQ-B; Raine & Benishay, 1995) was used to screen individuals. There is evidence that schizotypy accounts for 10% of the population (see Lenzenweger, 2006, for a conceptual review); we therefore used a strategy wherein the top 5% of scorers (1.65 standard deviations [SD] from the ethnicity and gender-determined means) on the SPQ-B subscales were contacted to participate in the laboratory segment of the study. Based on scores at the sex and ethnicity-derived 95th percentile or above on the positive, negative, or disorganized subscales, a schizotypy group was identified and recruited (n = 79). Additionally, a healthy control group (n = 34) was identified that had SPQ-B scores lower than the mean for each of the subscales (see Cohen, Callaway, Najolia, Larsen, & Strauss, 2011, for more details regarding recruitment). Selected participants were contacted via e-mail or phone by research assistants and asked to undergo an in-person testing session in our laboratory. All participants involved in the laboratory phase of the study were compensated $20. Measures Clinical Measures. The SCID for Axis I disorders (SCID-I; Steiner et al., 1995), the gold standard for clinical diagnosis, was used in this study. Diagnoses and symptom ratings were made using a consensus procedure led by Dr. Alex Cohen. In this manner, full interrater agreement was assured for each case. The Brief Psychiatric Rating Scale (BPRS; Lukoff, Nuechterlein, & Ventura, 1986)
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TABLE 1. Descriptive Statistics for the Demographic and Clinical Variables Across the Patient and Nonpatient Groups
% Women % Caucasian
Psychiatric Outpatient Group
Schizophrenia
Healthy Controls
Schizotypy
42
39
44
42
69
34
85
80
Age
45.96 ± 9.82
39.41 ± 10.80
19.89 ± 5.56
19.35± 1.67
Education
12.46 ± 2.67
11.47 ± 2.20
13.34 ± 0.59
13.66 ± 0..83
Mania/Excitement
10.0 ± 5.3
10.34 ±4.57
Negative
6.72 ± 2.92
8.53 ±3.65
Positive
7.8 ± 2.97
12.12 ± 5.27
BPRS Factor Scores
SPQ-B Scores Positive
–12.95 ± 3.63
2.85 ± 5.58
Negative
–13295 ± 2.88
4.24 ± 6.16
Disorganization
–10.74 ± 2.16
44.11 ± 4.39
is a standard assessment of 24 symptoms and was used to evaluate symptom severity across patient groups. Factor subscale scores reflecting positive (i.e., bizarre behavior, suspiciousness, unusual thought content, disorientation, and hallucinations items), negative (i.e., self-neglect, blunted affect, motor retardation, and emotional withdrawal items), depressive (i.e., depression, guilt, suicidality, and anxiety items), and mania/excitement (i.e., motor hyperactivity, elevated mood, excitement, distractibility, hostility, and grandiosity items) symptoms (defined in Ventura, Nuechterlein, Subotnik, Gutkind, & Gilbert, 2000) were employed here. Schizotypal Personality Questionnaire. The Schizotypal Personality Questionnaire-Brief (SPQ-B; Raine & Benishay, 1995) was used to identify individuals with psychometrically defined schizotypy. The SPQ-B is a 22-item instrument based on the original 74-item SPQ (Raine, 1991). The SPQ is one of the most commonly used measures for assessing schizotypy (Stefanis, Smyrnis, Avramopoulos, Ntzoufras, & Stefanis, 2004). Data reported here (see Table 1) display means
for participants broken down by those at the 95th percentile or above on the positive, negative, or disorganized subscales. We chose to administer the SPQ-B because of its brevity, as the SPQ-B has been shown to lead to fewer incomplete responses compared to the full SPQ (Cohen, Matthews, Najolia, & Brown, 2010). Olfaction Ability. The “Sniffin’ Sticks,” used in the present study, is an olfaction assessment measure developed in the 1990s to detect olfaction ability and discrimination (Hummel et al., 1997). The measure includes 12 different pens with a wide variety of smells (e.g., orange, leather). To expand the sensitivity of this measure to test our predictions, we modified the scoring protocol by adding a free recall phase before the recognition protocol. First, participants were asked to freely identify each smell. If the response was incorrect, participants were then provided a recognition response set that asked them to identify the smell from four options. Participants were awarded two points for a correct recall response and one point for a correct recognition response. To evaluate
Olfaction Across the Schizophrenia Spectrum 61
subjective experience of responses, participants were separately asked “How pleasant was this scent to you?” and “How unpleasant was this scent to you?” with answers for each question chosen from a diagram illustrating a 7-point Likert-type scale with anchors ranging from 1 (not at all) to 7 (extremely pleasant/unpleasant). The Sniffin’ Sticks measure has been used with patient and healthy control populations and has demonstrated adequate reliability and validity (Landis, Knecht, Huttenbrink, Lacroix, & Hummel, 2005; Negoias et al., 2010; Swiecicki et al., 2009). Analyses Analyses were conducted in four steps. First, we compared groups on age, sex, and ethnicity and compared BPRS and GAF scores to determine whether there were any potential demographic or clinical confounds