Epilepsy & Behavior 45 (2015) 225–228
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Reliability and validity of the Chinese version of the Neurological Disorders Depression Inventory for Epilepsy (C-NDDI-E) Yi Guo a, Zhe-Meng Chen b, Yin-Xi Zhang a, Ye-Bo Ge c, Chun-Hong Shen a, Yao Ding a, Shuang Wang a, Ye-Lei Tang a, Mei-Ping Ding a,⁎ a b c
Department of Neurology, Epilepsy Center, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China Department of Neurology, Jiaxing First Hospital, Jiaxing, China Department of Neurology, Ningbo Yinxian Hospital, Ningbo, China
a r t i c l e
i n f o
Article history: Received 7 November 2014 Revised 14 January 2015 Accepted 16 January 2015 Available online 29 March 2015 Keywords: Epilepsy Depression NDDI-E Screening tool Validity
a b s t r a c t Objective: The aim of this study was to evaluate the clinical reliability and validity of the Chinese version of the Neurological Disorders Depression Inventory for Epilepsy (C-NDDI-E). Methods: A total of 248 Chinese patients with epilepsy underwent psychometric tests, including the Chinese version of the Mini International Neuropsychiatric Interview (C-MINI), the Chinese version of the Beck Depression Inventory — II (C-BDI-II), and the C-NDDI-E. Results: None of the patients had difficulties understanding or completing the C-NDDI-E. Cronbach's α coefficient was 0.824. At a cutoff score of ≥ 14, the C-NDDI-E had a sensitivity of 0.854, a specificity of 0.899, a positive predictive value of 0.625, and a negative predictive value of 0.969. The scores for the C-NDDI-E were positively correlated with those for the C-BDI-II (P b 0.001). Conclusion: The C-NDDI-E is a reliable and valid screening tool for the detection of major depression in Chinese patients with epilepsy. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Depression is the most frequent psychiatric comorbidity in patients with epilepsy (PWE) [1]. It is associated with an increased seizure frequency, reduced tolerance to antiepileptic drugs (AEDs), worse response to pharmacologic and surgical treatments, and poorer quality of life [2,3]. Tellez-Zenteno et al. [4] reported that, in Canada, epilepsy was associated with an increased prevalence of depression compared with the general population (17.4% vs. 10.7%). The risk of suicide was 5–6 times higher in PWE than in the general population, and, in PWE, depression was considered as the main cause of suicidal ideation and suicide attempts [5,6]. The early diagnosis of depression and timely treatment will contribute to improvements in quality of life and reductions in the suicide rate of PWE. However, depression in PWE remains underrecognized and undertreated. One reason for this is that most depression scales cannot be used for routine screening in neurology or epilepsy clinics because they are time-consuming. In 2006, Gilliam et al. [7] developed a self-administered, 6-item screening instrument called the Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). This assessment tool can rapidly and accurately detect ⁎ Corresponding author at: Department of Neurology, Epilepsy Center, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China. Tel./fax: +86 571 87784750. E-mail address: [email protected] (M.-P. Ding).
http://dx.doi.org/10.1016/j.yebeh.2015.01.019 1525-5050/© 2015 Elsevier Inc. All rights reserved.
major depression in PWE. To date, validated versions of the NDDI-E have been made available in Brazil, Italy, Germany, Spain, Japan, Korea, Greece, Saudi Arabia, and Argentina [2,8–15]. The aims of the present study were to translate the English version of the NDDI-E into Chinese (C-NDDI-E) and to evaluate the clinical reliability and validity of this Chinese version. 2. Methods 2.1. Participants A total of 248 Chinese outpatients were recruited from the epilepsy clinics of the Second Affiliated Hospital, School of Medicine, Zhejiang University, China, between November 2012 and April 2013. All participants had been diagnosed by an experienced neurologist and met the diagnostic criteria for epilepsy defined by the International League Against Epilepsy (ILAE). The inclusion criteria were as follows: between 18–65 years of age; with a confirmed diagnosis according to the ILAE criteria; taking one or more AEDs with a stable drug dose for at least the previous 30 days; a graduate of primary school or over; with normal levels of general comprehension, reading comprehension, and communication ability; and capable of finishing the self-evaluation questionnaire. The exclusion criteria were as follows: suffering from severe neurological or psychiatric complications (e.g., dementia, delirium, aphasia, and other serious mental disorders); taking antidepressive
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Y. Guo et al. / Epilepsy & Behavior 45 (2015) 225–228
medications at the time of the study; unable to understand or finish the questionnaires; and refused to undertake all or part of the neuropsychological assessments. Each participant was evaluated within one day by a single neurologist who was familiar with the psychological assessment techniques. The C-MINI, C-NDDI-E, and C-BDI-II were completed in that sequence. The study protocol and informed consent were approved by the Hospital Ethics Committee, and all participants signed a written informed consent form prior to their inclusion. 2.2. Data collected
Table 1 A sample of the C-NDDI-E. NDDI-E中文版. The Chinese version of Neurological Disorders Depression Inventory for Epilepsy. 请根据您过去2周的情况, 圈出最合适的答案。 For the statements in the table, patients are asked to circle the number that best describes them over the past 2 weeks, including the day of the assessment.
