Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: A single-center study

Dongfeng Liang; Xiangli Yu; Xiaojie Guo; Jie Zhang; Ronghuan Jiang

doi:10.1371/journal.pone.0282419

. 2023 Mar 16;18(3):e0282419. doi: 10.1371/journal.pone.0282419

Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: A single-center study

Dongfeng Liang ^1,^*,^#, Xiangli Yu ^2,^#, Xiaojie Guo ^3,^#, Jie Zhang ¹, Ronghuan Jiang ^3,^*

Editor: Fatih Özden⁴

PMCID: PMC10019621 PMID: 36928443

Abstract

Chronic pain affects more than 30% of the general population. The 9-item Central Sensitization Inventory (CSI-9) is a shortened version of the CSI-25, which is a patient-reported instrument used to screen people at risk of central sensitization (CS). The aim of this study was to cross-culturally adapt and validate a Chinese version of the CSI-9. The Chinese CSI-9 was generated by translation of the original English version, back-translation, cultural adaptation, and revision using the Delphi method. The Chinese CSI-9 was administered to 235 patients with chronic pain and 55 healthy controls. Structural validity (confirmatory factor analysis), construct validity (correlations with other scales), test-retest reliability (intraclass correlation coefficient, ICC), and internal consistency (Cronbach’s α) were evaluated. Confirmatory factor analysis was performed using one factor. The Chinese CSI-9 score was positively correlated with the Pain Catastrophic Scale (PCS) total score (r = 0.463), PCS subscale scores (r = 0.347–0.463), Brief Pain Inventory (BPI) mean item score (r = 0.524), BPI total score (r = 0.773), and the number of painful sites (r = 0.451). The Chinese CSI-9 had excellent test-retest reliability (ICC = 0.958) and excellent internal consistency (Cronbach’s α = 0.902 in the overall sample and 0.828 in the chronic pain population). The optimal cut-off value for the Chinese CSI-9 was 18 points. The Chinese CSI-9 had excellent test-retest reliability and satisfactory structural validity and construct validity. The CSI-9 could potentially be utilized in China as a self-report questionnaire in both clinical practice and research settings.

Introduction

Up to 30% of people are affected by chronic pain [1, 2], which can be caused by musculoskeletal disorders (e.g., low back pain or neck pain and osteoarthritis), fibromyalgia, headache, temporomandibular joint disorder (TMD), and irritable bowel syndrome (IBS) [3]. Chronic pain negatively affects the quality of life and is associated with reduced mobility, psychological distress, sleep disturbance, and an economic burden [4]. In China, since chronic pain does not threaten the life of the patients, it is often overlooked, leading to low diagnosis rates, low treatment rates, insufficient pain control, poor management of pain, and neglect of pain management [2, 5].

The pathophysiologic mechanisms of many chronic pain syndromes are thought to involve central sensitization (CS) [6], which develops when nociceptor inputs increase the excitability of neurons in central nociceptive pathways [7]. CS generally manifests as allodynia (perceiving pain in response to a stimulus that does not normally induce pain), hyperalgesia (an elevated sensitivity to a normally painful stimulus), and aftersensations following cessation of the pain stimulus [7].

CS may be assessed through quantitative sensory testing, which evaluates the responses to thermal and mechanical stimuli [8]. Simpler methods of assessing CS include questionnaires such as the Central Sensitization Inventory (CSI), which is a patient-reported instrument designed to screen populations at risk of CS or to assess physical and emotional symptoms associated with CS [9]. The 25-item CSI (CSI-25) consists of two sections: part A rates the frequency of occurrence of 25 common symptoms of CS using a 5-point Likert scale (never, rarely, sometimes, often, or always), while part B is not scored but is used to report the previous diagnosis of 10 diseases related to central sensitivity syndrome (CSS). The CSI-25 has been shown to distinguish between patients with chronic pain and controls. However, the availability of a shorter form of the CSI would reduce the burden on the patient and thereby facilitate the screening of CS in both clinical and research settings.

In 2018, Nishigami et al. used successive Rasch analyses to simplify the CSI-25 into a 9-item CSI (CSI-9) [10]. The CSI-9 rates the frequency of occurrence of nine common symptoms of CS using a 5-point Likert scale (never, rarely, sometimes, often, or always), with a higher score indicating more severe CS. The CSI-9 was shown to have acceptable psychometric properties [10]. The main advantage of the CSI-9 is its practicality in clinical practice since it involves only nine items and is fast and easy to use. Furthermore, an optimal cut-off value of 20 points was shown to distinguish patients with fibromyalgia from those with musculoskeletal pain, while an optimal cut-off value of 17 points was demonstrated to distinguish patients with fibromyalgia from a healthy population of research subjects [11]. The above study suggested that a CSI-9 score of >20 could be used to screen for CS and help physicians identify patients who need targeted treatment. Research has shown that pain can be influenced by culture and that there are variations in pain beliefs, pain assessments, pain treatment strategies, and catastrophic pain scores between different countries and different languages [12–14]. Cultural differences can lead to bias, so it is essential to adopt a Chinese version for the application of CSI-9 in China. With the convenience of CSI-9 in clinical use, a Chinese CSI-9 would definitely improve the current situation in China. Still, no studies have described the translation and cross-cultural adaptation of the CSI-9 into Chinese, but a recent study reported a Chinese version of the CSI-25 [15].

The aim of this single-center study was to cross-culturally adapt the CSI-9 to Chinese and assess its psychometric characteristics (including internal consistency, test-retest reliability, construct validity, and factor structure) in patients with chronic pain. It was anticipated that the Chinese version of the CSI-9 would provide clinicians and researchers with a new instrument for the evaluation of chronic pain and CS.

Methods

Study participants

This single-center, cross-sectional study enrolled patients with chronic pain who attended the outpatient department or were admitted to the ward of the Rheumatology and Immunology Department, the First Medical Center, the Chinese People’s Liberation Army General Hospital. A group of healthy controls was recruited from the physical examination center of the First Medical Center, the Chinese People’s Liberation Army General Hospital, during the same period. The physical examination center, a department localized inside the hospital, offers routine regular physical examinations for ordinary people. The Ethics Committee of the Chinese People’s Liberation Army General Hospital approved this study (No. S2021-285-02), and all participants provided written consent.

The inclusion criteria for the patients with chronic pain were: (1) male or female aged >18 years old; (2) diagnosed with chronic pain (the presence of pain for ≥3 months), including fibromyalgia or musculoskeletal pain (e.g., lumbago, cervicodynia, hip pain, knee pain, ankle pain, shoulder pain, elbow pain, hand and wrist pain, lateral epicondylalgia, and temporomandibular joint pain); (3) pain severity, scored on the Numeric Rating Scale (NRS) of 0–10, was ≥3 points for the majority of time during the previous 1 week; and (4) pain symptoms and treatment regimen had been stable for >1 month. The inclusion criteria for the healthy controls were: (1) male or female aged >18 years old; (2) not diagnosed with CS or chronic pain during the previous 5 years; and (3) no long-term pain complaints. Patients with chronic pain were excluded from the analysis if any of the following criteria were met: (1) history of trauma or fracture during the previous 6 weeks; (2) acute disease (e.g., acute infection) during the previous 4 weeks; (3) cancer; (4) brain or spinal cord injury; (5) neurologic disease; (6) serious underlying disease (such as severe cardiopulmonary, gastrointestinal or genitourinary disease) that might affect the scoring of the scale; and (7) mental illness or severe emotional disorder. Additional exclusion criteria for both groups were: (1) the participant had difficulty interpreting Chinese or had a reading disorder; (2) in the opinion of the researchers, the participant would not be able to fully cooperate with the study protocol (including completion of the questionnaires) or had difficulty communicating; (3) the participant did not fill in all the items in the CSI-9 scale; (4) the participant consistently chose a particular option or exhibited clear regularity in the selection of answers; and (5) the participant failed to answer the questions in accordance with the instructions or provided unrelated answers.

Study design

The study was divided into two parts. First, the original CSI-9 was translated, back-translated, and cross-culturally adapted using the Brislin bidirectional translation method [16]. Second, the sociodemographic data of patients and healthy controls were collected, and the participants were asked to fill in the Chinese CSI-9, Brief Pain Inventory (BPI), and Pain Catastrophic Scale (PCS) on site.

