Int J Psychiatry Clin Pract 2015; 19: 40–44. © 2015 Informa Healthcare ISSN 1365-1501 print/ISSN 1471-1788 online. DOI: 10.3109/13651501.2014.981544

ORIGINAL ARTICLE

Neurological soft signs in adolescents with borderline personality traits

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Jinqiang Zhang1,2, Lin Cai1,3, Xiongzhao Zhu1,2, Jinyao Yi1,2, Shuqiao Yao1,4, Muli Hu1, Mei Bai1, Lingyan Li1 & Yuping Wang1 1

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Medical Psychological Institute, Second Xiangya Hospital, Central South University, Changsha, P. R. China, 2National Technology Institute of Psychiatry, Central South University, Changsha, P. R. China, 3School of Sociology and Psychology, Southwest University for Nationalities, Chengdu, Sichuan, P. R. China, and 4Key Laboratory of Psychiatry and Mental Health of Hunan Province, Central South University, Changsha, P. R. China Abstract Objective. This study investigated the prevalence and severity of neurological soft signs (NSS), and their relationships with borderline personality (BP) traits in adolescents. Methods. Eighty-nine adolescents with BP traits (BP-trait group), and 89 adolescents without traits of any personality disorder (control group), were recruited in China. BP traits were diagnosed by the BPD subscale of the Personality Diagnostic Questionnaire for the DSM-IV (PDQ-4⫹). The soft sign subscales of the Cambridge Neurological Inventory were administered to all participants. The group differences in prevalence of soft signs and in NSS scores were analyzed, as well as the associations between the NSS scale and borderline personality traits. Results. Five soft signs were significantly more frequent in adolescents with BP traits. A total of 59.6% of adolescents with BP traits exhibited at least 1 NSS, whereas only 34.8% of adolescents without BP traits did (p ⬍ 0.01). A total of 42.7% of adolescents in the BP-trait group exhibited at least 2 NSS, while only 16.9% of adolescents without BP traits did (p ⬍ 0.001). Moreover, adolescents with BP traits showed more sensory integration, disinhibition, total neurological soft signs, left-side soft signs, and right-side soft signs, than adolescents without BP traits. Sensory integration and disinhibition were positively associated with BP traits. Conclusion. These findings suggest that adolescents with BP traits may have a nonfocal abnormality of the central nervous system. Key words: Neurological soft signs, borderline personality, traits, adolescents (Received 14 July 2014; accepted 16 October 2014)

Introduction Borderline personality disorder (BPD) is a severe mental illness characterized by affective disturbance, disturbed cognition, impulsivity, and intensely unstable relationships (American Psychiatric Association 1994). Individuals with BPD have a tendency of suicide, self-injury, and distress, and are associated with substantial morbidity of other mental disorders and impaired cognitive function (Ansell et al. 2007; Skodol et al. 2002; Yen et al. 2004). Early manifestations of BPD usually appear during adolescence, as early as 14 years of age (Chanen et al. 2004; Meijer et al. 1998; Westen et al. 2003). The reported prevalence of BPD in adolescents ranges from 2% to 14% (Bernstein et al. 1993; Chabrol et al. 2001;Leung and Leung 2009). Although BPD is one of the most frequently studied personality disorders, the physiopathologic processes involved in the development of BPD remain unclear. Studies with electroencephalographic (EEG) scalp records have demonstrated that individuals with BPD exhibit non-EEG-localizable brain dysfunction (Cowdry et al. 1985; De la Fuente et al. 1998; Tanahashi 1988; Van Reekum 1993). Mauchnik et al. recently reviewed Correspondence: Xiongzhao Zhu, PhD, MD, Medical Psychological Institute, Second Xiangya Hospital, Central South University, Changsha, Hunan 410011, P. R. China. Tel: ⫹ 86 731 85292126. Fax: ⫹ 86 731 85361328. E-mail: [email protected]