Item
总是或经常有 Always or often
有时候 Sometimes
很少 Rarely
没有 Never
一切都是纠结
4
3
2
1
4
3
2
1
4
3
2
1
4
3
2
1
4
3
2
1
4
3
2
1
项目
Everything is a struggle 做什么都是错的
Nothing I do is right 有罪恶感
Patient details collected included sex, age, occupational status, marital status, duration of education, age at onset, course of epilepsy, type of seizures, seizure frequency, and the number of AEDs.
Feel guilty 我倒不如死了的好
I'd be better off dead 不顺心
Frustrated
2.3. Instruments 2.3.1. The Chinese version of the Mini International Neuropsychiatric Interview (C-MINI) The MINI is an internationally recognized brief and effective structured diagnostic interview for major psychiatric disorders as described by the DSM-IV and ICD-10, which has been proven to have high levels of reliability and validity [16]. In 2009, the MINI was translated into Chinese (C-MINI). An evaluation of the reliability and the validity of the C-MINI in patients with mental disorders showed that the tool had high levels of sensitivity and specificity for the diagnosis of major depressive episodes [17]. Only the major depression module of the C-MINI was administered in this study, which is considered to be the gold standard for the diagnosis of major depression. 2.3.2. The Chinese version of the Neurological Disorders Depression Inventory for Epilepsy (C-NDDI-E) The translation from the English to the Chinese version of the NDDI-E was performed using the Brislin technique [18]. The original English version was translated into Chinese by two authors (Y.G. and S.W.), and the translated version was then back-translated into English by two native Chinese-speaking bilingual translators who were not previously familiar with the NDDI-E. Finally, the two versions were compared by a native English speaker who concluded that they were identical. To check the understanding of the Chinese scale, we initially tested five patients with epilepsy, and all necessary changes were made to produce a revised version according to the feedback from these initial tests. The C-NDDI-E is a 6-item self-administered instrument with a total score that ranges from 6 to 24, which is used to assess depressive symptoms over the past 2 weeks. Each item is assigned a score of 1–4 (1 indicates ‘never’, while 4 indicates ‘always or often’). A sample of the C-NDDI-E is shown in Table 1. 2.3.3. The Chinese version of the Beck Depression Inventory — II (C-BDI-II) The BDI-II is a 21-item self-administered instrument, with each item assigned a score of 0–3 (3 indicates the most severe symptoms). This was designed to assess the severity of symptoms of depression for the past 2 weeks. The BDI-II is a reliable and well-validated measure for screening depression symptoms in adults, and the simplified Chinese version has become widely used in China [19]. The C-BDI-II was selected as an external validation criterion for this study. 2.4. Statistical analysis Statistical analysis was performed using SPSS software, version 16.0 (SPSS Inc., Chicago, IL, USA). A significance level of P b 0.05 (two-tailed) was adopted. Categorical variables between the group with major depression and the group without depression were compared using the chi-square test and Fisher's exact test, while continuous variables were compared using the nonparametric Mann–Whitney U test.
很难找到快乐
Difficulty finding pleasure
Logistic regression analysis was performed for multiple factor analysis. Cronbach's coefficient α and item–total (corrected item–total correlation) and interitem correlations (Spearman's ρ) were computed to ascertain the internal consistency of the C-NDDI-E. Receiver operating characteristic (ROC) analysis was performed to assess the utility of the C-NDDI-E global score to distinguish the diagnosis of major depression as defined by the C-MINI. The area under the curve (AUC) and its 95% confidence intervals (CIs) for the ROC curve were calculated. Nonparametric correlations (Spearman's ρ value) were calculated between the C-NDDI-E and the BDI-II. A further set of ROC analyses was carried out by using the BDI-II cutoff for depression as a criterion to split the groups (data are shown in the supplementary data). 3. Results A total of 248 PWE (129 males and 119 females) were included in this study. Using the C-MINI, we found that forty-one PWE had major depression and that 207 PWE had no depression. 3.1. Demographic and clinical characteristics of the PWE Demographic and clinical characteristics of the PWE are shown in Table 2; there were no significant differences between the group of PWE with major depression and the group of PWE without depression in terms of sex, age, marital status, occupational status, duration of education, seizure frequency, being seizure-free for the last 6 months, and the number of AEDs (P N 0.05). There were statistically significant differences in terms of age at onset, seizure duration, and presence of partial complex seizures between the two groups (P b 0.05). Further multivariate analysis showed that the age at onset of epilepsy and the disease course were not independent risk factors (P N 0.05), but complex partial seizure type was an independent risk factor for major depression coexisting with epilepsy (P b 0.05, Table 3). As shown in Table 2, the CNDDI-E and BDI-II scores were significantly higher in the group with major depression than in the group without depression (P b 0.05). 3.2. Evaluation of the C-NDDI-E The C-NDDI-E was easily understood by all patients, and each patient completed the test within 2 min. The Cronbach's α value for the C-NDDI-E was 0.824, which represents acceptable levels of internal consistency and reliability. As shown in Table 4, all C-NDDI-E items were significantly and positively associated with the total C-NDDI-E score, and none of these would have increased α if deleted. The ROC analysis of the C-NDDI-E is shown in Table 5 and in Fig. 1. The ROC analysis showed an AUC of 0.929 (95% CI: 0.895–0.964;
Y. Guo et al. / Epilepsy & Behavior 45 (2015) 225–228 Table 2 Demographic and clinical characteristics of the PWE.
Table 4 Corrected item–total correlations and Cronbach's α if the item is deleted from the C-NDDI-E.
