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Peculiar word use as a possible trait marker in schizophrenia
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Schizophrenia Research 103 (2008) 311 – 317 www.elsevier.com/locate/schres
Peculiar word use as a possible trait marker in schizophrenia Bora Baskak a,⁎, E. Tugba Ozel a , E. Cem Atbasoglu a , Seda C. Baskak b a
Ankara University, School of Medicine, Psychiatry Department, Neuropsychiatry Research Unit, Dikimevi, Ankara, Turkey b Bolu Izzet Baysal Psychiatry Hospital, Turkey Received 1 January 2008; received in revised form 11 April 2008; accepted 18 April 2008 Available online 5 June 2008
Abstract Peculiar word use in schizophrenia has been emphasized by many authors, however the definition or the linguistic and clinical correlates of this phenomenon are not clear. We propose a new, standard and reliable method to extract a numerical measure of peculiar word use with operationalized definitions. We applied a modified version of the Controlled Word Association Test (Turkish version) to a pool of healthy subjects (N = 55) and used the data as norm to compare the degree of peculiarity and patterns of word association among patients with schizophrenia (N = 33), their healthy siblings (N = 31) and healthy controls (N = 32). We also explored the relationship of peculiar word use with patterns of word association (semantic versus phonologic) and formal thought disorder. Patients and their siblings performed worse on measures of verbal fluency. They also generated more peculiar words and relied less on semantic associations, compared to healthy controls. Peculiar word use was associated with the severity of formal thought disorder and the tendency to make use of phonologic associations in the patient group and their siblings, whereas neither of the word association patterns predicted peculiar word use in the control group. Our results provide empirical support to previous observations about the peculiarity of schizophrenic speech. Peculiar word use could be associated with a deficit to employ semantic classifications in verbal fluency tasks and thus relying more on sound-based associations. Excess use of phonologic associations may be playing a mediating role between semantic processing abnormalities and formal thought disorder. © 2008 Elsevier B.V. All rights reserved. Keywords: Schizophrenia; Schizophrenic language; Siblings; Semantics; Phonetics
1. Introduction Schizophrenia patients demonstrate multilevel language impairments that have been accepted as one of the fundamental (Bleuler, 1950), and diagnostic (American Psychiatric Association, 1994) signs of schizophrenia. These impairments include phonetic abnormalities (e.g., errors in timing, intonation and quality of speech) (Rieber and Vetter, 1994) and semantic abnormalities such as impaired semantic store (Chen et al., 2000), ⁎ Corresponding author. Tel.: +90 312 595 62 47. E-mail address: [email protected] (B. Baskak). 0920-9964/$ - see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2008.04.025
retrieval (Allen et al., 1993) and deficits in structure of semantic network (Aloia et al., 1996). Following Crow's (2000) hypothesis about the coheritability of language and schizophrenia, DeLisi (2001) highlighted that deficits in specifically human aspects of language may be related to the genetics of schizophrenia. In a recent review Covington et al. (2005) addressed the need for studies about the heredity of schizophrenic language impairment that may provide a solid biological basis for the disease. Some language abnormalities (e.g. deficits in verbal fluency [VF]) have been shown in healthy relatives of schizophrenic patients (Laurent et al., 2000) and proposed as possible
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trait markers of predisposition to schizophrenia (Chen et al., 2000). Peculiar word use is one of the language abnormalities in schizophrenia that has been emphasized by many authors (Harrow and Prosen, 1979; Pinard and Lecours, 1983; Johnston and Holzman, 1979; Holzman et al., 1986; Solovay et al., 1987; Liddle et al., 2002). Despite the fact that it is a common clinical observation, studies involving quantitative assessment of this abnormality are relatively scarce, probably because agreement on the degree of peculiar word use is more difficult compared to other language abnormalities. Pinard and Lecours (1983) observed that schizophasic discourse often included rare words, and interpreted this as evidence of a large and intact vocabulary in schizophrenia. Johnston and Holzman (1979) proposed that the peculiar verbalizations in schizophrenic speech were representations of the underlying thought disorder. Holzman et al. (1986) later highlighted that the thinking of schizophrenic patients was confused and fluid, usually peppered with many idiosyncratic and peculiar words and phrases. Thus, in Johnston and Holzman's Thought Disorder Index (TDI) (1979), peculiar verbalizations represent a very mild qualitative form of thought disorder. They are subjectively identified and rated for frequency of instances during a Rorschach Inkblot Test. Liddle et al. (2002) operationally defined and grounded peculiarity in a continuous spectrum as a weaker form of neologism in the Thought and Language Index (TLI). Peculiarity of speech is rated as a separate item in these two scales — ‘peculiar word use’ in the TLI and ‘idisyncratic verbalizations’ in the TDI. It should be noted, however, that both these items have a weak interrater reliability; in fact they achieve the lowest interrater reliability figures among the other items in the TLI and TDI. Low interrater agreement could be due to a higher degree of subjectivity involved in rating peculiarity unless the patient's speech is analyzed quantitatively. This subjectivity is probably a consequence of the difficulty in making an operational definition of peculiarity, compared to other abnormalities in language, which either lend themselves to a more strict definition (e.g., loosening of associations, tangentiality, etc.), or are more readily observable since they are severe by definition (e.g., neologisms or incoherence). Patients with schizophrenia rarely use words that are obviously peculiar (Cuesta and Peralta, 1999). Rather, peculiarity of schizophrenic speech can be identified through detection of subtle examples that take place on a continuum between ‘normal’ and ‘obviously peculiar’. A unit-by-unit analysis of the patient's speech targeting to extract a relatively accurate numerical measure of peculiarity would address the issue of subjectivity in assessment, however, such a method would be time-consuming,