publications on neuroimaging studies of BPD, and concluded that structural and functional brain dysfunctions exist in BPD (Mauchnik and Schmahl 2010). Neurological soft signs (NSS) are nonspecific indicators of brain dysfunction, which present as nonlocalizing minor neurological abnormalities in sensory integration, motor coordination, and sequencing of complex motor tasks (Shaffer et al. 1983). NSS were observed both in individuals that displayed clinical symptoms of psychosis, and those that displayed minor, non-clinical signs of psychopathology, which were considered characteristics of individuals with an underlying vulnerability to psychopathology (Levit-Binnun and Golland 2012). Studies indicate that higher frequencies of NSS are present in patients with BPD (Brown et al. 2009; De la Fuente et al. 2006, 2011; Gardner et al. 1987; Reynolds and Lane 2008; Stein et al. 1993). De la Fuente et al. (2006) found that 100% of the BPD patients in their study had one or more NSS, while only 35% of healthy individuals had one or more soft signs. It has been reported that BP traits mainly occur in adolescents, and adolescents who exhibit BP traits are at high risk for the development of BPD (Bornovalova et al. 2009; Winograd et al. 2008). Adolescence is a period characterized by significant neurological development. Therefore, adolescents with BP traits are ideal for accurate evaluation of the abnormal brain development involved in early BPD

NSS in adolescents with BP traits 41

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DOI: 10.3109/13651501.2014.981544

progression, because there are fewer confounding factors of treatment or side effects of treatment on brain morphology in adolescents, in contrast to adults. However, most of the current studies only measure NSS in patients with BPD, and very little is known about individuals who demonstrate only BP traits. Whether adolescents with BP traits are associated with higher frequencies of NSS has rarely been reported, and requires investigation. BPD commonly exhibits co-morbidity with other personality disorders, such as schizotypal personality disorder and antisocial personality disorder (Becker et al. 2000). These two personality disorders have recently been demonstrated to coincide with higher levels of NSS (Chan et al. 2010; Stein et al. 1993). However, previous studies did not exclude BPD patients with these two personality disorders. Therefore, it is difficult to know whether BPD is independently related to NSS. Furthermore, the adolescents displayed a broader pattern of co-morbidity of BPD than adults, and it is not clear whether adolescents with BP traits correlated with NSS independently. In this study, we investigated the prevalence and severity of neurological soft signs, and their relationship with BP traits in adolescents. Methods Participants A total of 3167 adolescents were recruited by cluster sampling from middle and high schools of 5 cities in China (Beijing, Suzhou, Changsha, Chengdu and Yinchuan). The participants were excluded if (1) they had a history of head injury, neurological disease or mental disorders, (2) they suffered from alcoholism or drug abuse, and (3) could not provide consent forms signed by themselves or by their guardians. The final sample consisted of 3010 adolescents (1522 male vs.1488 female), with ages ranging from 14 to 18 years (16.33 ⫾ 1.15 years). Most individuals (94.0%) were Han Chinese, and only 6.0% belonged to an ethnic minority, which is similar to the ethnic distribution of the Chinese population. The study was approved by the Ethics Committee of Central South University. According to the cut-off scores on the subscales of the Personality Diagnostic Questionnaire for the DSM-IV (PDQ-4⫹), eighty-nine individuals with a raw score equal to or higher than the cut-off score on the BPD subscale of PDQ-4⫹, and without co-morbidity of other personality disorders, were considered to have psychometrically defined BP traits (BP-trait group), and eighty-nine participants (gender matched) with raw scores below the cut-off scores of any personality disorder subscales of PDQ-4⫹ were randomly selected as healthy controls (control group). There were no significant group differences in age, sex, and right-handedness (Table I), while the BP-trait group scored significantly higher on the BPD subscale of PDQ-4⫹ than the control group. Measurements Personality diagnostic questionnaire for DSM-IV. The selfreported PDQ-4 ⫹ was adopted to screen for the presence or absence of 12 kinds of personality disorder traits in the DSM-IV, which includes 107 items and is answered using a

Table I. Demographic parameters and the BPD subscale of PDQ-4 ⫹ for the BP-trait group and the control group. BP-trait group (N ⫽ 89)

Control group (N ⫽ 89)