Development of the Chinese CSI-9

The study researchers contacted the author of the original CSI-9, Katsuyoshi Tanaka, by email in May 2021 and were given permission to develop a Chinese version of the scale. The process of translation, back-translation, and cross-cultural adaptation was carried out in strict accordance with established guidelines to ensure maximum equivalence between the Chinese version of the CSI-9 and the original instrument [16]. Seven experts in fibromyalgia, pain, and the psychology of pain (all working in pain or rheumatology & immunology departments) participated in the Delphi consultation on the Chinese version. With regard to the translation process, the implementation process was as follows. A preliminary Chinese version of the scale was generated by translating and back-translating the original CSI-9 using the Brislin bidirectional translation method. First, two experts (LD and ZG) and a Chinese professional translator (Shanghai Richard Translation Co.) translated the scale from English to Chinese, and the researchers integrated it into the original Chinese version. Then, a professional translator of Chinese nationality and a professional English native-speaking translator (Shanghai Richard Translation Co.) back-translated the original Chinese version of the scale, namely, Chinese to English. After that, the researchers combined the results of the English-to-Chinese translation and Chinese-to-English translation to form the first Chinese version of the scale again. Finally, the first Chinese version of the scale was tested by doctors and patients, and the translated items were modified again according to the test results to obtain the final version of the Chinese CSI-9.

Six patients with chronic pain who had different ages, genders, and education levels were asked to provide feedback on version B of the Chinese CSI-9 as part of a pilot test. The respondents gave their opinions on the comprehensibility and accuracy of the questions and answers and provided an overall evaluation of the questionnaire. Additionally, the response time and response rate were recorded. Next, a group of seven experts in the diagnosis and treatment of chronic pain and six patients used the Delphi method [17] to revise and optimize the wording and structure of the items in the scale after taking into account the opinions and feedback of the patients, thereby generating the final version of the Chinese CSI-9.

The final version of the Chinese CSI-9 comprised two parts. Part A contained 9 items, each of which was scored using a 5-point Likert scale with “0” for “never” and “4” for “always”. The total score of part A ranged from 0 to 36, and a higher score indicated more severe CS. Severity was divided into three grades: subclinical (0–9 points), mild (10–19 points), and moderate/severe (≥20 points) [10]. Part B was not scored but was used to obtain information regarding a history of CS-related diseases, including restless leg syndrome (RLS), chronic fatigue syndrome (CFS), fibromyalgia, TMD, migraine or TTH, IBS, multiple chemical sensitivity (MCS), neck injury (including whiplash injury), anxiety or panic attacks, and depression.

Data collection

All participants were asked to fill in paper versions of the Chinese CSI-9 and two comparator scales (the Chinese versions of the BPI [18] and PCS [19] scales) on-site. The comparator scales were used to investigate the construct validity of the Chinese CSI-9. The Chinese BPI assesses the characteristics of pain, such as intensity, location, and duration. The Chinese PCS contains 13 items graded on a 5-point Likert scale (“0” for “never” and “4” for “always”), and its total score ranges from 0 to 52, with a higher score indicative of more catastrophic pain. Sociodemographic data were also obtained for all the participants.

Validity assessment

Confirmatory factor analysis was used to assess structural validity by evaluating the similarity of the dimensions and factor loadings between the Chinese CSI-9 and the original CSI-9. The indices used to determine the model fit were: chi-square/degrees of freedom (χ²/df), goodness-of-fit index (GFI), adjusted goodness-of-fit index (AGFI), comparative fit index (CFI), Tucker-Lewis Coefficient (TLI) and root mean square error of approximation (RMSEA). A model with χ²/df<3, RMSEA<0.08, GFI>0.90, CFI>0.90, and TLI>0.90 suggested a good fit [20].

Construct validity was assessed by examining the correlations between the Chinese CSI-9 score and the Chinese PCS total score, Chinese PCS subscale scores (rumination, magnification, and helplessness), Chinese BPI total score, Chinese BPI mean item score, pain duration, and the number of body locations experiencing pain. Each correlation was measured by determining Spearman’s rank correlation coefficient (r).

Criterion validity was explored by comparing the Chinese CSI-9 part A score between patients with/without each CSS-related diagnosis in part B and between patients with/without one CSS-related diagnosis, two CSS-related diagnoses, and more than three CSS-related diagnoses according to part B. Discriminatory analysis was also used to compare the differences in each item between patients with chronic pain and healthy controls. The criteria for interpreting model fit and magnitude of correlations in convergent validity were specified in advance.

Reliability assessment

Cronbach’s α coefficient was used to evaluate internal consistency [21]. In this study, reliability was poor for 0.5 ≤ Cronbach’s α < 0.6, acceptable for 0.6 ≤ Cronbach’s α < 0.7, good for 0.7 ≤ Cronbach’s α < 0.9, and excellent for Cronbach’s α ≥ 0.9.

Test-retest reliability was used to assess the stability of the CSI-9. When tested for the first time, all subjects were confirmed by randomization whether to be tested for the second time at 7 ± 1 days after the first test. Those who were retested were required to maintain a stable therapeutic regimen (i.e., no changes in drugs and dosages) between the first and second tests. The intraclass correlation coefficient (ICC) was calculated by a two-way random-effects model; an absolute agreement was used, and test-retest reliability was classified as moderate for 0.50 ≤ ICC < 0.75, good for 0.75 ≤ ICC < 0.90, and excellent for ICC ≥ 0.90 [22].

Measurement error

Bland-Altman plots were generated to determine the mean differences and visualize systematic errors in the baseline.

Floor and ceiling effects

Floor and ceiling effects were considered to be present if ≥15% of the patients reported the lowest (0) or highest (100) possible CSI score [23].

Exploratory analysis of the utility of the Chinese CSI-9 as a screening tool for CS

Receiver operating characteristic (ROC) curve analyses were used to evaluate whether the Chinese CSI-9 might have utility as a screening tool for CS. Optimal cut-off values for the CSI-9 score were determined according to the Youden index. The area under the ROC curve (AUC) and its 95% confidence interval (95%CI), sensitivity, specificity, positive predictive value (PPV), negative predictive value (PPV), and accuracy were calculated.

Statistical analysis

The sample size calculation was based on CFA, as designed in the protocol, and including at least 200 patients would meet the needs for validation, and 50 would be sufficient for retest reliability. The analyses were performed using SPSS 22.0 and AMOS 23.0 (IBM, Armonk, NY, USA), and the Bland-Altman plots were drawn using MedCalc 19.6.1 (MedCalc Software, Ostend, Belgium). All statistical tests were two-sided, and P < 0.05 was considered statistically significant. Continuous variables conforming to a normal distribution are shown as the mean ± standard deviation, and those not conforming to a normal distribution are expressed as the median (interquartile range). Categorical variables are expressed as the number of cases (percentage). Continuous variables conforming to a normal or approximately normal distribution were compared between two groups using the t-test for independent samples and among multiple groups using one-way analysis of variance (ANOVA). Non-normally distributed continuous variables were compared between groups using the Mann-Whitney U test (two groups) or the Kruskal-Wallis test (multiple groups). The chi-squared test or Fisher’s exact test was used to analyze categorical data.

Results

Cross-cultural adaptation of the CSI-9 into Chinese

The CSI was forward-translated into Chinese and backward-translated into English without difficulty. The patients in the pilot test indicated that the Chinese CSI-9 was straightforward to understand, so no further changes were made to the scale.

Baseline characteristics of the study participants

A total of 308 participants were screened for inclusion in the study. Two participants were excluded for repeated entry of information, eleven were excluded for failing to follow the instructions on the questionnaires or failing to complete the questionnaires accurately/fully, and five were excluded because the pain had been present for less than 3 months. Therefore, 290 participants were included in the final analysis.

The baseline characteristics of the study participants are presented in Table 1. The study population included 235 patients with chronic pain (114 cases of fibromyalgia and 121 cases of musculoskeletal pain) and 55 healthy controls. There were significant differences between groups in age, gender, body mass index (BMI), and employment status (P < 0.05) but not weight, height, marital status, or years of education (Table 1). Furthermore, the pain severity score, PCS score, PCS subscale scores, CSI-9 score, and CSI severity score were all markedly higher in patients with chronic pain than in healthy controls (P < 0.001; Table 1).

Table 1. Baseline data.