Total (n = 248)
Gender Male Female Average age (years) Age at onset (years) Marital status Married Unmarried Divorced Occupational status In-service Unemployed Student Retired Others Duration of education (years) Seizure type Simple partial seizure Complex partial seizure Secondarily generalized seizure Tonic–clonic seizure Myoclonic seizure Course (years) Seizure frequency (time/month) Seizure-free for the last 6 months Number of AEDs Monotherapy Dual therapy Polytherapy (≥3 AEDs) NDDI-E BDI-II
With major depression (n = 41)
Without depression (n = 207)
19 22 30.5 ± 10.4 17.6 ± 9.6
110 97 31.1 ± 10.3 20.7 ± 10.4
17 22 2
112 89 6
23 10 2 4 2 10.6 ± 2.9
46 37 11 7 6 11.5 ± 3.1
6 15 21 7 1 12.9 ± 8.9 12.0 ± 23.4 8
20 43 135 32 0 10.3 ± 9.9 5.3 ± 13.4 53
23 11 7 16.0 ± 2.8 22.27 ± 8.6
116 63 28 9.4 ± 3.1 8.3 ± 7.2
P-value
0.426a
0.174b
0.116c 0.400a 0.029a 0.111a 0.795a 0.165a 0.030c 0.091c 0.511a 0.797a
b0.001c b0.001c
standard error: 0.017; P b 0.001). At a cutoff score of ≥14, the C-NDDI-E showed a sensitivity of 0.854, a specificity of 0.899, a positive predictive value (PPV) of 0.625, and a negative predictive value (NPV) of 0.969. The C-NDDI-E scores were significantly and positively correlated with those of the C-BDI-II (Spearman's ρ = 0.724, P b 0.001). 4. Discussion The results showed that the optimal cutoff score for the C-NDDI-E was ≥14. At this cutoff, the C-NDDI-E yielded a sensitivity of 0.853, a specificity of 0.899, a NPV of 0.968, and a PPV of 0.625, which were comparable with other versions of the NDDI-E [2,8–15]. These findings confirm the efficiency of the C-NDDI-E as a screening tool for major depressive episodes in PWE. At this cutoff, the AUC was 0.929, which indicated a high level of diagnostic accuracy compared with the gold standard, the C-MINI. Cronbach's α coefficient value of 0.824 was comparable with that in the original version (0.85), which indicates acceptable levels of internal consistency and reliability for the C-NDDI-E.
Table 3 Multiple factor analysis for risk factors for epilepsy coexistent with major depression. Regression coefficient
95% CI
SE
P-value
0.029 −0.011 −0.807
0.986–1.075 0.952–0.027 0.216–0.923
0.022 0.019 0.371
0.183 0.565 0.03
95% CI: 95% confidence interval; SE: standard error.
Item
Corrected item– total correlation
Cronbach's alpha if item is deleted
Everything is a struggle Nothing I do is right Feel guilty I'd be better off dead Frustrated Difficulty finding pleasure
0.650 0.615 0.474 0.513 0.666 0.649
0.783 0.792 0.819 0.812 0.780 0.785
0.694c 0.039c 0.311a
The C-MINI was used as the gold standard for the diagnosis of current major depression. Values are expressed as a number or the mean (SD). a Chi-square test. b Fisher's exact test. c Mann–Whitney U test.
Age at onset Course Complex partial seizure
227
Studies regarding the optimal cutoff scores for the NDDI-E have been inconsistent between different versions. The cutoff score of N15 has been applied for the English, Brazilian Portuguese, Greek, Arabic, and Argentinean Spanish versions [2,7,8,14,15]; ≥14 for the Italian, Spanish, and German versions [9–11]; N16 for the Japanese version [12]; and N11 for the Korean version [13]. Our optimal cutoff score was ≥14, which is consistent with that in the Italian, Spanish, and German versions. The differences between cutoff scores between other language versions of the NDDI-E may reflect differences in the study populations and culture. For example, the study sample in South Korea included 64% of male patients compared with only 52% of males in our sample. This alone could explain the lower cutoff score for the Korean version, as depressive symptoms in males are less obvious than in females. Furthermore, the Japanese have been described as reluctant to present with or admit to their depressive symptoms [12]. Therefore, only 7% of the Japanese patients were diagnosed with major depression using the MINI compared with 16.5% in our study, which contributed to the lower cutoff score compared with that in the Japanese version. The C-NDDI-E has high levels of construct validity according to its correlation with the C-BDI-II, which is the most widely used selfreporting scale for depression [19]. Compared with the C-BDI-II, the C-NDDI-E is a very convenient tool not only because of its brief completion time (b2 min in our study) but also because of its relative ease of scoring. In the setting of busy outpatient clinics, PWE are more willing to complete the C-NDDI-E, while patients may refuse to answer certain items (e.g., loss of interest in sex) in the C-BDI-II. In our study, the multivariate analysis showed that complex partial seizures are associated with the risk of major depression in epilepsy. As previous studies have reported, complex partial seizures are more likely to be associated with coexisting depression compared with tonic–clonic seizures [20,21]. However, this result is inconsistent with the findings from other populations [8,12,14], and further studies will need to be conducted to assess the risk factors for depression in Chinese PWE. Although the C-NDDI-E is a brief, self-administered, and valid screening instrument, it is not routinely used in the clinic. A survey by Shneker et al. in 2009 showed that only 38% of American neurologists used a screening instrument for depression in PWE, and, of this 38%, only 5% used the NDDI-E [22]. Therefore, it is very important to popularize the use of this validated C-NDDI-E in China. Based on our experiences, some strategies, such as training the epilepsy specialists and integrating the scale into the outpatient medical record system, are good ways to increase its utilization. The main limitation of our work was that the patient sample was collected from the epilepsy clinic of a tertiary care university hospital, which might have biased the study towards more severely affected patients. Hence, this study should provide the basis for the further assessment of the C-NDDI-E in wider health-care settings. Furthermore, the C-NDDI-E cannot be used to evaluate the severity of depression, and it can only be used as a screening tool. A C-NDDI-E score of ≥ 14 should trigger further diagnostic steps. In our study, the same rater carried out the C-MINI, C-NDDI-E, and C-BDI-II sequentially, and the rater was not aware of the results of the two self-reported assessments before carrying out the C-MINI; therefore, a rater bias is highly unlikely.