compared to the assessment of other symptoms. Thus a relatively practical method that is capable of identifying slight forms of peculiarity with a higher degree of interrater reliability could prove useful in clinical research. The first aim of this study is to propose and test the reliability of a method that would achieve the standards mentioned above. We propose a method that involves a modified version of the Controlled Oral Word Association Test COWAT (Lezak, 1995) in rating peculiar word use. This allows the rater to base the rating of the peculiarity of each word uttered by the subject on the frequency of its use by a pool group, rather than making a forced choice between “peculiar” and “non-peculiar”. The second aim of the study is to test the hypothesis that peculiar word use is more common in schizophrenia patients and their healthy relatives compared to healthy controls, in order to study the potential value of peculiarity as a trait marker for schizophrenia. We were also interested in the relationship of peculiar word use with patterns of association between the uttered words. The relationship of peculiar word use with other forms of thought disorder has been theoretically explained by some authors, but empirical research on this question is scarce. One assumption is that excess use of sound-based (compared to context-based) associations renders schizophrenic speech “difficult to understand”. Chaika (1974) speculated that the structure of speech in schizophrenia is disturbed because of a distraction by the sounds of words, so that a discourse becomes a non-informative string of word associations. This was referred to as ‘glossomania’ by Pinard and Lecours (1983) and later used by Andreasen (1987) for the definition of derailment and clang associations. In fact, verbal fluency (VF) studies point out to a disproportionate impairment of semantic relative to phonetic fluency in schizophrenia patients (Kremen et al., 2003; Phillips et al., 2004; Bozikas et al., 2005). However, the relationship of this language abnormality with peculiar word use has not been empirically tested before. Thus, the third aim of this study is to test the hypothesis that the degree of peculiar word use is associated with a disproportionate amount of phonetic compared to semantic associations by using operationalized definitions and reliable measures for both peculiarity and word association patterns. 2. Methods and materials 2.1. The groups The Turkish version of the modified COWAT (Lezak, 1995), as will be described below, was first applied to 55 healthy subjects (relatives or acquaintances of the
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she had attributed to that word and the answer was noted. Then the word lists were analyzed by two blind raters for the following variables: Total VF performance: The sum of the total number of words starting with the letter ‘a’ and the letter ‘s’ generated by the subject during COWAT. In order to control the influence of VF performance, all scores were divided by the total VF performance. Familiarity score: The number of times that a word was generated by the subjects in the pool group. For example a word generated by 4 subjects in the pool would have a familiarity score of 4. Perseverated words and neologisms were not counted. Peculiarity score: This was defined as the inverse of the familiarity score (1 / familiarity). Uniqueness score: Number of unique words, i.e., words that were not generated by any subject in the pool. Neologism score: Total number of neologisms generated by the patient. A word was accepted as a neologism when the word was not recognized by any of the two raters and was not included in a comprehensive dictionary of Turkish (Turkish Dictionary of Turkish Language Association, 2000). In order to analyze the word association pattern, the raters assessed all word pairs, i.e., all two consecutive words in the list, e.g., the first and the second, the second and the third…, so that the total number of pairs was n + 1 in a list of n words. In order to identify all associations, each word uttered by the subject was assessed for the presence or absence of a semantic or phonologic relation with the preceding one, e.g., the 2nd with the 1st, 3rd with the 2nd… 11th with the 10th. All relatedness scores were also controlled for (divided by) the total VF performance. Semantic relationship has been defined as a categoric or a contextual relationship (Kerns et al., 1999). Categoric relatedness score was the sum of categoric relations (two words that belong to the same category like two animals, two country names, two human names etc.).
hospital staff, stratified for their level of education) in order to generate a “pool” that would constitute the norm for the frequency of the words to be generated by the study groups. The three study groups were 33 consecutive outpatients followed with a diagnosis of DSM-IV schizophrenia at a university hospital, 31 non-psychotic siblings of schizophrenia patients and 32 healthy controls. All patients were under medication with atypical antipsychotics and clinically stable at the time of the study, as indicated by their Scale for the Assessment of Positive (SAPS) and Negative Symptoms (SANS) scores (Andreasen, 1987). The groups were matched for age, education and balanced for sex. All subjects signed written informed consent. The Turkish version of the modified form of COWAT was applied to the three groups and their familiarity and peculiarity scores were calculated based on the frequency of the words in the pool group. The pool group, as well as the controls and siblings of schizophrenia patients were evaluated by two experienced psychiatrists in order to rule out the existence of a psychotic disorder or a history of any psychiatric treatment. However, disorders other than those with overt psychosis were not assessed in detail. Sociodemographic and clinical features of the three groups are presented in Table 1. 2.2. Evaluation of peculiar word use and association patterns with the COWAT Subjects were expected to generate as many words as they could starting with the letter ‘a’ and the letter ‘s’ (frequently used vowel and consonant, respectively, in Turkish) during a period of 3 min for each. The words generated were audiorecorded and listed by a rater. If the subject produced a neologism or generated a word that was difficult to understand, he/she was asked what he/ Table 1 Sociodemographic and clinical features of the groups
Gender (F/M) Age (years ± SD) Education (years ± SD) Mean duration of illness (years ± SD) SAPS score (sum of all items) (mean ± SD) FTD score (sum of all items) (mean ± SD) SANS score (sum of all items) (mean ± SD)
Patients
Siblings
Controls
N = 33
N = 31
N = 32
15/18 32.3 ± 9.9 12.0 ± 2.2 5.0 ± 4.8 30.66 ± 18.54 8.87 ± 7.54 33.66 ± 15.05
The “Pool” N = 55 2
12/19 33.9 ± 10.2 12.9 ± 6.0
16/16 34.9 ± 9.9 12.5 ± 3.9
X = 0.82, p = 0.66 F = 0.66, df = 2, p = 0.52 F = 0.44, df = 2, p = 0.65
28/27 27.6 ± 9.2 11.3 ± 3.2
– – –
– – –
– – –
– – –
F: female, M: male, SD: standard deviation, FTD: formal thought disorder, SAPS: Scale for the Assessment of Positive Symptoms, SANS: Scale for the Assessment of Negative Symptoms.