Age (years) 16.28 ⫾ 1.02 16.43 ⫾ 1.20 Male: female 27:62 27:62 Right handed 89 87 BPD score 6.36 ⫾ 0.64 1.38 ⫾ 1.61

t value x2 value P value 0.88 0.00 2.02 27.14

0.382 1.000 0.155 0.000

true/false format (Hyler 1994). The Chinese version of the PDQ-4 ⫹ has been demonstrated to be reliable, and has been validated (Yang et al. 2000; Ling et al. 2010; Huang et al. 2007). The borderline personality subscale of the PDQ-4 ⫹ includes 9 items, each of which represents a single DSM-IV diagnostic criterion (Hyler 1994). The original author of the PDQ-4 ⫹ suggested a cut-off score of 5 or higher for BPD (Hyler 1994); however, the PDQ-4 ⫹ showed higher negative predictive power than positive predictive power when screening for the presence or absence of personality disorder categories in Chinese psychiatric patients (Chan et al. 2010), so in this study, we adopted a cut-off score of 6 or higher to define borderline personality traits, consisting of raw scores at the top fifth percentile of the current sample. Cut-off scores of other subscales of the PDQ-4⫹, suggested by the original author, were also adopted to exclude individuals with any traits of the other 11 personality disorders (Paranoid, Schizoid, Schizotypal, Antisocial, Histrionic, Narcissistic, Depressive, Avoidant, Dependent, Obsessive-Compulsive, and Negativistic). Cambridge neurological inventory. Neurological soft signs were examined using cambridge neurological inventory (CNI), as previously described (Chen et al. 1995). The CNI consists of three subscales: motor coordination (MC), sensory integration (SI), and disinhibition (DI). Each of these soft signs was scored with 0 (absent), 1 (present), or 2 points (strongly present where applicable). Soft signs that could be scored on both the left and right sides were treated as independent scores. Higher scores indicate more severe NSS. The Chinese version of CNI has demonstrated good psychometric properties (Chen et al. 2000; Chan et al. 2010). In our study, the inter-rater reliability of the soft signs examined was evaluated by comparing the investigators’ ratings with those of 15 videotaped examinations. The intraclass correlation coefficient (ICC) was used to evaluate the inter-rater reliability. The ICC for the NSS total scale was 0.98, with a range of subscales from 0.96 to 0.99. Data analysis Data were analyzed using the Statistical Package for Social Sciences (SPSS) version 15.0. Data were presented as the mean ⫾ standard deviation (M ⫾ SD). The Mann-Whitney test was used to analyze the differences in prevalence of soft signs, while independent-samples t test and Cohen’s d value were used to analyze the differences in NSS scores between individuals with BP traits and those without traits of any personality disorder. Logistic regression analysis was used to predict associations between NSS and borderline

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Table II. Distribution of NSS in the BP-trait group and the control group.

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Signs MC Finger-thumb tapping (L) Finger-thumb tapping (R) Finger-thumb opposition (L) Finger-thumb opposition (R) Diadochokinesia (L) Diadochokinesia (R) Fist-edge-palm test (L) Fist-edge-palm test (R) Oseretsky test (L) Oseretsky test (R) SI Extinction Finger agnosia (L) Finger agnosia (R) Stereognosis (L) Stereognosis (R) Graphesthesia (L) Graphesthesia (R) Left-right orientation DI Mirror movements 1 (L) Mirror movements 1 (R) Mirror movements 2 (L) Mirror movements 2 (R) Go/no-go test At least 1 neurological soft sign At least 2 neurological soft signs

BP-trait group (N ⫽ 89) n (%)

Control group (N ⫽ 89) n (%)

x2 value

P value

0 (0.00) 1 (1.12) 3 (3.37) 1 (1.12) 2 (2.25) 0 (0.00) 8 (8.99) 6 (6.74) 7 (7.87) 8 (8.99)

1 (1.12) 2 (2.25) 3 (3.37) 2 (2.25) 0 (0.00) 0 (0.00) 3 (3.37) 4 (4.49) 6 (6.74) 5 (5.62)

1.01 0.34 0.00 0.34 2.02 – 2.42 0.42 0.08 0.75

0.316 0.560 1.000 0.560 0.155 – 0.120 0.515 0.773 0.387

3 (3.37) 30 (33.71) 26 (29.21) 3 (3.37) 6 (6.74) 8 (8.99) 7 (7.87) 11 (12.36)