that should be controlled for. Second, we compared the four groups on olfaction performance using an analysis of variance (ANOVA). Third, we compared the four groups on subjective experience of the olfaction stimuli using an ANOVA. For the second and third analyses, we predicted that, in line with the current literature, we would find deficits in accuracy and hedonic evaluation of olfaction for those with schizophrenia as compared to the psychiatric group without psychosis. We also hypothesized that we would see deficits in accuracy and hedonic evaluation for those with schizotypy compared to the healthy control group. The patient and nonpatient groups were also compared to each other, although a priori predictions were not made. Finally, we computed correlations between BPRS symptom factors and olfaction variables for the schizophrenia group and SPQ factors and the olfaction variables for the schizotypy group. This comparison evaluated whether olfaction deficits were associated with specific schizophrenia/schizotypy symptoms.
RESULTS
Demographic Variables Table 1 contains demographic and clinical information. Within the total sample, age was significantly different across groups, F(3, 173) = 156.2, p < .01. Age was significantly higher for the patient groups compared to the schizotypy and healthy control groups (ps < .05). Education levels were significantly different across groups, F(3, 173) = 17.63, p < .01. These education levels were significantly higher for the healthy control and schizotypy groups compared to the patient groups (ps < .05). The schizophrenia versus patient control group had significantly more severe BPRS negative and positive symptoms (ts[55] = 2.03 and 3.67, ps < .05), but the groups were not statistically dissimilar with respect to other BPRS symptom factors (ps > .10). Smoking status, sex, age, and education were not significantly related to any of the dependent measures in this study. There were no statistically significant differences on subjective or objective olfaction ratings between unipolar and bipolar patients and the psychiatric outpatient group. Olfactory Accuracy Variables Across Groups A one-way ANOVA comparing the four groups revealed a significant difference between groups in olfaction accuracy, F(3, 175) = 36.02, p < 01. The post hoc t tests revealed that the psychiatric outpatient group and the schizophrenia group were impaired in olfaction ability compared to the schizotypy and healthy control groups (ps < .05), but the groups did not differ from each other (ps > .05) (see Figure 1).
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FIGURE 1. Average accuracy means. Higher means represent higher accuracy. Brackets denote which groups were significantly different from each other.
Subjective Olfaction Variables Across Groups A one-way ANOVA comparing the four groups also revealed a significant difference between groups on subjective rating of smells, F(3, 165) = 2.10, p < .05. The results of post hoc comparisons indicated that both patient groups (psychiatric outpatient and schizophrenia) showed similar levels of subjective olfactory evaluation (see Table 1). The schizotypy group was associated with less pleasant ratings compared to the healthy control participants (ps < .05) (see Figure 2). Bivariate Correlations Between Olfaction Ratings and Symptom Ratings Negative BPRS factor scores and negative SPQ scores were correlated with subjective smell ratings, suggesting that negative symptoms were related to negative evaluation of smell. This suggests that the greater the negative symptoms, the poorer the participants rated hedonic experience of smell. See Table 2 for additional correlations between BPRS symptoms and SPQ symptoms and objective and subjective olfaction rat-
ings. Olfaction scores, both objective and subjective, were not significantly associated with any other symptoms or trait scores. DISCUSSION
The present study was designed to address inconsistency in the literature regarding whether olfaction deficits reflect a vulnerability marker of the schizophrenia spectrum. This study is the first to our knowledge to evaluate olfaction both in patients with schizophrenia and in individuals with psychometrically defined schizotypy. There were three major findings from this study. First, individuals with psychometrically defined schizotypy showed no objective olfaction deficits compared to the healthy control group, and these groups were significantly more accurate in objective smell ratings compared with both outpatient groups. This finding argues against claims that deficits in olfaction identification reflect a vulnerability marker of those with psychometric schizotypy. While it may be true that olfaction inaccuracy is a marker for those at ultrahigh risk, it is unlikely that the lack of group differences reflects a sensitivity issue for this population on the schizophrenia spectrum,
Olfaction Across the Schizophrenia Spectrum 63
FIGURE 2. Average pleasant ratings across groups. Higher means represent higher pleasant rating of smell. Brackets denote which groups were significantly different from each other.