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Table 2 Comparison of the three groups for peculiarity and relatedness scores (MANOVA)
Familiarity score (1 / peculiarity score) Semantic relatedness score Phonologic relatedness score
Patients (n = 33)
Siblings (n = 31)
Controls (n = 32)
(mean ± SD)
(mean ± SD)
(mean ± SD)
4.43 ± 0.34 0.204 ± 0.128 0.268 ± 0.159
4.07 ± 0.31 0.165 ± 0.104 0.309 ± 0.129
6.11 ± 0.15 0.359 ± 0.124 0.231 ± 0.089
F = 14.73 df = 2 p b 0.001⁎ F = 23.11 df = 2 p b 0.001⁎ F = 2.88 df = 2 P = 0.061
SD= standard deviation, ⁎Post-hoc analysis: controls N patients = siblings for familiarity and semantic relatedness scores.
Contextual relatedness score was the total number of two temporally (like armour and ammo) or functionally (like spoon and soup) related word pairs. Thus, the Semantic relatedness score was the sum of categoric and contextual relatedness scores. Phonologic relatedness was defined as the presence of either a shared syllable or a phoneme or a rhyme in two consecutive words. Phonologic relatedness score was the sum of phonologic relations between the words. Total relatedness score was the sum of word pairs that were either semantically or phonologically related. Raters performed a pilot study on 20 word lists to secure high interrater reliability regarding the relatedness scores. 2.3. Analysis We compared the total VF performance and scores of uniqueness and neologism between the three groups with analyses of variance (ANOVA). Peculiarity and scores of semantic and phonologic relatedness were compared with a multivariate analysis of variance (MANOVA). The distributions of peculiarity and familiarity scores were tested for normality by the Kolmogorov–Smirnov Test. Peculiarity scores were skewed (p b 0.001), whereas familiarity scores were normally distributed (p = 0.098). Therefore we included the familiarity scores (1 / peculiarity) in the statistical analyses.
Pearson correlation coefficients were calculated to test the relationships between peculiarity, severity of formal thought disorder and relatedness patterns. Finally, in order to examine the relationship of peculiarity with semantic and phonologic relations and the severity of formal thought disorder, we applied a stepwise linear regression, where peculiarity was the dependent variable and phonologic and semantic relatedness scores and the SAPS–FTD subscore were the independent variables. We used the SPSS 13.0 version for all analyses. 3. Results The method we used to quantify and calculate the word association patterns (semantic and/or phonologic) had a high interrater reliability (the interclass correlation coefficients were 0.983 for categoric relations, 0.938 for contextual relations and 0.915 for phonologic relations.) Controls performed significantly better on VF compared to the patients and their siblings (controls: 70.34 ± 17.7, patients: 49.52 ± 19.7, siblings: 52.58± 12.4) (F =14.14, df= 2, pb 0.001). Post-hoc analysis revealed that patients' and siblings' performance were similar. Comparison of peculiar word use and semantic and phonologic relatedness ratings among the three groups is presented in Table 2. The overall MANOVA was significant (Wilk's lambda = 0.564, F = 10.07, p b 0.001).
Table 3 Correlations of peculiarity, relation patterns and total FTD scores for three groups Semantic relatedness score (Pearson correlation, p) Patients group
Siblings group Control Group
FS SRS PRS FS SRS FS SRS
Phonologic relatedness score (Pearson correlation, p)
FTD score (sum of SAPS–FTD items) (Pearson correlation, p)
0.14, p = 0.44
− 0.55, p = 0.01⁎ − 0.23, p = 0.19
0.11, p = 0.17
− 0.57, p = 0.001⁎ 0.02, p = 0.91 0.25, p = 0.16 0.20, p = 0.25
− 0.51, p = 0.02⁎ − 0.22, p = 0.21 0.66, p = 0.001⁎
− 0.07, p = 0.7
FS = familiarity score, SRS = semantic relatedness score, PRS = phonologic relatedness score, FTD = SAPS formal thought disorder subscore, ⁎Statistically significant.
B. Baskak et al. / Schizophrenia Research 103 (2008) 311–317
As shown in Table 2, patients and siblings differed from controls not only in terms of their tendency to use a higher number of peculiar words (as indicated by the higher familiarity score in the control group) but also in terms of lower semantic relatedness scores. The phonologic relatedness scores, on the other hand, were not significantly different between the three groups. The Pearson correlation coefficients among the familiarity score, semantic relatedness score, phonologic relatedness score and SAPS–FTD subscore are presented in Table 3. The three groups showed different patterns of correlations. In the patient group peculiarity was correlated with phonologic relations and FTD. In the sibling group peculiarity was correlated with phonologic relations. For either group there was no correlation between semantic relations and peculiarity. In the control group no correlation was found between peculiarity and any of the word relation patterns. Stepwise linear regression analyses revealed different relationship patterns for the three groups: In the patient group phonologic relations were included in the model that explained 30% of the variance in peculiarity (r-square = 0.297, Beta = − 0.55 SD = 1.67, t = − 3.62, p b 0.001). Semantic relations and FTD were excluded from the model. A similar pattern was found for the siblings group where phonological relations were responsible for 32% of the variance in peculiarity (r-square =0.323, Beta= −0.57, SD =0.69, t=−3.72, p b 0.001). Semantic relations were excluded from the model. Peculiarity was not explained by either semantic or phonologic relations in the control group. Patients and their siblings produced more unique words than controls (patients: 0.33 ± 0.14, siblings: 0.30 ± 0.14, controls: 0.20 ± 0.06) (F = 10.71, p b 0.001). Patients produced more neologisms than both their siblings and controls (patients; 0.03± 0.03, siblings; 0.01 ± 0.01 and controls; 0.003 ± 0.007) (F = 11.55, df = 2, p b 0.001). 4. Discussion This study used an operationalized definition and a new, standard and reliable rating of peculiar word use in order to compare its severity among patients with schizophrenia, their healthy siblings and healthy controls as well as to analyze the relationship of peculiar word use with the tendency to use semantic or phonologic word associations during a VF task. Relationships among peculiar word use, word association patterns (semantic versus phonologic) and the severity of FTD were also explored in the three groups using correlation and regression analyses. One important finding was that patients and their siblings were similar to one another and different from