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Y. Guo et al. / Epilepsy & Behavior 45 (2015) 225–228
Table 5 ROC curve analysis and diagnostic efficiency statistical analysis of the C-NDDI-E for the diagnosis of current major depression based on the C-MINI. Cutoff score
NPV
PPV
Specificity
Sensitivity
Positive
Negative
AUC
SE
95% CI
P
≥13 ≥14 ≥15
0.977 0.968 0.954
0.513 0.625 0.653
0.830 0.899 0.918
0.902 0.853 0.780
56
192
0.929
0.017
0.895–0.964
b0.001
NPV: negative predictive value; PPV: positive predictive value; ROC: Receiver operating characteristic; AUC: area under the ROC curve; SE: standard error; 95% CI: 95% confidence interval.
However, we carried out an additional set of analyses using the C-BDI-II as a criterion for depression (scores b 20 vs. = 20), which produced results similar to those obtained using the C-MINI as a criterion for depression. In conclusion, the C-NDDI-E is a self-rating instrument with good levels of sensitivity and specificity and is recommended for routine use as a time-saving and efficient tool to recognize possible major depressive episodes in Chinese PWE.
Acknowledgments This work was supported by grants from the National Natural Science Foundation of China [grant numbers 81471316 and 81171227], the Traditional Chinese Medicine Program of Zhejiang Province [grant number 2010ZA069], and the Major Program of Zhejiang Province Science and Technology Foundation, China [grant number 2012C13018-4]. Conflict of interest statement The authors declare no conflict of interest.
Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.yebeh.2015.01.019.
Fig. 1. Receiver operating characteristic curve of the Chinese version of the NDDI-E.
References [1] Gaitatzis A, Trimble MR, Sander JW. The psychiatric comorbidity of epilepsy. Acta Neurol Scand 2004;110:207–20. [2] Thomson AE, Calle A, Fontela ME, Yepez L, Munoz GF, Jauregui A, et al. Screening of major depression in epilepsy: the Neurologic Depression Disorders Inventory in Epilepsy-Spanish version (Argentina). Epilepsia 2014;55:331–4. [3] Gilliam F, Hecimovic H, Sheline Y. Psychiatric comorbidity, health, and function in epilepsy. Epilepsy Behav 2003;4(Suppl. 4):S26–30. [4] Tellez-Zenteno JF, Patten SB, Jette N, Williams J, Wiebe S. Psychiatric comorbidity in epilepsy: a population-based analysis. Epilepsia 2007;48:2336–44. [5] Christensen J, Vestergaard M, Mortensen PB, Sidenius P, Agerbo E. Epilepsy and risk of suicide: a population-based case–control study. Lancet Neurol 2007;6:693–8. [6] Lim HW, Song HS, Hwang YH, Lee HW, Suh CK, Park SP, et al. Predictors of suicidal ideation in people with epilepsy living in Korea. J Clin Neurol 2010;6:81–8. [7] Gilliam FG, Barry JJ, Hermann BP, Meador KJ, Vahle V, Kanner AM. Rapid detection of major depression in epilepsy: a multicentre study. Lancet Neurol 2006;5:399–405. [8] de Oliveira GN, Kummer A, Salgado JV, Portela EJ, Sousa-Pereira SR, David AS, et al. Brazilian version of the Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). Epilepsy Behav 2010;19:328–31. [9] Mula M, Iudice A, La Neve A, Mazza M, Bartolini E, De Caro MF, et al. Validation of the Italian version of the Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). Epilepsy Behav 2012;24:329–31. [10] Metternich B, Wagner K, Buschmann F, Anger R, Schulze-Bonhage A. Validation of a German version of the Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). Epilepsy Behav 2012;25:485–8. [11] Di Capua D, Garcia-Garcia ME, Reig-Ferrer A, Fuentes-Ferrer M, Toledano R, Gil-Nagel A, et al. Validation of the Spanish version of the Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). Epilepsy Behav 2012;24:493–6. [12] Tadokoro Y, Oshima T, Fukuchi T, Kanner AM, Kanemoto K. Screening for major depressive episodes in Japanese patients with epilepsy: validation and translation of the Japanese version of Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). Epilepsy Behav 2012;25:18–22. [13] Ko PW, Hwang J, Lim HW, Park SP. Reliability and validity of the Korean version of the Neurological Disorders Depression Inventory for Epilepsy (K-NDDI-E). Epilepsy Behav 2012;25:539–42. [14] Zis P, Yfanti P, Siatouni A, Tavernarakis A, Gatzonis S. Validation of the Greek version of the Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). Epilepsy Behav 2013;29:513–5. [15] Alkhamees HA, Selai CE, Shorvon SD, Kanner AM. The use of the NDDI-E in Arabic to identify symptoms of depression of moderate or greater severity in people with