because the measure of olfaction employed in this study was probably more sensitive than those used in prior studies. In support of this conclusion, note that the healthy controls received, on average, less than half of the potential points for the identification trials. In contrast, the demarcation for poor performance on the UPSIT is approximately 87% correct (Minor et al., 2004). Second, there was a distinct pattern for subjective in-the-moment hedonic experience of olfaction stimuli for those with schizotypy compared to matched controls. The schizotypy group reported smells as subjectively less pleasant than controls, indicating that there is a difference for the at-risk group in comparative emotional experience. Interestingly, and consistent with prior studies (see Minor & Cohen, 2010, for a review), patients with schizophrenia do not generally show reduced hedonic experience of olfactory stimuli in the laboratory (Berenbaum, 1992). Thus, there appears to be a discrepancy regarding experience in patients with schizophrenia and those with psychometrically defined schizotypy. That is, university students with psychometrically defined schizotypy are more pathological compared to older chronic patients with schizophrenia with regard to hedonic olfactory experience. The resolution to this discrepancy is not im-
mediately clear, although it is worth noting that individuals with schizotypy have reported less pleasant experience in reaction to in-the-moment evaluation of visual images in another study from our laboratory (Cohen et al., 2011). Further research regarding this discrepancy seems an important endeavor. Third, as supported by the previous research, we found that individuals with schizophrenia are impaired in olfaction identification. Interestingly, the psychiatric outpatient group, comprising individuals with mood disorders, revealed a similar impairment consistent with the literature, which raises questions about the specificity of olfaction deficits in schizophrenia. Previous research indicates impairment of objective olfaction in those with mood disorders (Pause et al., 2001). The similarities in these heterogeneous groups provide credence to the theory that olfactory impairment may be a symptom of general serious mental illness, not just a schizophrenia-specific phenomenon. Limitations of these results must be noted based on inequitable sample sizes, with the schizotypy group being much larger than all other groups. We were unable to control for some factors that may affect smell, including specific allergies, smoking, or perfumes, due to lack of comprehensive
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TABLE 2. Bivariate Correlations Between Schizophrenia Spectrum Symptoms and Objective Olfaction Ratings Olfaction Accuracy
Olfaction Subjective Pleasant Rating
.08
.11
BPRS Negative
–.37**
–.37**
BPRS Positive
–.02
–.07
BPRS Depression
.14
–.64
Schizophrenia Group and Psychiatric Outpatient Group (n = 59) BPRS Mania
Schizotypy and Healthy Controls (n = 117) SPQ-B Positive
–.05
–.16
SPQ-B Negative
–.04
–.28**
SPQ-B Disorganized
.06
–.21
Note. **Correlation is significant at .01 levels (two-tailed).
detail on these variables. These data suggest an overall accuracy deficit among those with serious mental illness and also a subjective difference in olfaction experiences for those at risk for schizophrenia. In the future, it may be important to consider these variables as potential confounds. Future research should explore this distinct difference for those with schizotypy and elaborate how subjective ex-
perience of olfaction directly relates to psychiatric risk and vulnerability. This research may inform identification of illness susceptibility, and therefore be important to consider in early intervention. The present data highlight the need to explore whether olfaction accuracy deficits are distinct to those withschizophrenia or are characteristic of those with psychiatric illness generally.