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healthy controls in terms of their tendency to generate a higher number of peculiar words as well as their tendency to rely less on semantic associations during the VF task. Second, peculiar word use was associated with the severity of formal thought disorder and the tendency to make use of phonologic associations in the patient group as well as their siblings, but not in healthy controls. Finally, peculiar word use was predicted only by the frequency of phonologic associations (and not by the frequency of semantic associations) in the patient and sibling groups, whereas neither of the word association patterns predicted peculiar word use in the control group. As pointed out by Harvey (2000), research on language and communication in schizophrenia should integrate linguistic methods with clinical and neurocognitive assessment. A unit-by-unit analysis of speech as we utilized in this study may be useful to determine subtle forms of language abnormalities to be used in future studies. To our knowledge this is the first study that quantified peculiar word use with an objective and reliable method and explored its relationships with word association patterns and the severity of formal thought disorder. The method stipulated a quantification of peculiarity on a continuum rather than employing a forced choice between “peculiar” and “not peculiar”, which would have rendered the ratings more subjective and probably less ecologically valid. This appears to be an important advantage of our method, since schizophrenic language is characterized by subtle forms of peculiarity rather than the frequent use of definitely bizarre words, neologisms or idiosyncrasies. Another advantage of this method is that it allows a quantification of peculiar word use in healthy relatives, who are even less likely to exhibit obvious examples of peculiarity. The tendency of our patient group to generate a higher number of rarely used words provides empirical support to previous observations about the peculiarity of schizophrenic speech (Pinard and Lecours, 1983; Holzman et al., 1986; Liddle et al., 2002). The more remarkable finding was the similarity between healthy siblings and patients in terms of their tendency to peculiar word use. Since peculiar word use is a language related abnormality, this finding might support the hypothesis that epigenetic variations associated with chromosomal rearrangements relates to the evolution of language could account for predisposition to schizophrenia (Crow, 2007). Studies with larger sample sizes will yield more accurate estimates of the effect size of the difference. The tendency to use peculiar words (as quantified by the number of rarely used words by a healthy population) deserves further study as a trait marker candidate for schizophrenia. In general,
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besides being capable of identifying asymptomatic carriers, a trait marker is considered to be stable and unaffected by treatment status (Gorman and Papp, 1994). Therefore before accepting peculiar word use as a trait marker, it should also be shown in longitudinal studies and especially in antispychotic naive patients. If peculiar word use is identified as an endophenotype, it could be integrated in future studies that will collect data on other correlates of schizophrenia, such as imaging or genetics. Goldberg et al. (1998) suggested that thought disorder in schizophrenia is associated with and may result from semantic processing abnormalities. Kerns et al. (1999) showed that formal thought disorder was associated with producing fewer semantically related words. Chen et al. (2000) suggested that excess use of sound-based associations is a presentation of formal thought disorder. Our results suggest that the relationship of peculiar word use with the tendency to use phonologic relations may be a consequence of an effort to compensate defects in semantic association (categorization) by relying more on phonologic associations. Peculiar word use could be associated with a deficit to employ categoric classifications in VF tasks and thus relying on sound-based associations. This could be related with the executive dysfunction in schizophrenia. Deficits in executive functioning (e.g. concept formation) could also be included in future studies to support this explanation. Excess use of phonologic relations may be playing a mediating role between semantic processing abnormalities and formal thought disorder. Some presentations of formal thought disorder like tangentiality may be directly related with defects in semantic processing, while a phonologic compansation compensation may be playing a more predominant role in some other formal thought disorders like clang associations, peculiar word use, neologisms or derailment. The main limitation of this study is the sample size, especially of the “pool”, which served as the norm on which the peculiarity scores were based. Therefore this study should better be regarded as a pilot study with positive results, thus justifying larger studies in different cultures, more heterogeneous groups and different languages with varying phonetic properties. Second, similar sociocultural background and/or upbringing in the same household might have resulted in a similar vocabulary in the patient and sibling groups, thus approximating both the performance and the association patterns in the two groups. Although the groups were matched in terms of education, this possibility cannot be completely ruled out with available data. Future studies could enroll healthy siblings from other patients' families and overcome this limitation. A third limitation
of the study is that psychiatric disorders other than those with overt psychosis were not ruled out in the healthy groups. Our groups consisted of patients with varying levels of formal thought disorder. The relationship of peculiarity with formal thought disorder may better be understood if studied in schizophrenia patients with and without this symptom. If the value of peculiar word used as a trait marker can be confirmed in larger groups, the following studies could look at the differences between patients with and without formal thought disorder. Finally, it must be noted that in the Turkish Language, deriving a new word from a root involves the use of suffices more frequently than the use of prefaces. We believe that this property of Turkish must have had a similar influence in the use of semantic and phonologic associations as well as the choice of rare (peculiar) and common (familiar) words and therefore not biased the results. However, studies in different languages are definitely needed, if peculiar word use will be tested as a potential universal trait marker for schizophrenia.
Role of funding source Funding for this study; design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication was provided by the authors. Contributors Bora Baskak and E. Tugba Ozel Kizil designed the study and wrote the protocol. E. Tugba Ozel Kizil and Seda Baskak collected the data. Bora Baskak and E. Cem Atbasoglu undertook the statistical analysis. Seda Celik Baskak contributed to the design of the study and the writing of the manuscript. Bora Baskak completed the literature search. E. Cem Atbasoglu supervized supervised the study design and the writing of the manuscript. All authors contributed to and have approved the final manuscript. Conflict of interest All authors declare that they have no conflicts of interest. Acknowledgement None.