epilepsy. Epilepsy Behav 2014;32:55–8. [16] Devinsky O, Barr WB, Vickrey BG, Berg AT, Bazil CW, Pacia SV, et al. Changes in depression and anxiety after resective surgery for epilepsy. Neurology 2005;65: 1744–9. [17] Si TM, Shu L, Dang WM, Su YA, Chen JX, Dong WT, et al. Evaluation of the reliability and validity of Chinese version of the Mini-International Neuropsychiatric Interview in patients with mental disorders. Chin Ment Health J 2009;23:493–7. [18] Cha ES, Kim KH, Erlen JA. Translation of scales in cross-cultural research: issues and techniques. J Adv Nurs 2007;58:386–95. [19] Wang Z, Yuan CM, Huang J, Li ZZ, Chen J, Zhang HY, et al. Reliability and validity of the Chinese version of Beck Depression Inventory-II among depression patients. Chin Ment Health J 2011;25:476–80. [20] Reisinger EL, DiIorio C. Individual, seizure-related, and psychosocial predictors of depressive symptoms among people with epilepsy over six months. Epilepsy Behav 2009;15:196–201. [21] Piazzini A, Canevini MP, Maggiori G, Canger R. Depression and anxiety in patients with epilepsy. Epilepsy Behav 2001;2:481–9. [22] Shneker BF, Cios JS, Elliott JO. Suicidality, depression screening, and antiepileptic drugs: reaction to the FDA alert. Neurology 2009;72:987–91.
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Reliability and validity of the Chinese version of the Neurological Disorders Depression Inventory for Epilepsy (C-NDDI-E) Yi Guo a, Zhe-Meng Chen b, Yin-Xi Zhang a, Ye-Bo Ge c, Chun-Hong Shen a, Yao Ding a, Shuang Wang a, Ye-Lei Tang a, Mei-Ping Ding a,⁎ a b c
Department of Neurology, Epilepsy Center, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China Department of Neurology, Jiaxing First Hospital, Jiaxing, China Department of Neurology, Ningbo Yinxian Hospital, Ningbo, China
a r t i c l e
i n f o
Article history: Received 7 November 2014 Revised 14 January 2015 Accepted 16 January 2015 Available online 29 March 2015 Keywords: Epilepsy Depression NDDI-E Screening tool Validity
a b s t r a c t Objective: The aim of this study was to evaluate the clinical reliability and validity of the Chinese version of the Neurological Disorders Depression Inventory for Epilepsy (C-NDDI-E). Methods: A total of 248 Chinese patients with epilepsy underwent psychometric tests, including the Chinese version of the Mini International Neuropsychiatric Interview (C-MINI), the Chinese version of the Beck Depression Inventory — II (C-BDI-II), and the C-NDDI-E. Results: None of the patients had difficulties understanding or completing the C-NDDI-E. Cronbach's α coefficient was 0.824. At a cutoff score of ≥ 14, the C-NDDI-E had a sensitivity of 0.854, a specificity of 0.899, a positive predictive value of 0.625, and a negative predictive value of 0.969. The scores for the C-NDDI-E were positively correlated with those for the C-BDI-II (P b 0.001). Conclusion: The C-NDDI-E is a reliable and valid screening tool for the detection of major depression in Chinese patients with epilepsy. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Depression is the most frequent psychiatric comorbidity in patients with epilepsy (PWE) [1]. It is associated with an increased seizure frequency, reduced tolerance to antiepileptic drugs (AEDs), worse response to pharmacologic and surgical treatments, and poorer quality of life [2,3]. Tellez-Zenteno et al. [4] reported that, in Canada, epilepsy was associated with an increased prevalence of depression compared with the general population (17.4% vs. 10.7%). The risk of suicide was 5–6 times higher in PWE than in the general population, and, in PWE, depression was considered as the main cause of suicidal ideation and suicide attempts [5,6]. The early diagnosis of depression and timely treatment will contribute to improvements in quality of life and reductions in the suicide rate of PWE. However, depression in PWE remains underrecognized and undertreated. One reason for this is that most depression scales cannot be used for routine screening in neurology or epilepsy clinics because they are time-consuming. In 2006, Gilliam et al. [7] developed a self-administered, 6-item screening instrument called the Neurological Disorders Depression Inventory for Epilepsy (NDDI-E). This assessment tool can rapidly and accurately detect ⁎ Corresponding author at: Department of Neurology, Epilepsy Center, Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China. Tel./fax: +86 571 87784750. E-mail address: [email protected] (M.-P. Ding).