Variable	Overall sample	Fibromyalgia	Musculoskeletal pain (n	Healthy controls	P
Variable	(n = 290)	(n = 114)	(n = 121)	(n = 55)	P
Age (years)	44.0 ± 12.7	41.6 ± 12.0	46.0 ± 13.9	44.8 ± 10.3	0.026
Gender					0.021
Male	68 (23.4%)	17 (14.9%)	36 (29.8%)	15 (27.3%)
Female	222 (76.6%)	97 (85.1%)	85 (70.2%)	40 (72.7%)
Weight (kg)	62.9 ± 10.5	61.5 ± 10.0	63.1 ± 10.8	65.5 ± 10.7	0.066
Height (cm)	163.6 ± 7.4	163.3 ± 7.1	164.6 ± 7.7	162.3 ± 7.0	0.139
BMI (kg/m ² )	23.5 ± 3.4	23.0 ± 3.3	23.3 ± 3.2	24.8 ± 3.5	0.006
Marital status					0.849
Married	243 (83.8%)	94 (82.5%)	102 (84.3%)	47 (85.5%)
Single	32 (11.0%)	15 (13.2%)	11 (8.9%)	6 (10.9%)
Divorced	10 (3.4%)	3 (2.6%)	5 (4.1%)	2 (3.6%)
Widowed	5 (1.7%)	2 (1.8%)	3 (2.4%)	0
Education level (years)	11.7 ± 4.1	12.3 ± 4.0	11.5 ± 4.4	11.0 ± 3.2	0.090
Employment status					<0.001
Unemployed	91 (31.2%)	42 (36.8%)	40 (32.5%)	9 (16.4%)
Employed	148 (51.0%)	49 (43.0%)	56 (46.3%)	43 (78.2%)
Retired	44 (15.2%)	18 (15.8%)	24 (19.8%)	2 (3.6%)
Student	7 (2.4%)	5 (4.4%)	1 (0.8%)	1 (1.8%)
BPI score	42.3 ± 27.0	58.8 ± 18.6	45.6 ± 19.1	0.4 ± 1.7	<0.001
Pain duration (months)	2042.4 ± 2697.4	1970.4 ± 2786.6	2110.2 ± 2620.3	0.0 ± 0.0	0.693
Location of pain
Head	81 (27.9%)	56 (49.1%)	24 (19.8%)	1 (1.8%)	<0.001
Neck	135 (46.6%)	79 (69.3%)	55 (45.5%)	1 (1.8%)	<0.001
Chest	49 (16.9%)	37 (32.5%)	12 (9.9%)	0	<0.001
Back	147 (50.7%)	85 (74.6%)	62 (51.2%)	0	<0.001
Abdomen	35 (12.1%)	30 (26.3%)	5 (4.1%)	0	<0.001
Waist	151 (52.1%)	79 (69.3%)	71 (58.7%)	1 (1.8%)	<0.001
Hip	107 (36.9%)	70 (61.4%)	37 (30.6%)	0	<0.001
Left shoulder	122 (42.1%)	78 (68.4%)	44 (36.4%)	0	<0.001
Left upper arm	83 (28.6%)	61 (53.5%)	22 (18.2%)	0	<0.001
Left elbow	69 (23.8%)	51 (44.7%)	18 (14.9%)	0	<0.001
Left forearm	57 (19.7%)	43 (37.7%)	14 (11.6%)	0	<0.001
Left palm	70 (24.1%)	43 (37.7%)	27 (22.3%)	0	<0.001
Left thigh	73 (25.2%)	52 (45.6%)	21 (17.4%)	0	<0.001
Left knee	118 (40.7%)	69 (60.5%)	49 (40.5%)	0	<0.001
Left lower leg	68 (23.4%)	53 (46.5%)	13 (10.7%)	2 (3.6%)	<0.001
Left foot	78 (26.9%)	55 (48.2%)	23 (19.0%)	0	<0.001
Right shoulder	123 (42.4%)	78 (68.4%)	45 (37.2%)	0	<0.001
Right upper arm	82 (28.3%)	63 (55.3%)	19 (15.7%)	0	<0.001
Right elbow	72 (24.8%)	56 (49.1%)	16 (13.2%)	0	<0.001
Right forearm	65 (22.4%)	51 (44.7%)	14 (11.6%)	0	<0.001
Right palm	74 (25.5%)	41 (36.0%)	32 (26.4%)	1 (1.8%)	<0.001
Right thigh	79 (27.2%)	58 (50.9%)	21 (17.4%)	0	<0.001
Right knee	129 (44.5%)	73 (64.0%)	56 (46.3%)	0	<0.001
Right lower leg	72 (24.8%)	59 (51.8%)	13 (10.7%)	0	<0.001
Right foot	80 (27.6%)	54 (47.4%)	26 (21.5%)	0	<0.001
PCS score	24.7 ± 14.40	32.86 ± 9.93	25.60 ± 12.50	5.85 ± 7.18	<0.001
PCS subscale scores
Rumination	9.0 ± 4.8	11.3 ± 3.5	9.7 ± 4.1	2.8 ± 3.3	<0.001
Magnification	5.2 ± 3.5	6.9 ± 2.6	5.4 ± 3.3	1.1 ± 1.5	<0.001
Helplessness	10.7 ± 7.0	14.7 ± 5.2	10.8 ± 6.2	2.2 ± 3.3	<0.001
CSI score	18.0 ± 9.0	25.2 ± 5.3	17.0 ± 6.2	5.1 ± 3.7	<0.001
CSI severity					<0.001
Subclinical (0 to 9)	62 (21.4%)	0 (0.0%)	15 (12.4%)	47 (85.5%)
Mild (10 to 19)	87 (30.0%)	14 (12.3%)	65 (53.7%)	8 (14.5%)
Moderate/severe (≥20)	141 (48.6%)	100 (87.7%)	41 (33.9%)	0 (0.0%)
Number of diagnoses in CSI part B	0.9 ± 1.1	1.8 ± 1.1	0.6 ± 0.9	0.0±0.0

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Structural validity

Table 2 summarizes the results of the structural validity evaluation (Table 2). The model fit indices were χ² = 97.608, df = 27, χ²/df = 3.615, TLI = 0.927, CFI = 0.945, RMSEA = 0.095, GFI = 0.929, AGFI = 0.882. The result of the correlations met the pre-specified criteria for convergent and divergent validities of the Chinese CSI-9 with those variables.

Table 2. Structural validity of the Chinese central sensitization inventory.

No.	Item	Mean ± SD	Factor 1
1	Unrefreshed in morning	2.2 ± 1.3	0.692
2	Muscles stiff/achy	2.5 ± 1.4	0.773
3	Pain all over body	2.2 ± 1.5	0.865
4	Headaches	1.3 ± 1.2	0.567
5	Do not sleep well	2.1 ± 1.4	0.711
6	Difficulty concentrating	1.6 ± 1.3	0.712
7	Stress makes symptoms worse	1.5 ± 1.3	0.692
8	Tension neck and shoulder	2.3 ± 1.4	0.752
9	Poor memory	2.1 ± 1.3	0.623

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Construct validity

As shown in Table 3, the calculation of the Pearson correlation coefficient demonstrated that the CSI-9 score was positively correlated with the PCS total score (r = 0.463), PCS rumination, magnification, and helplessness subscale scores (r = 0.347–0.463), BPI mean item score (r = 0.524), BPI total score (r = 0.773), and the number of painful body sites (r = 0.451). However, the CSI-9 score was not correlated with the duration of pain (Table 3).

Table 3. Construct validity in the overall sample (n = 290).

Scale	Construct validity	r	95% CI
CSI	PCS	0.463	0.354, 0.557
	Rumination subscale of PCS	0.347	0.225, 0.467
	Magnification subscale of PCS	0.386	0.275, 0.492
	Helplessness subscale of PCS	0.463	0.361, 0.568
	BPI mean item score	0.524	0.421, 0.616
	BPI total score	0.773	0.416, 0.620
	Duration of pain	-0.003	-0.133, 0.126
	Number of sites of pain	0.451	0.353, 0.547

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BPI: Brief Pain Inventory; CI: confidence interval; CSI: Central Sensitization Inventory; PCS: Pain Catastrophic Scale; r: Pearson correlation coefficient.