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Schizophrenia Research 103 (2008) 311 – 317 www.elsevier.com/locate/schres
Peculiar word use as a possible trait marker in schizophrenia Bora Baskak a,⁎, E. Tugba Ozel a , E. Cem Atbasoglu a , Seda C. Baskak b a
Ankara University, School of Medicine, Psychiatry Department, Neuropsychiatry Research Unit, Dikimevi, Ankara, Turkey b Bolu Izzet Baysal Psychiatry Hospital, Turkey Received 1 January 2008; received in revised form 11 April 2008; accepted 18 April 2008 Available online 5 June 2008
Abstract Peculiar word use in schizophrenia has been emphasized by many authors, however the definition or the linguistic and clinical correlates of this phenomenon are not clear. We propose a new, standard and reliable method to extract a numerical measure of peculiar word use with operationalized definitions. We applied a modified version of the Controlled Word Association Test (Turkish version) to a pool of healthy subjects (N = 55) and used the data as norm to compare the degree of peculiarity and patterns of word association among patients with schizophrenia (N = 33), their healthy siblings (N = 31) and healthy controls (N = 32). We also explored the relationship of peculiar word use with patterns of word association (semantic versus phonologic) and formal thought disorder. Patients and their siblings performed worse on measures of verbal fluency. They also generated more peculiar words and relied less on semantic associations, compared to healthy controls. Peculiar word use was associated with the severity of formal thought disorder and the tendency to make use of phonologic associations in the patient group and their siblings, whereas neither of the word association patterns predicted peculiar word use in the control group. Our results provide empirical support to previous observations about the peculiarity of schizophrenic speech. Peculiar word use could be associated with a deficit to employ semantic classifications in verbal fluency tasks and thus relying more on sound-based associations. Excess use of phonologic associations may be playing a mediating role between semantic processing abnormalities and formal thought disorder. © 2008 Elsevier B.V. All rights reserved. Keywords: Schizophrenia; Schizophrenic language; Siblings; Semantics; Phonetics
1. Introduction Schizophrenia patients demonstrate multilevel language impairments that have been accepted as one of the fundamental (Bleuler, 1950), and diagnostic (American Psychiatric Association, 1994) signs of schizophrenia. These impairments include phonetic abnormalities (e.g., errors in timing, intonation and quality of speech) (Rieber and Vetter, 1994) and semantic abnormalities such as impaired semantic store (Chen et al., 2000), ⁎ Corresponding author. Tel.: +90 312 595 62 47. E-mail address: [email protected] (B. Baskak). 0920-9964/$ - see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.schres.2008.04.025
retrieval (Allen et al., 1993) and deficits in structure of semantic network (Aloia et al., 1996). Following Crow's (2000) hypothesis about the coheritability of language and schizophrenia, DeLisi (2001) highlighted that deficits in specifically human aspects of language may be related to the genetics of schizophrenia. In a recent review Covington et al. (2005) addressed the need for studies about the heredity of schizophrenic language impairment that may provide a solid biological basis for the disease. Some language abnormalities (e.g. deficits in verbal fluency [VF]) have been shown in healthy relatives of schizophrenic patients (Laurent et al., 2000) and proposed as possible
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trait markers of predisposition to schizophrenia (Chen et al., 2000). Peculiar word use is one of the language abnormalities in schizophrenia that has been emphasized by many authors (Harrow and Prosen, 1979; Pinard and Lecours, 1983; Johnston and Holzman, 1979; Holzman et al., 1986; Solovay et al., 1987; Liddle et al., 2002). Despite the fact that it is a common clinical observation, studies involving quantitative assessment of this abnormality are relatively scarce, probably because agreement on the degree of peculiar word use is more difficult compared to other language abnormalities. Pinard and Lecours (1983) observed that schizophasic discourse often included rare words, and interpreted this as evidence of a large and intact vocabulary in schizophrenia. Johnston and Holzman (1979) proposed that the peculiar verbalizations in schizophrenic speech were representations of the underlying thought disorder. Holzman et al. (1986) later highlighted that the thinking of schizophrenic patients was confused and fluid, usually peppered with many idiosyncratic and peculiar words and phrases. Thus, in Johnston and Holzman's Thought Disorder Index (TDI) (1979), peculiar verbalizations represent a very mild qualitative form of thought disorder. They are subjectively identified and rated for frequency of instances during a Rorschach Inkblot Test. Liddle et al. (2002) operationally defined and grounded peculiarity in a continuous spectrum as a weaker form of neologism in the Thought and Language Index (TLI). Peculiarity of speech is rated as a separate item in these two scales — ‘peculiar word use’ in the TLI and ‘idisyncratic verbalizations’ in the TDI. It should be noted, however, that both these items have a weak interrater reliability; in fact they achieve the lowest interrater reliability figures among the other items in the TLI and TDI. Low interrater agreement could be due to a higher degree of subjectivity involved in rating peculiarity unless the patient's speech is analyzed quantitatively. This subjectivity is probably a consequence of the difficulty in making an operational definition of peculiarity, compared to other abnormalities in language, which either lend themselves to a more strict definition (e.g., loosening of associations, tangentiality, etc.), or are more readily observable since they are severe by definition (e.g., neologisms or incoherence). Patients with schizophrenia rarely use words that are obviously peculiar (Cuesta and Peralta, 1999). Rather, peculiarity of schizophrenic speech can be identified through detection of subtle examples that take place on a continuum between ‘normal’ and ‘obviously peculiar’. A unit-by-unit analysis of the patient's speech targeting to extract a relatively accurate numerical measure of peculiarity would address the issue of subjectivity in assessment, however, such a method would be time-consuming,