http://dx.doi.org/10.1016/j.yebeh.2015.01.019 1525-5050/© 2015 Elsevier Inc. All rights reserved.
major depression in PWE. To date, validated versions of the NDDI-E have been made available in Brazil, Italy, Germany, Spain, Japan, Korea, Greece, Saudi Arabia, and Argentina [2,8–15]. The aims of the present study were to translate the English version of the NDDI-E into Chinese (C-NDDI-E) and to evaluate the clinical reliability and validity of this Chinese version. 2. Methods 2.1. Participants A total of 248 Chinese outpatients were recruited from the epilepsy clinics of the Second Affiliated Hospital, School of Medicine, Zhejiang University, China, between November 2012 and April 2013. All participants had been diagnosed by an experienced neurologist and met the diagnostic criteria for epilepsy defined by the International League Against Epilepsy (ILAE). The inclusion criteria were as follows: between 18–65 years of age; with a confirmed diagnosis according to the ILAE criteria; taking one or more AEDs with a stable drug dose for at least the previous 30 days; a graduate of primary school or over; with normal levels of general comprehension, reading comprehension, and communication ability; and capable of finishing the self-evaluation questionnaire. The exclusion criteria were as follows: suffering from severe neurological or psychiatric complications (e.g., dementia, delirium, aphasia, and other serious mental disorders); taking antidepressive
226
Y. Guo et al. / Epilepsy & Behavior 45 (2015) 225–228
medications at the time of the study; unable to understand or finish the questionnaires; and refused to undertake all or part of the neuropsychological assessments. Each participant was evaluated within one day by a single neurologist who was familiar with the psychological assessment techniques. The C-MINI, C-NDDI-E, and C-BDI-II were completed in that sequence. The study protocol and informed consent were approved by the Hospital Ethics Committee, and all participants signed a written informed consent form prior to their inclusion. 2.2. Data collected
Table 1 A sample of the C-NDDI-E. NDDI-E中文版. The Chinese version of Neurological Disorders Depression Inventory for Epilepsy. 请根据您过去2周的情况, 圈出最合适的答案。 For the statements in the table, patients are asked to circle the number that best describes them over the past 2 weeks, including the day of the assessment.
Item
总是或经常有 Always or often
有时候 Sometimes
很少 Rarely
没有 Never
一切都是纠结
4
3
2
1
4
3
2
1
4
3
2
1
4
3
2
1
4
3
2
1
4
3
2
1
项目
Everything is a struggle 做什么都是错的
Nothing I do is right 有罪恶感
Patient details collected included sex, age, occupational status, marital status, duration of education, age at onset, course of epilepsy, type of seizures, seizure frequency, and the number of AEDs.
Feel guilty 我倒不如死了的好
I'd be better off dead 不顺心
Frustrated
2.3. Instruments 2.3.1. The Chinese version of the Mini International Neuropsychiatric Interview (C-MINI) The MINI is an internationally recognized brief and effective structured diagnostic interview for major psychiatric disorders as described by the DSM-IV and ICD-10, which has been proven to have high levels of reliability and validity [16]. In 2009, the MINI was translated into Chinese (C-MINI). An evaluation of the reliability and the validity of the C-MINI in patients with mental disorders showed that the tool had high levels of sensitivity and specificity for the diagnosis of major depressive episodes [17]. Only the major depression module of the C-MINI was administered in this study, which is considered to be the gold standard for the diagnosis of major depression. 2.3.2. The Chinese version of the Neurological Disorders Depression Inventory for Epilepsy (C-NDDI-E) The translation from the English to the Chinese version of the NDDI-E was performed using the Brislin technique [18]. The original English version was translated into Chinese by two authors (Y.G. and S.W.), and the translated version was then back-translated into English by two native Chinese-speaking bilingual translators who were not previously familiar with the NDDI-E. Finally, the two versions were compared by a native English speaker who concluded that they were identical. To check the understanding of the Chinese scale, we initially tested five patients with epilepsy, and all necessary changes were made to produce a revised version according to the feedback from these initial tests. The C-NDDI-E is a 6-item self-administered instrument with a total score that ranges from 6 to 24, which is used to assess depressive symptoms over the past 2 weeks. Each item is assigned a score of 1–4 (1 indicates ‘never’, while 4 indicates ‘always or often’). A sample of the C-NDDI-E is shown in Table 1. 2.3.3. The Chinese version of the Beck Depression Inventory — II (C-BDI-II) The BDI-II is a 21-item self-administered instrument, with each item assigned a score of 0–3 (3 indicates the most severe symptoms). This was designed to assess the severity of symptoms of depression for the past 2 weeks. The BDI-II is a reliable and well-validated measure for screening depression symptoms in adults, and the simplified Chinese version has become widely used in China [19]. The C-BDI-II was selected as an external validation criterion for this study. 2.4. Statistical analysis Statistical analysis was performed using SPSS software, version 16.0 (SPSS Inc., Chicago, IL, USA). A significance level of P b 0.05 (two-tailed) was adopted. Categorical variables between the group with major depression and the group without depression were compared using the chi-square test and Fisher's exact test, while continuous variables were compared using the nonparametric Mann–Whitney U test.