Test-retest reliability

Among 117 patients with chronic pain who completed the CSI-9 on two separate occasions, three were excluded because the interval between the two tests was less than 6 days, three were excluded because the questionnaires were incomplete or clearly contained errors, and two were excluded because they had suffered from chronic pain for <90 days. Therefore, 109 patients were included in the assessment of test-retest reliability. The test-retest reliability (two-way random-effects model) of the CSI-9 total score (Table 4) was excellent in the overall sample (ICC = 0.958) and was good in the chronic pain group (ICC = 0.875) and healthy control group (ICC = 0.807). Furthermore, the test-retest reliability was good-to-excellent (ICC ≥ 0.75) for all of the items in the overall sample, 6 of the 9 items in the chronic pain group, but only 2 of the 9 items in the healthy control group (Table 4).

Table 4. Test-retest reliability (two-way random-effects model).

		Overall sample		Chronic pain		Healthy controls
		(n = 109)		(n = 58)		(n = 51)
No.	Items	ICC	95% CI	ICC	95% CI	ICC	95% CI
1	Unrefreshed in morning	0.798	0.718, 0.857	0.678	0.510, 0.796	0.639	0.445, 0.776
2	Muscles stiff/achy	0.939	0.912, 0.958	0.705	0.547, 0.814	0.807	0.684, 0.885
3	Pain all over body	0.924	0.891, 0.947	0.803	0.688, 0.879	0.563	0.343, 0.725
4	Headaches	0.815	0.741, 0.870	0.797	0.679, 0.874	0.422	0.168, 0.624
5	Do not sleep well	0.837	0.771, 0.886	0.842	0.747, 0.903	0.479	0.235, 0.666
6	Difficulty concentrating	0.851	0.789, 0.895	0.804	0.690, 0.879	0.717	0.552, 0.828
7	Stress makes symptoms worse	0.813	0.738, 0.868	0.739	0.596, 0.837	0.633	0.434, 0.773
8	Tension neck and shoulder	0.884	0.834, 0.920	0.805	0.692, 0.879	0.710	0.541, 0.823
9	Poor memory	0.866	0.810, 0.906	0.865	0.783, 0.918	0.609	0.404, 0.756
All	Total score	0.958	0.939, 0.971	0.875	0.798, 0.924	0.807	0.684, 0.885

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ICC, intraclass correlation coefficient; CI, confidence interval.

The ICC values shown for each item resulted from the remaining items after the deletion of that item.

CSS-related disorders

The CSS-related disorders reported by the patients in part B of the CSI-9 are shown in the S1 Table. The average number of diagnoses for patients with chronic pain was 1.17 ± 1.14, and the proportion of patients reporting 1, 2, and ≥3 CSS-related syndromes was 38.3%, 16.6%, and 13.2%, respectively. The most common CSS-related disorders reported by the patients with chronic pain were fibromyalgia (51.5%), anxiety/panic attacks (20.9%), migraine/tension-type headache (TTH) (17.0%), and depression (12.8%). The remaining six CSS-related syndromes were each reported by less than 5% of the patients with chronic pain. None of the healthy controls reported any CSS-related disorders.

Measurement error

Bland-Altman plots revealed that the mean differences for the overall sample and patients with chronic pain were not significantly different from zero, and no systematic bias was detected (Fig 1).

Fig 1 — A. Overall sample. B: Patients with chronic pain. The mean differences for the overall sample and chronic pain group did not significantly differ from zero, and no systematic bias was detected.

Criterion validity

Table 5 shows that the CSI-9 score was significantly higher in patients with at least one CSS-related diagnosis in part B of the instrument (P < 0.001 vs. no CSS-related diagnoses), patients with at least two CSS-related diagnoses (P < 0.001 vs. ≤1 CSS-related diagnosis) and patients with at least 3 CSS-related diagnoses (P < 0.001 vs. ≤2 CSS-related diagnoses). When the items in part B were analyzed individually, the CSI-9 score was significantly higher in patients who had fibromyalgia (P < 0.001), migraine/TTH (P < 0.001), IBS (P = 0.040), neck injury (P = 0.021), anxiety/panic attacks (P < 0.001) or depression (P < 0.001) when compared with patients who did not report these CSS-related disorders (Table 5). The CSI-9 score did not differ significantly between patients with/without TMD, RLS, CFS, or MCS (Table 5).

Table 5. Criterion validity in the overall sample (n = 290).

No.	CSS diagnosis (CSI part B)	Presence of symptom	n (%)	CSI part A score (mean ± SD)	P
1	Restless leg syndrome	Yes	4 (1.4%)	22.3 ± 7.5	0.278
		No	286 (98.6%)	17.9 ± 9.1
2	Chronic fatigue syndrome	Yes	2 (0.7%)	21.5 ± 6.4	0.603
		No	288 (99.3%)	17.9 ± 9.1
3	Fibromyalgia	Yes	121 (41.7%)	24.8 ± 5.6	<0.001
		No	169 (58.3%)	13.1 ± 7.8
4	Temporomandibular joint disorder	Yes	4 (1.4%)	24.3 ± 5.0	0.160
		No	286 (98.6%)	17.9 ± 9.1
5	Migraine or tension headache	Yes	40 (13.8%)	24.2 ± 6.4	<0.001
		No	250 (86.2%)	16.9 ± 9.0
6	Irritable bowel syndrome	Yes	8 (2.8%)	24.5 ± 5.7	0.040
		No	282 (97.2%)	17.8 ± 9.1
7	Multiple chemical sensitivities	Yes	5 (1.7%)	22.8 ± 7.9	0.204
		No	285 (98.3%)	17.9 ± 9.0
8	Neck injury (including whiplash)	Yes	11 (3.8%)	23.8 ± 5.4	0.021
		No	279 (96.2%)	17.7 ± 9.1
9	Anxiety or panic attacks	Yes	49 (16.9%)	16.7 ± 9.1	<0.001
		No	241 (83.1%)	24.2 ± 5.5
10	Depression	Yes	30 (10.3%)	25.4 ± 6.1	<0.001
		No	260 (89.7%)	17.1 ± 8.9
	At least 1 CSS symptom	Yes	90 (31.0%)	21.6 ± 6.1	<0.001
		No	200 (69.0%)	16.3 ± 9.7
	At least 2 CSS symptoms	Yes	39 (13.4%)	23.8 ± 5.2	<0.001
		No	251 (86.6%)	17.0 ± 9.2
	At least 3 CSS symptoms	Yes	31 (10.7%)	27.4 ± 4.5	<0.001
		No	259 (89.3%)	16.8 ± 8.8

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Internal consistency

For the overall sample, Cronbach’s α value was 0.902 for the overall scale, indicating excellent internal consistency (Table 6). For patients with chronic pain, Cronbach’s α value was 0.828 for the overall scale, with good internal consistency (Table 6). The Cronbach’s alpha displayed in Table 6 for each item represented the total Cronbach’s alpha of CSI-9 except the corresponding item.

Table 6. Internal consistency.

No.	CSI items	Overall sample (N = 290)	Chronic pain sample (N = 235)
1	Unrefreshed in the morning	0.893	0.811
2	Muscles stiff/achy	0.888	0.819
3	Pain all over body	0.880	0.794
4	Headache.	0.901	0.824
5	‘Do not sleep well	0.891	0.807
6	Difficulty concentrating	0.890	0.802
7	Stress makes symptoms worse	0.892	0.806
8	Tension neck and shoulder	0.889	0.808
9	Poor memory	0.897	0.824
	Total	0.902	0.828

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The ICC values shown for each item resulted from the remaining items after the deletion of that item.

Discriminatory analysis

The patients with chronic pain had a higher score for every item of part A of the CSI-9 than the group of healthy controls (P < 0.001 for all items) (S2 Table).

Floor and ceiling effects

Eight participants (2.8%) had a CSI-9 score of 0, and two participants (0.7%) had a CSI-9 score of 100 points. Therefore, ceiling and floor effects were not observed.

Exploratory analysis of the utility of the Chinese CSI-9 as a screening tool for CS

ROC curve analysis demonstrated that a CSI-9 score > 18 points (the optimal cut-off value) predicted the presence of CS in the overall sample with an AUC of 0.873 (95%CI, 0.829–0.909), a sensitivity of 79.4%, a specificity of 79.2%, a PPV of 82.5%, an NPV of 75.7% and an accuracy of 79.3% (Table 7). Interestingly, the sensitivity, NPV, and accuracy were lower when a cut-off value of 20 points was used, as described previously [11], although the specificity and PPV were higher using a cut-off value of 20 points (Table 7). In the chronic pain group, a CSI-9 value > 19 points (the optimal cut-off) detected the presence of CS with an AUC of 0.785 (95%CI, 0.727–0.836), a sensitivity of 74.4%, a specificity of 70.7%, a PPV of 84.4%, an NPV of 56.4% and an accuracy of 73.2% (Table 7).