compared to the assessment of other symptoms. Thus a relatively practical method that is capable of identifying slight forms of peculiarity with a higher degree of interrater reliability could prove useful in clinical research. The first aim of this study is to propose and test the reliability of a method that would achieve the standards mentioned above. We propose a method that involves a modified version of the Controlled Oral Word Association Test COWAT (Lezak, 1995) in rating peculiar word use. This allows the rater to base the rating of the peculiarity of each word uttered by the subject on the frequency of its use by a pool group, rather than making a forced choice between “peculiar” and “non-peculiar”. The second aim of the study is to test the hypothesis that peculiar word use is more common in schizophrenia patients and their healthy relatives compared to healthy controls, in order to study the potential value of peculiarity as a trait marker for schizophrenia. We were also interested in the relationship of peculiar word use with patterns of association between the uttered words. The relationship of peculiar word use with other forms of thought disorder has been theoretically explained by some authors, but empirical research on this question is scarce. One assumption is that excess use of sound-based (compared to context-based) associations renders schizophrenic speech “difficult to understand”. Chaika (1974) speculated that the structure of speech in schizophrenia is disturbed because of a distraction by the sounds of words, so that a discourse becomes a non-informative string of word associations. This was referred to as ‘glossomania’ by Pinard and Lecours (1983) and later used by Andreasen (1987) for the definition of derailment and clang associations. In fact, verbal fluency (VF) studies point out to a disproportionate impairment of semantic relative to phonetic fluency in schizophrenia patients (Kremen et al., 2003; Phillips et al., 2004; Bozikas et al., 2005). However, the relationship of this language abnormality with peculiar word use has not been empirically tested before. Thus, the third aim of this study is to test the hypothesis that the degree of peculiar word use is associated with a disproportionate amount of phonetic compared to semantic associations by using operationalized definitions and reliable measures for both peculiarity and word association patterns. 2. Methods and materials 2.1. The groups The Turkish version of the modified COWAT (Lezak, 1995), as will be described below, was first applied to 55 healthy subjects (relatives or acquaintances of the
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she had attributed to that word and the answer was noted. Then the word lists were analyzed by two blind raters for the following variables: Total VF performance: The sum of the total number of words starting with the letter ‘a’ and the letter ‘s’ generated by the subject during COWAT. In order to control the influence of VF performance, all scores were divided by the total VF performance. Familiarity score: The number of times that a word was generated by the subjects in the pool group. For example a word generated by 4 subjects in the pool would have a familiarity score of 4. Perseverated words and neologisms were not counted. Peculiarity score: This was defined as the inverse of the familiarity score (1 / familiarity). Uniqueness score: Number of unique words, i.e., words that were not generated by any subject in the pool. Neologism score: Total number of neologisms generated by the patient. A word was accepted as a neologism when the word was not recognized by any of the two raters and was not included in a comprehensive dictionary of Turkish (Turkish Dictionary of Turkish Language Association, 2000). In order to analyze the word association pattern, the raters assessed all word pairs, i.e., all two consecutive words in the list, e.g., the first and the second, the second and the third…, so that the total number of pairs was n + 1 in a list of n words. In order to identify all associations, each word uttered by the subject was assessed for the presence or absence of a semantic or phonologic relation with the preceding one, e.g., the 2nd with the 1st, 3rd with the 2nd… 11th with the 10th. All relatedness scores were also controlled for (divided by) the total VF performance. Semantic relationship has been defined as a categoric or a contextual relationship (Kerns et al., 1999). Categoric relatedness score was the sum of categoric relations (two words that belong to the same category like two animals, two country names, two human names etc.).
hospital staff, stratified for their level of education) in order to generate a “pool” that would constitute the norm for the frequency of the words to be generated by the study groups. The three study groups were 33 consecutive outpatients followed with a diagnosis of DSM-IV schizophrenia at a university hospital, 31 non-psychotic siblings of schizophrenia patients and 32 healthy controls. All patients were under medication with atypical antipsychotics and clinically stable at the time of the study, as indicated by their Scale for the Assessment of Positive (SAPS) and Negative Symptoms (SANS) scores (Andreasen, 1987). The groups were matched for age, education and balanced for sex. All subjects signed written informed consent. The Turkish version of the modified form of COWAT was applied to the three groups and their familiarity and peculiarity scores were calculated based on the frequency of the words in the pool group. The pool group, as well as the controls and siblings of schizophrenia patients were evaluated by two experienced psychiatrists in order to rule out the existence of a psychotic disorder or a history of any psychiatric treatment. However, disorders other than those with overt psychosis were not assessed in detail. Sociodemographic and clinical features of the three groups are presented in Table 1. 2.2. Evaluation of peculiar word use and association patterns with the COWAT Subjects were expected to generate as many words as they could starting with the letter ‘a’ and the letter ‘s’ (frequently used vowel and consonant, respectively, in Turkish) during a period of 3 min for each. The words generated were audiorecorded and listed by a rater. If the subject produced a neologism or generated a word that was difficult to understand, he/she was asked what he/ Table 1 Sociodemographic and clinical features of the groups
Gender (F/M) Age (years ± SD) Education (years ± SD) Mean duration of illness (years ± SD) SAPS score (sum of all items) (mean ± SD) FTD score (sum of all items) (mean ± SD) SANS score (sum of all items) (mean ± SD)
Patients
Siblings
Controls
N = 33
N = 31
N = 32
15/18 32.3 ± 9.9 12.0 ± 2.2 5.0 ± 4.8 30.66 ± 18.54 8.87 ± 7.54 33.66 ± 15.05
The “Pool” N = 55 2
12/19 33.9 ± 10.2 12.9 ± 6.0
16/16 34.9 ± 9.9 12.5 ± 3.9
X = 0.82, p = 0.66 F = 0.66, df = 2, p = 0.52 F = 0.44, df = 2, p = 0.65
28/27 27.6 ± 9.2 11.3 ± 3.2
– – –
– – –
– – –
– – –
F: female, M: male, SD: standard deviation, FTD: formal thought disorder, SAPS: Scale for the Assessment of Positive Symptoms, SANS: Scale for the Assessment of Negative Symptoms.