很难找到快乐
Difficulty finding pleasure
Logistic regression analysis was performed for multiple factor analysis. Cronbach's coefficient α and item–total (corrected item–total correlation) and interitem correlations (Spearman's ρ) were computed to ascertain the internal consistency of the C-NDDI-E. Receiver operating characteristic (ROC) analysis was performed to assess the utility of the C-NDDI-E global score to distinguish the diagnosis of major depression as defined by the C-MINI. The area under the curve (AUC) and its 95% confidence intervals (CIs) for the ROC curve were calculated. Nonparametric correlations (Spearman's ρ value) were calculated between the C-NDDI-E and the BDI-II. A further set of ROC analyses was carried out by using the BDI-II cutoff for depression as a criterion to split the groups (data are shown in the supplementary data). 3. Results A total of 248 PWE (129 males and 119 females) were included in this study. Using the C-MINI, we found that forty-one PWE had major depression and that 207 PWE had no depression. 3.1. Demographic and clinical characteristics of the PWE Demographic and clinical characteristics of the PWE are shown in Table 2; there were no significant differences between the group of PWE with major depression and the group of PWE without depression in terms of sex, age, marital status, occupational status, duration of education, seizure frequency, being seizure-free for the last 6 months, and the number of AEDs (P N 0.05). There were statistically significant differences in terms of age at onset, seizure duration, and presence of partial complex seizures between the two groups (P b 0.05). Further multivariate analysis showed that the age at onset of epilepsy and the disease course were not independent risk factors (P N 0.05), but complex partial seizure type was an independent risk factor for major depression coexisting with epilepsy (P b 0.05, Table 3). As shown in Table 2, the CNDDI-E and BDI-II scores were significantly higher in the group with major depression than in the group without depression (P b 0.05). 3.2. Evaluation of the C-NDDI-E The C-NDDI-E was easily understood by all patients, and each patient completed the test within 2 min. The Cronbach's α value for the C-NDDI-E was 0.824, which represents acceptable levels of internal consistency and reliability. As shown in Table 4, all C-NDDI-E items were significantly and positively associated with the total C-NDDI-E score, and none of these would have increased α if deleted. The ROC analysis of the C-NDDI-E is shown in Table 5 and in Fig. 1. The ROC analysis showed an AUC of 0.929 (95% CI: 0.895–0.964;
Y. Guo et al. / Epilepsy & Behavior 45 (2015) 225–228 Table 2 Demographic and clinical characteristics of the PWE.
Table 4 Corrected item–total correlations and Cronbach's α if the item is deleted from the C-NDDI-E.
Total (n = 248)
Gender Male Female Average age (years) Age at onset (years) Marital status Married Unmarried Divorced Occupational status In-service Unemployed Student Retired Others Duration of education (years) Seizure type Simple partial seizure Complex partial seizure Secondarily generalized seizure Tonic–clonic seizure Myoclonic seizure Course (years) Seizure frequency (time/month) Seizure-free for the last 6 months Number of AEDs Monotherapy Dual therapy Polytherapy (≥3 AEDs) NDDI-E BDI-II
With major depression (n = 41)
Without depression (n = 207)
19 22 30.5 ± 10.4 17.6 ± 9.6
110 97 31.1 ± 10.3 20.7 ± 10.4
17 22 2
112 89 6
23 10 2 4 2 10.6 ± 2.9
46 37 11 7 6 11.5 ± 3.1
6 15 21 7 1 12.9 ± 8.9 12.0 ± 23.4 8
20 43 135 32 0 10.3 ± 9.9 5.3 ± 13.4 53
23 11 7 16.0 ± 2.8 22.27 ± 8.6
116 63 28 9.4 ± 3.1 8.3 ± 7.2
P-value
0.426a
0.174b
0.116c 0.400a 0.029a 0.111a 0.795a 0.165a 0.030c 0.091c 0.511a 0.797a
b0.001c b0.001c
standard error: 0.017; P b 0.001). At a cutoff score of ≥14, the C-NDDI-E showed a sensitivity of 0.854, a specificity of 0.899, a positive predictive value (PPV) of 0.625, and a negative predictive value (NPV) of 0.969. The C-NDDI-E scores were significantly and positively correlated with those of the C-BDI-II (Spearman's ρ = 0.724, P b 0.001). 4. Discussion The results showed that the optimal cutoff score for the C-NDDI-E was ≥14. At this cutoff, the C-NDDI-E yielded a sensitivity of 0.853, a specificity of 0.899, a NPV of 0.968, and a PPV of 0.625, which were comparable with other versions of the NDDI-E [2,8–15]. These findings confirm the efficiency of the C-NDDI-E as a screening tool for major depressive episodes in PWE. At this cutoff, the AUC was 0.929, which indicated a high level of diagnostic accuracy compared with the gold standard, the C-MINI. Cronbach's α coefficient value of 0.824 was comparable with that in the original version (0.85), which indicates acceptable levels of internal consistency and reliability for the C-NDDI-E.
Table 3 Multiple factor analysis for risk factors for epilepsy coexistent with major depression. Regression coefficient
95% CI
SE
P-value
0.029 −0.011 −0.807
0.986–1.075 0.952–0.027 0.216–0.923
0.022 0.019 0.371
0.183 0.565 0.03
95% CI: 95% confidence interval; SE: standard error.