REFERENCES Amsterdam, J. D., Settle, R. G., Doty, R. L., Abelman, E., & Winokur, A. (1987). Taste and smell perception in depression. Biological Psychiatry, 22(12), 1481–1485. Berenbaum, H. (1992). Posed facial expressions of emotion in schizophrenia and depression. Psychological Medicine, 22(4), 929–937. Brewer, W. J., & Pantelis, C. (2010). Olfactory sensitivity: Functioning in schizophrenia and implications for understanding the nature and progression of psychosis. Vitamins and Hormones, 83, 305–329. doi:10.1016/S0083-6729(10)83013-4 Cohen, A. S., Brown, L. A., & Auster, T. L. (2012). Olfaction, “olfiction,” and the schizophrenia spectrum: An updated meta-analysis on identification and acuity. Schizophrenia Research, 135(1– 3), 152–157. doi:10.1016/j.schres.2011.12.005 Cohen, A. S., Callaway, D. A., Najolia, G. M., Larsen, J. T., & Strauss, G. P. (2011). On “risk” and reward: Investigating state anhedonia in psychometrically defined schizotypy and schizophre-
nia. Journal of Abnormal Psychology, 121(2), 407–415. doi:10.1037/a0026155 Cohen, A. S., Dinzeo, T. J., Nienow, T. M., Smith, D. A., Singer, B., & Docherty, N. M. (2005). Diminished emotionality and social functioning in schizophrenia. Journal of Nervous and Mental Disorders, 193(12), 796–802. doi:10.1037/ a0026155 Cohen, A. S., & Docherty, N. M. (2005). Symptom-oriented versus syndrome approaches to resolving heterogeneity of neuropsychological functioning in schizophrenia. Journal of Clinical Psychology, 17(3), 384–390. doi:10.1176/appi. pn.2013.4b2 Cohen, A. S., Matthews, R. A., Najolia, G. S., & Brown, L. A. (2010). Toward a more psychometrically sound brief measure of schizotypal traits: Introducing the SPQ Brief Revised. Journal of Personality Disorders, 24(4), 516–537. doi:10.1521/pedi.2010.24.4.516 Compton, M. T., & Chien, V. H. (2008). No association between psychometrically-determined
Olfaction Across the Schizophrenia Spectrum 65
schizotypy and olfactory identification ability in first-degree relatives of patients with schizophrenia and non-psychiatric controls. Schizophrenia Research, 100(13), 216–223. doi: 10.1016/j. schres.2007.11.021
Landis, B. N., Knecht, M., Huttenbrink, K. B., Lacroix, J. S., & Hummel, T. (2005). Clinical aspects of dysosmia and presentation of European Olfactory Test of “Sniffin Sticks”: A review. Journal of Otolaryngology, 34(2), 86–92.
Corcoran, C., Whitaker, A., Coleman, E., Fried, J., Feldman, J., Goudsmit, N., & Malaspina, D. (2005). Olfactory deficits, cognition and negative symptoms in early onset psychosis. Schizophrenia Research, 80(2–3), 283–293.
Lenzenweger, M. F. (2006). Schizotaxia, schizotypy, and schizophrenia: Paul E. Meehl’s blueprint for the experimental psychopathology and genetics of schizophrenia. Journal of Abnormal Child Psychology, 115, 195–220.
Cumming, A. G., Matthews, N. L., & Park, S. (2010). Olfactory identification and preference in bipolar disorder and schizophrenia. European Archives of Psychiatry and Clinical Neurosciences, 261(4), 251–259 .doi:10.1007/s00406 010-01457
Lobbestael, J., Leurgans, M., & Arntz, A. (2011). Inter-rater reliability of the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID I) and Axis II Disorders (SCID II). Clinical Psychology & Psychotherapy, 18(1), 75–79. doi:10.1002/ cpp.693
Doop, M. L., & Park, S. (2006). On knowing and judging smells: Identification and hedonic judgment of odors in schizophrenia. Schizophrenia Research, 81(2–3), 317–319. doi:10.1016/j. schres.2005.08.006
Lukoff, D., Nuechterlein, K. H., & Ventura, J. (1986). Manual for the expanded Brief Psychiatric Rating Scale (BPRS). Schizophrenia Bulletin, 12, 594–602.