Table 7. Utility of the Chinese 9-item Central Sensitization Inventory in the diagnosis of central sensitization.

Population	Outcome^a	Cut-off	Sensitivity (95%CI)	Specificity (95%CI)	PPV	NPV	Accuracy	AUC (95%CI)
Overall sample (n = 290)	Presence of CS	18	79.4% (72.3%, 85.4%)	79.2% (71.2%, 85.8%)	82.5%	75.7%	79.3%	0.873 (0.829, 0.909)
Overall sample (n = 290)		20^b	69.4% (61.6%, 76.4%)	85.4% (78.1%, 91.0%)	85.4%	69.4%	76.6%	—
Chronic pain sample (n = 235)		19	74.4% (66.9%, 80.9%)	70.7% (59.0%, 80.6%)	84.4%	56.4%	73.2%	0.785 (0.727, 0.836)

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^a Persons who had any one of the diseases in Part B of the CSI were diagnosed as having central sensitization. ^b A cut-off value of 20 was used according to the literature;¹⁵ the optimal cut-off values of 18 and 19 were calculated in the present study. AUC: area under the receiver operating characteristic curve; CI: confidence interval; CS: central sensitization; NPV: negative predictive value; PPV: positive predictive value.

Discussion

This study successfully developed a new version of the CSI-9 intended for use in China through a process that involved translation, back-translation, and cultural adaptation. The CSI-9 had reasonable construct validity, good-to-excellent test-retest reliability, good criterion validity, and excellent internal consistency. Furthermore, confirmatory factor analysis was used to test the structural validity, with one main factor that explained the majority of the total variance for the items in part A of the Chinese CSI-9. The instrument developed in this study could potentially be utilized as a tool to screen for CS in patients with chronic pain in China.

Structural validity relates to the extent to which the scores of a scale are an adequate reflection of the dimensionality of the construct to be measured [24]. Confirmatory factor analysis identified one factor between the items in part A of the Chinese CSI-9, along with the original CSI-9 [10]. Nevertheless, the factors have been reported for various versions of the CSI-25. For example, confirmatory factor analysis of the original English language version of the CSI-25 identified four main factors (“physical symptoms”, “emotional distress”, “headache/jaw symptoms”, and “urological symptoms”) [9], and the same four factors were described for the German CSI-25 [25]. Four main factors were also reported for the Dutch CSI-25 (“general disability and physical symptoms”, “emotional distress”, “higher central sensitivity”, and “urological and dermatological symptoms”) [26], while the Japanese version identified five factors (“emotional distress”, “headache/jaw symptoms”, “urological and general symptoms”, “muscle symptoms” and “sleep disturbance”) [27].

The construct validity of the Chinese CSI-9 was assessed by comparing it with other scales (the PCS and BPI) that evaluate similar qualities. The Chinese CSI-9 score was positively correlated with the total PCS score (r = 0.463) and its rumination, magnification, and helplessness subscale scores (r = 0.347–0.463). Furthermore, the Chinese CSI-9 score was also positively correlated with the BPI mean item score (r = 0.524), BPI total score (r = 0.773), and the number of painful body sites (r = 0.451). Hence, the Chinese CSI-9 exhibited a good correlation with a scale that evaluates pain characteristics such as intensity, location, and duration (BPI) but was less strongly correlated with a scale that assesses an individual’s experience of pain (PCS). Published data are lacking regarding the correlation of the original CSI-9 with other instruments, such as the BPI and PCS. However, our findings are broadly consistent with previous studies exploring the construct validity of the CSI-25. For example, the Greek CSI-25 correlated with the PCS score (r = 0.680) [28], and the Nepali CSI-25 correlated with the PCS score (r = 0.50), pain intensity measured by the Numerical Rating Scale (NRS; r = 0.25), and the total number of pain types (r = 0.35) [29]. The Japanese CSI-25 was positively correlated with the pain intensity (r = 0.42) and pain interference (r = 0.48) scores of the BPI [27], and the Italian CSI-25 was correlated with the NRS score (r = 0.427) [30]. The Chinese CSI-9 score was not correlated with the duration of pain, which is consistent with previous analyses of the CSI-25 [27, 29].

The test-retest reliability of the Chinese CSI-25 was excellent in the overall sample (ICC = 0.958), which is consistent with the good test-retest reliability reported for the original CSI-9 (ICC = 0.79) [10]. The test-retest reliability of the CSI-9 was also comparable to that described for the English (ICC = 0.817) [9], German (ICC = 0.917) [25], Dutch (ICC = 0.88–0.91) [26], Japanese (ICC = 0.85) [27], Greek (ICC = 0.991) [28], Nepali (ICC = 0.98) [29] and Persian (ICC = 0.934) [31] versions of the CSI-25.

The Chinese CSI-9 had a Cronbach’s α value of 0.902 in the overall sample (excellent internal consistency) and 0.828 in patients with chronic pain (good internal consistency), which compares with a Cronbach’s α value of 0.80 for the original CSI-9 [10], 0.879 for the English CSI-25 [9], 0.928 for the German CSI-25 [25], 0.78 for the Dutch CSI-25 [26], 0.89 for the Japanese CSI-25 [27], 0.993 for the Greek CSI-25 [28], 0.91 for the Nepali CSI-25 [29], 0.87 for the Italian CSI-25 [30], 0.87 for the Persian CSI-25 [31] and 0.872 for the Spanish CSI-25 [32].

A prior analysis of the original CSI-9 found that a cut-off value of 20 points was optimal for distinguishing patients with fibromyalgia from patients with musculoskeletal disorders (sensitivity of 92.3% and specificity of 93.3%), while a cut-off value of 17 points was optimal for distinguishing patients with fibromyalgia from healthy controls (sensitivity of 96.2% and specificity of 100%) [11]. By comparison, the optimal cut-off value for the Chinese CSI-9 was 18 points for the overall sample (sensitivity of 79.4% and specificity of 79.2%) and 19 points for the chronic pain group (sensitivity of 74.4% and specificity of 70.7%). Notably, the sensitivity, NPV, and accuracy of the Chinese CSI-9 were lower when a cut-off value of 20 points [11] was used, although the specificity and PPV were higher using a cut-off value of 20 points. The reasons underlying the difference in the optimal cut-off value between the Chinese and original versions of the CSI-9 remain undetermined, but the possibilities include differences in the characteristics of the study population (patients with chronic pain and healthy controls). Additional studies are required to confirm the optimal cut-off value for the Chinese CSI-9.

The management of chronic pain in China is still in its infancy [2, 5]. Indeed, although distressful and significantly affects the quality of life, chronic pain does not threaten the life of the patients, and healthcare priority is directed towards dangerous conditions. A major issue with chronic pain is that it is subjective, no device or blood test can quantify it, and its perception depends upon the individual. Such a situation calls for pragmatic evaluation tools for chronic pain, which are able to raise the diagnosis rate and further increase the treatment rate. The simplified CSI-9 that was validated in Chinese in this study is indeed convenient and easy to use in clinical practice. According to the results, CSI-9 was very suitable for the Chinese population. This validation and adaption of CSI-9 in China are of great significance for the improvement of future management strategies for chronic pain in China. The application of Chinese CSI-9 can help minimize the under-diagnosis rate, increase timely and appropriate treatments, alleviate patients’ pain, and increase patient satisfaction.

This study has some limitations. This was a single-center study, so the results may not be generalized to other patients with chronic pain. The CSS-related disorders diagnosed in part B of the CSI-9 were self-reported and not confirmed by a clinician; moreover, some patients may have had other CSS-related conditions not included in the scale. The use of a self-reporting scale would be predicted to introduce response bias. Alternative methods (such as quantitative sensory testing) were not carried out to confirm the presence/absence of CS. The pre-final questionnaire was tested on only six participants instead of the 30–40 recommended by Beaton et al. [33] because of the limited patient population. The ability of the Chinese CSI-9 to detect CS was not assessed in a separate validation group. Some study patients were receiving therapy, and this may have decreased the severity of their chronic pain/CS symptoms. Finally, a responsiveness analysis was not carried out to evaluate the effects of treatment.