1 (1.12) 9 (10.11) 10 (11.24) 1 (1.12) 3 (3.37) 8 (8.99) 3 (3.37) 3 (3.37)

1.02 14.48 8.91 1.02 1.05 0.00 1.70 4.96

0.312 0.000 0.003 0.312 0.305 1.000 0.193 0.026

9 (10.11) 3 (3.37) 1 (1.12) 0 (0.00) 6 (6.74) 53 (59.55) 38 (42.70)

1 (1.12) 1 (1.12) 0 (0.00) 0 (0.00) 0 (0.00) 31 (34.83) 15 (16.85)

6.78 1.02 1.01 – 6.21 10.91 14.21

0.009 0.312 0.316 – 0.013 0.001 0.000

Notes: L: left hand, R: right hand. Mirror movements 1: During Finger-thumb opposition. Mirror movements 2: During Dysdiadochokinesia.

personality traits. A value of p ⬍ 0.05 was considered statistically significant. Results The prevalence of NSS in the BP-trait group and in the control group NSS from the two groups are presented in Table II. Five soft signs were significantly more frequent in the BP-trait group. A total of 59.6% of the participants in the BP-trait group exhibited at least one NSS, whereas only 34.8% of the participants in the control group exhibited at least one NSS. A total of 42.7% of the participants in the BP-trait group exhibited at least two NSS, whereas only 16.9% of the participants in the control group exhibited at least two NSS.

The severity of NSS in the BP-trait group and in the control group The scores of NSS subscales, NSS total scale, left-side NSS and right-side NSS, are summarized in Table III. All scores, except the motor coordination subscale score, are significantly different between the two groups, and participants in the BP-trait group showed more severe NSS than those in the control group. Influence of BP traits on NSS Logistic regression analyses were performed to determine the associations between the NSS subscales, NSS total scale, and borderline personality traits. The results indicated that NSS were significantly associated with BP traits (model likelihood ratio ⫽ 26.55, P ⬍ 0.000). Sensory integration

Table III. Comparison of NSS between the BP-trait group and the control group.

Motor Coordination Sensory Integration Disinhibition Total neurological soft signs Left-side neurological soft signs Right-side neurological soft signs

BP-trait group (N ⫽ 89)

Control group (N ⫽ 89)