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Table 2 Comparison of the three groups for peculiarity and relatedness scores (MANOVA)
Familiarity score (1 / peculiarity score) Semantic relatedness score Phonologic relatedness score
Patients (n = 33)
Siblings (n = 31)
Controls (n = 32)
(mean ± SD)
(mean ± SD)
(mean ± SD)
4.43 ± 0.34 0.204 ± 0.128 0.268 ± 0.159
4.07 ± 0.31 0.165 ± 0.104 0.309 ± 0.129
6.11 ± 0.15 0.359 ± 0.124 0.231 ± 0.089
F = 14.73 df = 2 p b 0.001⁎ F = 23.11 df = 2 p b 0.001⁎ F = 2.88 df = 2 P = 0.061
SD= standard deviation, ⁎Post-hoc analysis: controls N patients = siblings for familiarity and semantic relatedness scores.
Contextual relatedness score was the total number of two temporally (like armour and ammo) or functionally (like spoon and soup) related word pairs. Thus, the Semantic relatedness score was the sum of categoric and contextual relatedness scores. Phonologic relatedness was defined as the presence of either a shared syllable or a phoneme or a rhyme in two consecutive words. Phonologic relatedness score was the sum of phonologic relations between the words. Total relatedness score was the sum of word pairs that were either semantically or phonologically related. Raters performed a pilot study on 20 word lists to secure high interrater reliability regarding the relatedness scores. 2.3. Analysis We compared the total VF performance and scores of uniqueness and neologism between the three groups with analyses of variance (ANOVA). Peculiarity and scores of semantic and phonologic relatedness were compared with a multivariate analysis of variance (MANOVA). The distributions of peculiarity and familiarity scores were tested for normality by the Kolmogorov–Smirnov Test. Peculiarity scores were skewed (p b 0.001), whereas familiarity scores were normally distributed (p = 0.098). Therefore we included the familiarity scores (1 / peculiarity) in the statistical analyses.
Pearson correlation coefficients were calculated to test the relationships between peculiarity, severity of formal thought disorder and relatedness patterns. Finally, in order to examine the relationship of peculiarity with semantic and phonologic relations and the severity of formal thought disorder, we applied a stepwise linear regression, where peculiarity was the dependent variable and phonologic and semantic relatedness scores and the SAPS–FTD subscore were the independent variables. We used the SPSS 13.0 version for all analyses. 3. Results The method we used to quantify and calculate the word association patterns (semantic and/or phonologic) had a high interrater reliability (the interclass correlation coefficients were 0.983 for categoric relations, 0.938 for contextual relations and 0.915 for phonologic relations.) Controls performed significantly better on VF compared to the patients and their siblings (controls: 70.34 ± 17.7, patients: 49.52 ± 19.7, siblings: 52.58± 12.4) (F =14.14, df= 2, pb 0.001). Post-hoc analysis revealed that patients' and siblings' performance were similar. Comparison of peculiar word use and semantic and phonologic relatedness ratings among the three groups is presented in Table 2. The overall MANOVA was significant (Wilk's lambda = 0.564, F = 10.07, p b 0.001).
Table 3 Correlations of peculiarity, relation patterns and total FTD scores for three groups Semantic relatedness score (Pearson correlation, p) Patients group
Siblings group Control Group
FS SRS PRS FS SRS FS SRS
Phonologic relatedness score (Pearson correlation, p)
FTD score (sum of SAPS–FTD items) (Pearson correlation, p)
0.14, p = 0.44
− 0.55, p = 0.01⁎ − 0.23, p = 0.19
0.11, p = 0.17
− 0.57, p = 0.001⁎ 0.02, p = 0.91 0.25, p = 0.16 0.20, p = 0.25
− 0.51, p = 0.02⁎ − 0.22, p = 0.21 0.66, p = 0.001⁎
− 0.07, p = 0.7
FS = familiarity score, SRS = semantic relatedness score, PRS = phonologic relatedness score, FTD = SAPS formal thought disorder subscore, ⁎Statistically significant.
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As shown in Table 2, patients and siblings differed from controls not only in terms of their tendency to use a higher number of peculiar words (as indicated by the higher familiarity score in the control group) but also in terms of lower semantic relatedness scores. The phonologic relatedness scores, on the other hand, were not significantly different between the three groups. The Pearson correlation coefficients among the familiarity score, semantic relatedness score, phonologic relatedness score and SAPS–FTD subscore are presented in Table 3. The three groups showed different patterns of correlations. In the patient group peculiarity was correlated with phonologic relations and FTD. In the sibling group peculiarity was correlated with phonologic relations. For either group there was no correlation between semantic relations and peculiarity. In the control group no correlation was found between peculiarity and any of the word relation patterns. Stepwise linear regression analyses revealed different relationship patterns for the three groups: In the patient group phonologic relations were included in the model that explained 30% of the variance in peculiarity (r-square = 0.297, Beta = − 0.55 SD = 1.67, t = − 3.62, p b 0.001). Semantic relations and FTD were excluded from the model. A similar pattern was found for the siblings group where phonological relations were responsible for 32% of the variance in peculiarity (r-square =0.323, Beta= −0.57, SD =0.69, t=−3.72, p b 0.001). Semantic relations were excluded from the model. Peculiarity was not explained by either semantic or phonologic relations in the control group. Patients and their siblings produced more unique words than controls (patients: 0.33 ± 0.14, siblings: 0.30 ± 0.14, controls: 0.20 ± 0.06) (F = 10.71, p b 0.001). Patients produced more neologisms than both their siblings and controls (patients; 0.03± 0.03, siblings; 0.01 ± 0.01 and controls; 0.003 ± 0.007) (F = 11.55, df = 2, p b 0.001). 4. Discussion This study used an operationalized definition and a new, standard and reliable rating of peculiar word use in order to compare its severity among patients with schizophrenia, their healthy siblings and healthy controls as well as to analyze the relationship of peculiar word use with the tendency to use semantic or phonologic word associations during a VF task. Relationships among peculiar word use, word association patterns (semantic versus phonologic) and the severity of FTD were also explored in the three groups using correlation and regression analyses. One important finding was that patients and their siblings were similar to one another and different from