Item
Corrected item– total correlation
Cronbach's alpha if item is deleted
Everything is a struggle Nothing I do is right Feel guilty I'd be better off dead Frustrated Difficulty finding pleasure
0.650 0.615 0.474 0.513 0.666 0.649
0.783 0.792 0.819 0.812 0.780 0.785
0.694c 0.039c 0.311a
The C-MINI was used as the gold standard for the diagnosis of current major depression. Values are expressed as a number or the mean (SD). a Chi-square test. b Fisher's exact test. c Mann–Whitney U test.
Age at onset Course Complex partial seizure
227
Studies regarding the optimal cutoff scores for the NDDI-E have been inconsistent between different versions. The cutoff score of N15 has been applied for the English, Brazilian Portuguese, Greek, Arabic, and Argentinean Spanish versions [2,7,8,14,15]; ≥14 for the Italian, Spanish, and German versions [9–11]; N16 for the Japanese version [12]; and N11 for the Korean version [13]. Our optimal cutoff score was ≥14, which is consistent with that in the Italian, Spanish, and German versions. The differences between cutoff scores between other language versions of the NDDI-E may reflect differences in the study populations and culture. For example, the study sample in South Korea included 64% of male patients compared with only 52% of males in our sample. This alone could explain the lower cutoff score for the Korean version, as depressive symptoms in males are less obvious than in females. Furthermore, the Japanese have been described as reluctant to present with or admit to their depressive symptoms [12]. Therefore, only 7% of the Japanese patients were diagnosed with major depression using the MINI compared with 16.5% in our study, which contributed to the lower cutoff score compared with that in the Japanese version. The C-NDDI-E has high levels of construct validity according to its correlation with the C-BDI-II, which is the most widely used selfreporting scale for depression [19]. Compared with the C-BDI-II, the C-NDDI-E is a very convenient tool not only because of its brief completion time (b2 min in our study) but also because of its relative ease of scoring. In the setting of busy outpatient clinics, PWE are more willing to complete the C-NDDI-E, while patients may refuse to answer certain items (e.g., loss of interest in sex) in the C-BDI-II. In our study, the multivariate analysis showed that complex partial seizures are associated with the risk of major depression in epilepsy. As previous studies have reported, complex partial seizures are more likely to be associated with coexisting depression compared with tonic–clonic seizures [20,21]. However, this result is inconsistent with the findings from other populations [8,12,14], and further studies will need to be conducted to assess the risk factors for depression in Chinese PWE. Although the C-NDDI-E is a brief, self-administered, and valid screening instrument, it is not routinely used in the clinic. A survey by Shneker et al. in 2009 showed that only 38% of American neurologists used a screening instrument for depression in PWE, and, of this 38%, only 5% used the NDDI-E [22]. Therefore, it is very important to popularize the use of this validated C-NDDI-E in China. Based on our experiences, some strategies, such as training the epilepsy specialists and integrating the scale into the outpatient medical record system, are good ways to increase its utilization. The main limitation of our work was that the patient sample was collected from the epilepsy clinic of a tertiary care university hospital, which might have biased the study towards more severely affected patients. Hence, this study should provide the basis for the further assessment of the C-NDDI-E in wider health-care settings. Furthermore, the C-NDDI-E cannot be used to evaluate the severity of depression, and it can only be used as a screening tool. A C-NDDI-E score of ≥ 14 should trigger further diagnostic steps. In our study, the same rater carried out the C-MINI, C-NDDI-E, and C-BDI-II sequentially, and the rater was not aware of the results of the two self-reported assessments before carrying out the C-MINI; therefore, a rater bias is highly unlikely.
228
Y. Guo et al. / Epilepsy & Behavior 45 (2015) 225–228
Table 5 ROC curve analysis and diagnostic efficiency statistical analysis of the C-NDDI-E for the diagnosis of current major depression based on the C-MINI. Cutoff score
NPV
PPV
Specificity
Sensitivity
Positive
Negative
AUC
SE
95% CI
P
≥13 ≥14 ≥15
0.977 0.968 0.954
0.513 0.625 0.653
0.830 0.899 0.918
0.902 0.853 0.780
56
192
0.929
0.017
0.895–0.964
b0.001
NPV: negative predictive value; PPV: positive predictive value; ROC: Receiver operating characteristic; AUC: area under the ROC curve; SE: standard error; 95% CI: 95% confidence interval.
However, we carried out an additional set of analyses using the C-BDI-II as a criterion for depression (scores b 20 vs. = 20), which produced results similar to those obtained using the C-MINI as a criterion for depression. In conclusion, the C-NDDI-E is a self-rating instrument with good levels of sensitivity and specificity and is recommended for routine use as a time-saving and efficient tool to recognize possible major depressive episodes in Chinese PWE.
Acknowledgments This work was supported by grants from the National Natural Science Foundation of China [grant numbers 81471316 and 81171227], the Traditional Chinese Medicine Program of Zhejiang Province [grant number 2010ZA069], and the Major Program of Zhejiang Province Science and Technology Foundation, China [grant number 2012C13018-4]. Conflict of interest statement The authors declare no conflict of interest.
Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.yebeh.2015.01.019.
Fig. 1. Receiver operating characteristic curve of the Chinese version of the NDDI-E.
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