t value

P value

Cohen’s d value

0.45 ⫾ 1.14 1.29 ⫾ 1.71 0.22 ⫾ 0.54 1.97 ⫾ 2.57 0.94 ⫾ 1.33 0.75 ⫾ 1.26

0.34 ⫾ 0.93 0.46 ⫾ 0.91 0.02 ⫾ 0.15 0.82 ⫾ 1.50 0.39 ⫾ 0.75 0.38 ⫾ 0.82

0.72 4.06 3.42 3.63 3.41 2.32

0.472 0.000 0.001 0.000 0.001 0.022

– 0.61 0.51 0.55 0.51 0.35

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and disinhibition were positively associated with BP traits (Wald Z ⫽ 10.66, P ⫽ 0.001, and Wald Z ⫽ 5.52, P ⫽ 0.019, respectively). Discussion Previous studies have demonstrated that patients with BPD coincidentally have higher frequencies of neurological soft signs. However, whether NSS are associated with BP traits, needs to be examined. The association of NSS with BP traits can be more accurately determined if early onset and treatment-naïve adolescents are examined, and a study on adolescents also has the added benefit of reducing confounding factors of treatment or side effects of treatment on brain morphology, which increases the accuracy in evaluating abnormalities in the brain during the development of BPD. In this study, we first demonstrated that adolescents with BP traits exhibit more NSS than adolescents without BP traits. Our study implicates that neural abnormality is involved in early stage development of BPD. The present findings in adolescents with BP traits are similar to findings in BPD patients (De la Fuente et al. 2006; Gardner et al. 1987; Stein et al. 1993). In this study, NSS were found in both adolescents with BP traits and adolescents without BP traits, which suggests that NSS may be common in the general population. However, adolescents with BP traits had a significantly higher association with NSS when a cut- off of at least one or two positive NSS was applied. These findings in adolescents with BP traits are similar to findings in BPD patients (De la Fuente et al.2006). Also, among the individual soft signs, five soft signs exhibited significantly higher frequency in adolescents with BP traits (finger agnosia, left-right orientation, mirror movements, go/no-go test), and these findings were similar to a previous report on BPD patients, including abnormalities in right/left confusion, awkward gait, adventitious overflow, and difficulty hopping on one foot (Gardner et al. 1987). The finger agnosia and left-right orientation reflect impairments in sensory integration, such as tactile sensation or sensory perceptual difficulties, and the go/no-go test and mirror movements are mainly used to evaluate withholding or inhibition of associated movements. Therefore, the results we obtained suggest that certain types of NSS might have greater clinical significance than others in BP traits, even in BPD. Our studies revealed that NSS, particularly sensory integration and disinhibition, were significantly associated with BP traits. As the significant frequency of sensory integration soft signs may imply general cognitive impairment (Arango et al. 1999), and BPD is characterized by impulsivity and various cognitive impairments (Judd 2005), the results of this study indicate that BP traits and NSS may share the same neural substrates. Using magnetic resonance imaging (MRI), Chanen et al. (2008) revealed a reduction in volume of the gray matter at the right-side of the orbitofrontal cortex, in the firstpresentation of adolescents with BPD. Brunner et al. (2010) also reported a decline of gray matter volume in the dorsolateral cortex bilaterally, and in the left orbitofrontal cortex in adolescents with BPD. However, a study of healthy subjects, by Dazzan et al. (2006), demonstrated that NSS

are associated with the reduction of gray matter volume in the cortical areas (including the middle and superior temporal gyri, inferior frontal gyrus, and anterior cingulate). Therefore, it is very difficult to conclude that NSS reflect the existence of gray matter impairment in BPD (De la Fuente et al. 2006). Our study demonstrated that adolescents with BP traits have more left-side and right-side NSS than controls, while the study by Stein et al. (Stein et al. 1993) found that BPD patients have significantly higher prevalence of NSS on the left side, suggesting right hemisphere impairment. This inconsistency may be caused by the heterogeneity of the study samples. Stein et al. (Stein et al. 1993) recruited 28 BPD patients that met the DSM-III-R criteria, but onethird of the patients also had antisocial personality disorder, and not all the patients were free of treatment. The current study has several limitations. First, selfreporting measures were used to assess BP traits. Although the design of PDQ-4 ⫹ accurately fits the DSM-IV personality disorder criteria, and the BPD subscale of PDQ-4 ⫹ has been strongly recommended for brief screenings, more sophisticated methods, such as the semi-structured interview, may provide better assessments for a clinical diagnosis of BPD. Second, the present study only examined NSS in adolescents with BP traits, and further research examining NSS in adolescents with other personality traits (especially schizotypal and antisocial) is necessary to clarify whether NSS were more prevalent in adolescents with BP traits or prevalent in adolescents with any type of personality disorder traits. Conclusion In conclusion, the current study suggests that adolescents with BP traits have significantly more and severe NSS than adolescents without BP traits. Neural abnormality is involved in the early stage development of BPD. However, the current conclusions need further support from neuroimaging studies. Key points • • •

NSS were found in both adolescents with BP traits and adolescents without BP traits. Adolescents with BP traits have significantly more and severe NSS than adolescents without BP traits. Sensory integration and disinhibition were positively associated with BP traits.

Acknowledgments The authors would like to thank Wenbing Gao (Chinese Academy of Sciences), Wenqing Fu (Suzhou University), Yi Huang (Sichuan University), and Jianqun Fang (Ningxia Medical University), for their contribution towards participant recruitment in sites. Statement of interest None of the authors reports conflicts of interest. This study was supported by grants from the National Key Technologies R&D Program in the 11th 5-year plan of China (Grant No. 2009BAI77B02) and from the National Natural Science Foundation of China (Grant No. 81370034).

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Neurological soft signs in adolescents with borderline personality traits.

This study investigated the prevalence and severity of neurological soft signs (NSS), and their relationships with borderline personality (BP) traits ...
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