Conclusion

In conclusion, a Chinese version of the CSI-9 was successfully generated using a process of translation, back-translation, and cultural adaptation. The Chinese CSI-9 had excellent test-retest reliability and satisfactory structural validity and construct validity. We propose that this simple scale could be used in China as a self-report questionnaire in clinical practice and research settings for screening CSS. Nevertheless, additional studies are required to confirm the optimal cut-off value of the CSI-9 before it can be used to screen for patients with CS.

Supporting information

S1 Data

(XLSX)

Click here for additional data file.^{(814.2KB, xlsx)}

S1 Table. Answers to part B of the Chinese 9-item central sensitization inventory.

(DOCX)

Click here for additional data file.^{(16KB, docx)}

S2 Table. Answers to part A of the Chinese 9-item central sensitization inventory.

(DOCX)

Click here for additional data file.^{(16.1KB, docx)}

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

The author(s) received no specific funding for this work.

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PLoS One. doi: 10.1371/journal.pone.0282419.r001

Decision Letter 0

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4 Nov 2022

PONE-D-22-25986Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center studyPLOS ONE

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Reviewer #1: Thank you for inviting me to have the opportunity to review this manuscript. This is a validation study culturally adapting the English short form of the Central Sensitization Inventory (CSI) into simplified Chinese in patients with chronic pain. I have the following comments and suggestions for the authors:

Abstract

1. In the abstract, it was reported that “chronic pain affects more than 20% of the general population” while “up to 30% of people are affected by chronic pain” was stated in the Introduction. It would be better for the authors to unify the percentage of people affected by chronic pain in both the Abstract and Introduction.

Introduction

2. The authors should notice that there is already a culturally adapted version of Chinese Central Sensitization Inventory published recently (Feng et al, 2022).

3. Lines 61-64, the sentence is not clear and it is suggested to be re-written for more clarity, e.g. “The current situation regarding the diagnosis and management of chronic pain is not satisfactory, with under diagnosis and treatment. Patients with chronic pain may be neglected for pain management or provided with insufficient pain control.”

Methods

4. Lines 107-8, the details of recruitment of the healthy controls should be provided. What was the physical examination center? Was this center located inside the hospital? What were its functions …?

5. Lines 113-5, lumbago and back pain are literally synonymous; and elbow pain should have included lateral epicondylitis which is now more appropriately labelled as lateral epicondylalgia.

6. The specified inclusion criteria for the healthy controls did not exclude any acute pain status of the controls. So were there any healthy subjects with acute pain included in the study?

7. Lines 136-7 and 147-8, the citation of the “Brislin bidirectional translation method” should be provided.

8. As the forward and backward translations of the CSI-9 were fundamentally important to develop a culturally valid Chinese CSI-9, more details of the translation processes (forward and backward) such as the aim to identify any issues of ambiguous meanings in the original questionnaire or any inconsistencies or conceptual errors in the translations, and more details of the background of the translators in the forward and backward translations such as working experience as healthcare professionals, and qualifications of the professional translators … should be provided. Did the expert committee consider the semantic, idiomatic, experiential and conceptual equivalences as mentioned by Beaton et al (2000) (reference number 15) in finalizing the initial draft of Chinese CSI-9?

9. If the authors really followed the steps outlined by Beaton et al (2000), there should be 3 forward translations, T1, T2 and T3 and the 3 translators agreed a preliminary version A. Also, there should be 2 backward translations, BT1 and BT2. Was there a common backward translated English version BT1-2, or the expert committee reviewed the version A (common forward translation) with BT1 and BT2 to produce the pre-final version B (Chinese CSI-9)? Please clarify.

10. As recommended by Beaton et al (2000), the pre-final version should be administered to 30 to 40 subjects for pilot testing. The authors have to justify why only 6 patients were recruited to test the pre-final version for obtaining feedback or to address the limited number of subjects during pilot testing in the Limitations.

11. It is uncommon to use the Delphi method to develop the final version of questionnaire from the pre-final version with the feedback from the pilot tested subjects. The authors should provide more justification for the use of the Delphi method in this aspect.

12. Lines 168-70, what is the rationale or justification underlying the grading of subclinical (0-9 points), mild (10-19 points) and moderate/severe (>/=20 points) for the Chinese CSI-9 part A? Is there any reference for supporting this grading?

13. The citations and brief measurement properties of the Chinese Brief Pain Inventory and Chinese Pain Catastrophic Scale should be provided.

14. In the validity assessment, the authors had actually examined the construct validity of the Chinese CSI-9 in terms of structural/factorial validity, convergent validity and discriminant/divergent validity (Portney, 2020, p.127-140). It was mentioned that “The principal components were screened by promax rotation, and items were deleted if they had a factor loading <0.4” (lines 187-8). Was principal components analysis conducted in addition to the confirmatory factor analysis (CFA)? Why this had to be done if CFA was already planned?

15. In CFA, the number of factors and items loading on those factors had to be specified before conducting the CFA. What were the initial considerations in determining the number of factors and which items should be loaded to which factors in the CFA?

16. The criteria for interpreting those indices of model fit in CFA and magnitude of correlations in convergent validity should be specified in advance.

17. Line 212, the authors have to elaborate, how the “stable therapeutic regimen” could determine which patients were stable for the test-retest? Were these “stable patients” determined solely by the doctors or researchers, or by the self-report of the patients?

18. Lines 213-4, the “intra-group correlation coefficient” should be more correctly be “intraclass correlation coefficient” (ICC). The authors need to provide the choice of model for the ICC, e.g. one-way random-effects model, two-way random-effects model or two-way mixed effects model and whether “consistency” or “absolute agreement” had been used for the latter two models.

19. The authors should provide the sample size estimations for different parts of the cross-cultural adaptation of the CSI-9, e.g. how many subjects should be required for the confirmatory factor analysis, test-retest reliability analysis, correlational analyses and ROC curve analyses?

Results

20. It was mentioned that there were 290 patients recruited in the final analysis, with 235 patients with chronic pain and 55 healthy controls. Does this mean that those healthy controls were actually “patients”?

21. In Table 1, one decimal place should be good enough for presenting the scores of those variables to avoid false precision. The “overall population” should be “overall sample” or “all participants”.

22. In Table 2 showing the 9 English items of CSI-9, except the item “I do not sleep well”, all the other 8 items are slightly different from the original items of the CSI-25 published by Mayer et al (2012). Were those 8 English items modified during the background translation of the Chinese CSI-9?

23. How did those 3 factors determined with the loading of the 9 items? It seems inappropriate to label the Factor 3 as “headache/jaw symptoms” as there was no item related to jaw symptom in the Chinese CSI-9.

24. The author should report the model fit indices of the CFA, e.g. GFI, AGFI, CFI, TLI and RMSEA in the Results.

25. In Table 3, did the result of correlations meet the pre-specified criteria for convergent and divergent validities of the Chinese CSI-9 with those variables?

26. The model of ICC should be specified in reporting the ICC values.

27. Cronbach’s alpha is a measure of the average inter-relatedness of items of a scale examined for the internal consistency of the scale. In Table 6, it appears that each of the 9 items had their own Cronbach’s alpha which is unconceivable as single item would not have correlation with other items!

Discussion

28. Lines 355-6, it is more appropriate to state that “structural validity” refers to the extent to which the scores of a scale are an adequate reflection of the dimensionality of the construct to be measured (Mokkink et al, 2010).

29. The development of the CSI-9 by Nishigami et al (2018) was resulted from the use of Rasch analysis to achieve unidimensionality, i.e. single factor. The authors should discuss whether they had conducted the CFA with single factor in mind and how they would end up with 3 factors from the CFA, contrary to the result of Nishigami et al’s study (2018).

30. The items of the original CSI-25 were developed by an interdisciplinary team of healthcare professionals but there was no description of how those items were identified or developed from any item pool extracted from the literature. There were no inputs and cognitive debriefing from the patients with chronic pain and central sensitization during the development phase of the original CSI-25. Therefore, the content validity of the CSI-25 may have limitations which may partly account for the different factor models found in different populations. The development of a short form of an original questionnaire would require rigorous methodology; otherwise the validity of the original questionnaire (especially content validity) may further be compromised (Goetz et al, 2013)! The authors should have a good discussion on these issues.