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healthy controls in terms of their tendency to generate a higher number of peculiar words as well as their tendency to rely less on semantic associations during the VF task. Second, peculiar word use was associated with the severity of formal thought disorder and the tendency to make use of phonologic associations in the patient group as well as their siblings, but not in healthy controls. Finally, peculiar word use was predicted only by the frequency of phonologic associations (and not by the frequency of semantic associations) in the patient and sibling groups, whereas neither of the word association patterns predicted peculiar word use in the control group. As pointed out by Harvey (2000), research on language and communication in schizophrenia should integrate linguistic methods with clinical and neurocognitive assessment. A unit-by-unit analysis of speech as we utilized in this study may be useful to determine subtle forms of language abnormalities to be used in future studies. To our knowledge this is the first study that quantified peculiar word use with an objective and reliable method and explored its relationships with word association patterns and the severity of formal thought disorder. The method stipulated a quantification of peculiarity on a continuum rather than employing a forced choice between “peculiar” and “not peculiar”, which would have rendered the ratings more subjective and probably less ecologically valid. This appears to be an important advantage of our method, since schizophrenic language is characterized by subtle forms of peculiarity rather than the frequent use of definitely bizarre words, neologisms or idiosyncrasies. Another advantage of this method is that it allows a quantification of peculiar word use in healthy relatives, who are even less likely to exhibit obvious examples of peculiarity. The tendency of our patient group to generate a higher number of rarely used words provides empirical support to previous observations about the peculiarity of schizophrenic speech (Pinard and Lecours, 1983; Holzman et al., 1986; Liddle et al., 2002). The more remarkable finding was the similarity between healthy siblings and patients in terms of their tendency to peculiar word use. Since peculiar word use is a language related abnormality, this finding might support the hypothesis that epigenetic variations associated with chromosomal rearrangements relates to the evolution of language could account for predisposition to schizophrenia (Crow, 2007). Studies with larger sample sizes will yield more accurate estimates of the effect size of the difference. The tendency to use peculiar words (as quantified by the number of rarely used words by a healthy population) deserves further study as a trait marker candidate for schizophrenia. In general,
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besides being capable of identifying asymptomatic carriers, a trait marker is considered to be stable and unaffected by treatment status (Gorman and Papp, 1994). Therefore before accepting peculiar word use as a trait marker, it should also be shown in longitudinal studies and especially in antispychotic naive patients. If peculiar word use is identified as an endophenotype, it could be integrated in future studies that will collect data on other correlates of schizophrenia, such as imaging or genetics. Goldberg et al. (1998) suggested that thought disorder in schizophrenia is associated with and may result from semantic processing abnormalities. Kerns et al. (1999) showed that formal thought disorder was associated with producing fewer semantically related words. Chen et al. (2000) suggested that excess use of sound-based associations is a presentation of formal thought disorder. Our results suggest that the relationship of peculiar word use with the tendency to use phonologic relations may be a consequence of an effort to compensate defects in semantic association (categorization) by relying more on phonologic associations. Peculiar word use could be associated with a deficit to employ categoric classifications in VF tasks and thus relying on sound-based associations. This could be related with the executive dysfunction in schizophrenia. Deficits in executive functioning (e.g. concept formation) could also be included in future studies to support this explanation. Excess use of phonologic relations may be playing a mediating role between semantic processing abnormalities and formal thought disorder. Some presentations of formal thought disorder like tangentiality may be directly related with defects in semantic processing, while a phonologic compansation compensation may be playing a more predominant role in some other formal thought disorders like clang associations, peculiar word use, neologisms or derailment. The main limitation of this study is the sample size, especially of the “pool”, which served as the norm on which the peculiarity scores were based. Therefore this study should better be regarded as a pilot study with positive results, thus justifying larger studies in different cultures, more heterogeneous groups and different languages with varying phonetic properties. Second, similar sociocultural background and/or upbringing in the same household might have resulted in a similar vocabulary in the patient and sibling groups, thus approximating both the performance and the association patterns in the two groups. Although the groups were matched in terms of education, this possibility cannot be completely ruled out with available data. Future studies could enroll healthy siblings from other patients' families and overcome this limitation. A third limitation
of the study is that psychiatric disorders other than those with overt psychosis were not ruled out in the healthy groups. Our groups consisted of patients with varying levels of formal thought disorder. The relationship of peculiarity with formal thought disorder may better be understood if studied in schizophrenia patients with and without this symptom. If the value of peculiar word used as a trait marker can be confirmed in larger groups, the following studies could look at the differences between patients with and without formal thought disorder. Finally, it must be noted that in the Turkish Language, deriving a new word from a root involves the use of suffices more frequently than the use of prefaces. We believe that this property of Turkish must have had a similar influence in the use of semantic and phonologic associations as well as the choice of rare (peculiar) and common (familiar) words and therefore not biased the results. However, studies in different languages are definitely needed, if peculiar word use will be tested as a potential universal trait marker for schizophrenia.
Role of funding source Funding for this study; design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication was provided by the authors. Contributors Bora Baskak and E. Tugba Ozel Kizil designed the study and wrote the protocol. E. Tugba Ozel Kizil and Seda Baskak collected the data. Bora Baskak and E. Cem Atbasoglu undertook the statistical analysis. Seda Celik Baskak contributed to the design of the study and the writing of the manuscript. Bora Baskak completed the literature search. E. Cem Atbasoglu supervized supervised the study design and the writing of the manuscript. All authors contributed to and have approved the final manuscript. Conflict of interest All authors declare that they have no conflicts of interest. Acknowledgement None.
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