Gross-Isseroff, R., Luca-Haimovici, K., Sasson, Y., Kindler, S., Kotler, M., & Zohar, J. (1994). Olfactory sensitivity in major depressive disorder and obsessive compulsive disorder. Biological Psychiatry, 35(10), 798–802. doi: 10.1016/00063223(94)91142-8 Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., & Kobal, G. (1997). ‘Sniffin’ Sticks’: Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chemical Senses, 22(1), 39–52. Ishizuka, K., Tajinda, K., Colantuoni, C., Morita, M., Winicki, J., Le, C., . . . Cascella, N. G. (2010). Negative symptoms of schizophrenia correlate with impairment on the University of Pennsylvania smell identification test. Neuroscience, 66(1), 106–110. doi:10.1016/j.neures.2009.10.001 Kamath, V., & Bedwell, J. S. (2008). Olfactory identification performance in individuals with psychometrically defined schizotypy. Schizophria Research, 100(1–3), 212–215. doi:10.1016/j. schres.2007.10.008 Kamath, V., Turetsky, B. I., & Moberg, P. J. (2011). Identification of pleasant, neutral, and unpleasant odors in schizophrenia. Psychiatry Research, 187(1–2), 30–35. doi:10.1016/j.psychres.2010.12.011
Minor, K. L., Wright, B. D., & Park, S. (2004). The Smell Identification Test as a measure of olfactory identification ability in schizophrenia and healthy populations: A Rasch psychometric study. Journal of Abnormal Psychology, 113(2), 207– 216. doi:10.1037/0021-843X.113.2.207 Minor, K. S., & Cohen, A. S. (2010). Affective reactivity of speech disturbances in schizotypy. Journal Psychiatry Research, 44(2), 99–105. doi:10.1016/j.jpsychires.2009.06.005 Moberg, P. J., Agrin, R., Gur, R. E., Gur, R. C., Turetsky, B. I., & Doty, R. L. (1999). Olfactory dysfunction in schizophrenia: A qualitative and quantitative review. Neuropsychopharmacology, 21(3), 325–340. doi:10.1016/S0893133X(99)00019-6 Moberg, P. J., Arnold, S. E., Doty, R. L., Kohler, C., Kanes, S., Seigel, S., . . . Turetsky, B. I. (2003). Impairment of odor hedonics in men with schizophrenia: Comparative study. American Journal of Psychiatry, 160(10), 1784–1789. Negoias, S., Croy, I., Gerber, J., Puschmann, S., Petrowski, K., Joraschky, P., & Hummel, T. (2010). Reduced olfactory bulb volume and olfactory sensitivity in patients with acute major depression. Neuroscience, 169(1), 415–421. doi:10.1016/j.neuroscience.2010.05.012
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Overall, J. E., & Gorham, D. R. (1962). The Brief Psychiatric Rating Scale. Psychological Reports, 10, 799–812. Pause, B. M., Miranda, A., Goder, R., Aldenhoff, J. B., & Ferstl, R. (2001). Reduced olfactory performance in patients with major depression. Journal of Psychiatry Reseach, 35(5), 271–277. doi:10.1016/S0022-3956(01)00029-2 Raine, A. (1991). The SPQ: A scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophrenia Bulletin, 17, 555–564. Raine, A., & Benishay, D. (1995). The SPQ-B: A brief screening instrument for schizotypal personality disorder. Journal of Personality Disorders, 9, 346–355. Schneider, F., Habel, U., Reske, M., Toni, I., Falkai, P., & Shah, N. J. (2000). Neural substrates of olfactory processing in schizophrenia patients and their healthy relatives. Psychiatry Research: Neuroimaging, 155(2), 103–112. doi:10.1016/j. pscychresns.2006.12.004 Stefanis, N. C., Smyrnis, N., Avramopoulos, D., Evdokimidis, I., Ntzoufras, I., & Stefanis, C. N. (2004). Factorial composition of self-rated schizotypal traits among young males undergoing military training. Schizophrenia Bulletin, 30, 335–350. Steiner, J. L., Tebes, J. K., Sledge, W. H., & Walker, M. L. (1995). A comparison of the Structured Clinical Interview for DSM-III-R and clinical diagnoses. Journal of Nervous and Mental Disorders, 183(6), 365–369.
Auster et al.
Swiecicki, L., Zatorski, P., Bzinkowska, D., Sienkiewicz-Jarosz, H., Szyndler, J., & Scinska, A. (2009). Gustatory and olfactory function in patients with unipolar and bipolar depression. Progress in Neuropsychopharmacology and Biological Psychiatry, 33(5), 827–834. doi:10.1016/j. pnpbp.2009.03.030 Turetsky, B. I., & Moberg, P. J. (2009). An odorspecific threshold deficit implicates abnormal intracellular cyclic AMP signaling in schizophrenia. American Journal of Psychiatry, 166(2), 226–233. doi:10.1176/appi.ajp.2008.07071210 Turetsky, B. I., Moberg, P. J., Arnold, S. E., Doty, R. L., & Gur, R. E. (2003). Low olfactory bulb volume in first-degree relatives of patients with schizophrenia. American Journal of Psychiatry, 160(4), 703–708. Ventura, J., Nuechterlein, K. H., Subotnik, K. L., Gutkind, D., & Gilbert, E. A. (2000). Symptom dimensions in recent-onset schizophrenia and mania: A principal components analysis of the 24-item Brief Psychiatric Rating Scale. Psychiatry Research, 97(2–3), 129–135. doi:10.1016/S01651781(00)00228-6 Wu, J., Buchsbaum, M. S., Moy, K., Denlea, N., Kesslak, P., Tseng, H., . . . Cotman, C. (1993). Olfactory memory in unmedicated schizophrenics. Schizophrenia Research, 9(1),41–47.
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