31. Lines 433-4, the application of Chinese CSI-9 should not be intended to “increase diagnosis rate” but to minimize “under-diagnosis” of central sensitization so that patients with central sensitization can receive timely and appropriate treatment.

32. Lines 436-7, the results may not “be generalized” to other patients with chronic pain.

Conclusion

33. Lines 452-3, it is suggested to rephrase the sentence as, “We propose that this simple scale could be used in China as a self-report questionnaire in clinical practice and research settings for screening central sensitization syndrome”.

References

Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine 2000; 25(24): 3186-91. doi: 10.1097/00007632-200012150-00014.

Feng B, Hu X, Lu WW, Wang Y, Ip WY. Cultural Validation of the Chinese Central Sensitization Inventory in patients with chronic pain and its predictive ability of comorbid central sensitivity syndromes. J Pain Res 2022; 15: 467-477. doi: 10.2147/JPR.S348842.

Goetz C, Coste J, Lemetayer F, Rat AC, Montel S, Recchia S, Debouverie M, Pouchot J, Spitz E, Guillemin F. Item reduction based on rigorous methodological guidelines is necessary to maintain validity when shortening composite measurement scales. J Clin Epidemiol 2013; 66(7): 710-8. doi: 10.1016/j.jclinepi.2012.12.015.

Mayer TG, Neblett R, Cohen H, Howard KJ, Choi YH, Williams MJ, Perez Y, Gatchel RJ. The development and psychometric validation of the central sensitization inventory. Pain Pract 2012; 12(4): 276-85. doi: 10.1111/j.1533-2500.2011.00493.x.

Mokkink LB, Terwee CB, Patrick DL, Alonso J, Stratford PW, Knol DL, Bouter LM, de Vet HC. The COSMIN study reached international consensus on taxonomy, terminology, and definitions of measurement properties for health-related patient-reported outcomes. J Clin Epidemiol 2010; 63(7): 737-45. doi: 10.1016/j.jclinepi.2010.02.006.

Nishigami T, Tanaka K, Mibu A, Manfuku M, Yono S, Tanabe A. Development and psychometric properties of short form of central sensitization inventory in participants with musculoskeletal pain: A cross-sectional study. PLoS One 2018;13(7): e0200152. doi: 10.1371/journal.pone.0200152.

Portney LG. Foundations of Clinical Research: Applications to Evidence-Based Practice, 4th ed, Philadelphia: F.A. Davis, 2020.

Reviewer #2: All in all, a very well written validity and reliability article. Just ı can say more healthy controls would be better. Congratulations to the authors.

**********

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Reviewer #1: Yes: Raymond CC Tsang

Reviewer #2: Yes: Esedullah AKARAS

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PLoS One. 2023 Mar 16;18(3):e0282419. doi: 10.1371/journal.pone.0282419.r002

Author response to Decision Letter 0

6 Dec 2022

Manuscript ID: PONE-D-22-25986

Title: Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center study

Name of Journal: Plos One

Response to Reviewers’ comments

Dear Editor PhD. Fatih Özden:

We thank you for carefully considering our manuscript, and we are grateful for your response and overall positive feedback. After carefully reviewing the comments made by the reviewers, we have modified the manuscript to improve the presentation and discussion of our study, providing a full context to the study.

Furthermore, we have thoroughly revised the manuscript and improved the language quality, taking into consideration the reviewers’ and editors’ comments. We hope that you now find the revised manuscript suitable for publication and look forward to contributing to your journal. We believe that the revised manuscript would be of interest to your readership.

Please do not hesitate to contact me with any questions or concerns regarding the current manuscript.

Best regards,

Dong-feng Liang

Reviewer #1

Thank you for inviting me to have the opportunity to review this manuscript. This is a validation study culturally adapting the English short form of the Central Sensitization Inventory (CSI) into simplified Chinese in patients with chronic pain. I have the following comments and suggestions for the authors:

Abstract

Response: We thank the Reviewer for pointing out that discrepancy. It was corrected.

Introduction

2. The authors should notice that there is already a culturally adapted version of Chinese Central Sensitization Inventory published recently (Feng et al, 2022).

Response: We thank the Reviewer for the comment. China is a huge country with many research teams in various regions. We were not aware that someone else was working on a Chinese CSI-9 version, and their paper was published after we finalized the present manuscript. Of note, they validated a Chinese version of the original CSI-25 [1], while we directly validated the CSI-9 in Chinese. Nevertheless, we added that paper to our manuscript.

Response: We thank the Reviewer. We revised that part of the Introduction.

Original version: In China, since the condition does not threaten the life of the patients, chronic pain is often overlooked. The current situation regarding the diagnosis and treatment of chronic pain is not satisfying, with low diagnosis rate, low treatment rate, insufficient pain control, poor management of pain, and neglect of pain management.

Revised version: In China, since chronic pain does not threaten the life of the patients, it is often overlooked, leading to low diagnosis rates, low treatment rates, insufficient pain control, poor management of pain, and neglect of pain management.

Methods

Response: The physical examination center is the department located inside the hospital that specializes in physical examination, and it offers routine regular physical examinations for ordinary people. It was clarified in the Methods-study participants section.

5. Lines 113-5, lumbago and back pain are literally synonymous; and elbow pain should have included lateral epicondylitis which is now more appropriately labelled as lateral epicondylalgia.

Response: The Reviewer is right. These were corrected as suggested.

6. The specified inclusion criteria for the healthy controls did not exclude any acute pain status of the controls. So were there any healthy subjects with acute pain included in the study?

Response: CSI focuses on chronic pain, not related to acute pain. Neither the chronic population nor healthy population in our study excluded acute pain. Whether there was acute pain did not affect the validity test or reliability test of CSI. The BPI of four individuals in the healthy population showed there had acute pain recently.

7. Lines 136-7 and 147-8, the citation of the “Brislin bidirectional translation method” should be provided.

Response: Brislin, R. W. (1970). Back-Translation for Cross-Cultural Research. Journal of Cross-Cultural Psychology, 1(3), 185–216. https://doi.org/10.1177/135910457000100301. It was added to the manuscript.

Response: The experts were all experienced in fibromyalgia, pain, and the psychology of pain:

1). Dongfeng Liang, Deputy Chief Physician, Department of Rheumatology and Immunology, First Medical Center, PLA General Hospital;

2). Wu Qingjun, Chief Physician of the Rheumatology and Immunology Department of Peking Union Medical College Hospital;

3). Luo Fang, Chief Physician of the Pain Department of Tiantan Hospital Affiliated to Capital Medical University;

4). Shi Hui, Deputy Chief Physician of the Psychiatry Department of Chaoyang Hospital Affiliated to Capital Medical University;

5). Yao Zhongqiang, Deputy Chief Physician of the Rheumatology and Immunology Department of the Third Affiliated Hospital of Beijing Medical University;

6). Xu Xiaoyan, Deputy Chief Physician of the Rheumatology and Immunology Department of Zhongda Hospital Affiliated to Southeast University;

7). Li Ling, Deputy Chief Physician of the Rheumatology and Immunization Department of Guangdong Provincial People’s Hospital.

All the above experts participated in the Delphi consultation on the Chinese version. With regard to the translation process, the implementation process was as follows.

1) Two experts (LD and ZG) and a Chinese professional translator (Shanghai Richard Translation Co.) translated the scale from English to Chinese, and the researchers integrated it into the original Chinese version.

2) A professional translator of Chinese nationality and a professional English native-speaking translator (Shanghai Richard Translation Co.) back-translated the original Chinese version of the scale, namely, Chinese to English.

3) The researchers combined the results of the English-to-Chinese translation and Chinese-to-English translation to form the first Chinese version of the scale again.

4) The first Chinese version of the scale was tested by doctors and patients, and the translated items were modified again according to the test results to obtain the final version of the Chinese CSI-9.

Response: We used the Brislin bidirectional translation method [2]. All the above experts participated in the Delphi consultation on the Chinese version. The implementation of the translation process was described as in the above response.

Response: We thank the Reviewer for the comment. A pre-study of 30-40 was impossible in our clinical setting, and the time required to perform it would have incurred the risk of making the first participants obsolete by the time all participants completed the questionnaires. Therefore, we administered the questionnaire to 10 participants. It was added as a limitation.

Response: The Delphi method was applied in order to consult as many experienced experts in various hospitals across China as possible (seven experts in total), thus increasing the usability and readability of Chinese CSI-9. Furthermore, the results from six patients were also considered. All results from the doctors and patients were fully discussed to achieve the final Chinese CSI-9.

Response: The cutoff points were according to the original CSI-9 version [3]. We added the reference to the manuscript.

13. The citations and brief measurement properties of the Chinese Brief Pain Inventory and Chinese Pain Catastrophic Scale should be provided.

Response: The citations and measurements of Chinese BPI and Chinese PCS scales were clarified in the “Data collection” section and the “Validity assessment” section in Methods.

Wang XS, Mendoza TR, Gao SZ, Cleeland CS. The Chinese version of the Brief Pain Inventory (BPI-C): its development and use in a study of cancer pain. Pain. 1996 Oct;67(2-3):407-16. doi: 10.1016/0304-3959(96)03147-8. PMID: 8951936.

Shen B, Wu B, Abdullah TB, Zhan G, Lian Q, Vania Apkarian A, Huang L. Translation and validation of Simplified Chinese version of the Pain Catastrophizing Scale in chronic pain patients: Education may matter. Mol Pain. 2018 Jan-Dec;14:1744806918755283. doi: 10.1177/1744806918755283. Epub 2018 Jan 21. PMID: 29353539; PMCID: PMC5788090.

Response: The CFA results indicated no need to delete items. EFA delete items by principal components analysis. If the result of CFA was not satisfying, then EFA was conducted. Principal components analysis was not conducted in this study. The mistake occurred during manuscript preparation and translation. It has been deleted to avoid misunderstanding.

Response: The Chinese CSI-9 was a validation of the Chinese version from the original English CSI-9. All items and factors were determined according to the original version.

16. The criteria for interpreting those indices of model fit in CFA and magnitude of correlations in convergent validity should be specified in advance.

Response: The criteria for interpreting model fit and magnitude of correlations in convergent validity were specified in advance. It was clarified in the Methods section.

Response: Test-retest reliability was used to assess the stability of the CSI-9. When tested for the first time, all subjects were confirmed by randomization whether to be tested for the second time at 7 ± 1 days after the first test. Those who are retested were required to maintain a stable therapeutic regimen (i.e., no changes in drugs and dosages) between the first and second tests. It was clarified in the “Reliability assessment” section.

Response: It was corrected into “intraclass correlation coefficient (ICC)”. We used “two-way random-effects model” and “absolute agreement”. It was clarified in the manuscript.

Response: The sample size calculation was based on CFA, as designed in the protocol, and including at least 200 patients would meet the needs for validation, and 50 would be sufficient for retest reliability. The necessary sample sizes for other measurements were all not that large as CFA.

Results

Response: We apologize for the wrong choice of word. In fact, the healthy controls were included from the physical examination department who were intended for a routine health check. It was corrected.

Response: We thank the Reviewer. The tables were revised accordingly.

Response: Indeed, the items were modified during the translation process. To avoid misunderstanding, we revised the items in Tables 2, 4, and 6, and kept them the same with those in Mayer et al (2012).

Response: We were wrong to label the three factors. According to the original CSI-9, we redid the statistical analysis as one factor as follows:

Structural validity

CSI items Mean (SD) Factor 1

1 Unrefreshed in morning 2.2±1.3 0.692

2 Muscles stiff/achy 2.5±1.4 0.773

3 Pain all over body 2.2±1.5 0.865

4 Headaches 1.3±1.2 0.567

5 Do not sleep well 2.1±1.4 0.711

6 Difficulty concentrating 1.6±1.3 0.712

7 Stress makes symptoms worse 1.5±1.3 0.692

8 Tension neck and shoulder 2.3±1.4 0.752

9 Poor memory 2.1±1.3 0.623

24. The author should report the model fit indices of the CFA, e.g. GFI, AGFI, CFI, TLI and RMSEA in the Results.

Response: We thank the Reviewer. The model fit indices were chi-square (CMIN)=60.05, degree of freedom (DF)=24, P<0.001, CMIN/DF=2.877, Tucker-Lewis index (TLI)=0.948, comparative fit index (CFI)=0.965, root mean square error of approximation (RMSEA)=0.081. They were added to the results.

25. In Table 3, did the result of correlations meet the pre-specified criteria for convergent and divergent validities of the Chinese CSI-9 with those variables?

Response: We thank the Reviewer. Yes, the result of the correlations met the pre-specified criteria for convergent and divergent validities of the Chinese CSI-9 with those variables.

26. The model of ICC should be specified in reporting the ICC values.

Response: We thank the Reviewer. It was the “two-way random-effects model”. It was clarified in the “Test-retest reliability” in the Results.

Response: The Cronbach’s alpha displayed in Table 6 was not for each item itself, and it was the total Cronbach’s alpha of CSI-9 except the corresponding item. It was clarified in the text. The Greek adaption of CSI-25 also displayed like this.

Bilika P, Neblett R, Georgoudis G, Dimitriadis Z, Fandridis E, Strimpakos N, Kapreli E. Cross-cultural Adaptation and Psychometric Properties of the Greek Version of the Central Sensitization Inventory. Pain Pract. 2020 Feb;20(2):188-196. doi: 10.1111/papr.12843. Epub 2020 Jan 6. PMID: 31605651.

Discussion

Response: We thank the Reviewer. It was revised as suggested.

Response: We thank the Reviewer. We were wrong. It was to be a single factor. We redid the calculation and provided the results above. It was corrected.

Response: We thank the Reviewer, but the Chinese CSI-9 was not a simplified version of the Chinese CSI-25. It is a translation of the validated original CSI-9.

Response: We agree with the Reviewer. It was revised as suggested.

32. Lines 436-7, the results may not “be generalized” to other patients with chronic pain.

Response: It was corrected.

Conclusion

Response: We thank the Reviewer. It was revised as suggested.

References

Beaton DE, Bombardier C, Guillemin F, Ferraz MB. Guidelines for the process of cross-cultural adaptation of self-report measures. Spine 2000; 25(24): 3186-91. doi: 10.1097/00007632-200012150-00014.

Portney LG. Foundations of Clinical Research: Applications to Evidence-Based Practice, 4th ed, Philadelphia: F.A. Davis, 2020.

Response: We thank the Reviewer. We carefully read the above references and we added some of them into the manuscript where appropriate.

Reviewer #2:

All in all, a very well written validity and reliability article. Just ı can say more healthy controls would be better. Congratulations to the authors.

Response: We thank the Reviewer for the comment. We revised the whole manuscript according to your Reviewers’ comments.

References

1. Feng B, Hu X, Lu WW, Wang Y, Ip WY. Cultural Validation of the Chinese Central Sensitization Inventory in Patients with Chronic Pain and its Predictive Ability of Comorbid Central Sensitivity Syndromes. J Pain Res. 2022;15:467-77. Epub 2022/02/26. doi: 10.2147/JPR.S348842. PubMed PMID: 35210847; PubMed Central PMCID: PMCPMC8857991.

2. Brislin RW. Back-Translation for Cross-Cultural Research. J Cross Cultural Psychol. 1970;1(3):185-216. doi: 10.1177/135910457000100301.

3. Nishigami T, Tanaka K, Mibu A, Manfuku M, Yono S, Tanabe A. Development and psychometric properties of short form of central sensitization inventory in participants with musculoskeletal pain: A cross-sectional study. PLoS One. 2018;13(7):e0200152. Epub 2018/07/06. doi: 10.1371/journal.pone.0200152. PubMed PMID: 29975754; PubMed Central PMCID: PMCPMC6033441.

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PLoS One. doi: 10.1371/journal.pone.0282419.r003

Decision Letter 1

Fatih Özden

12 Dec 2022

PONE-D-22-25986R1Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center studyPLOS ONE

Dear Dr. Liang,

Additional Editor Comments:

The reviewer suggested a minor revision. I look forward to your revised article.

Please submit your revised manuscript by Jan 26 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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We look forward to receiving your revised manuscript.

Kind regards,

Fatih Özden, PhD

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: No

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

**********

6. Review Comments to the Author

Reviewer #1: Most of the issues have been addressed by the authors, except the following:

1. In the Abstract (lines 33-35) and Discussion (lines 366-367), it is still stated that “confirmatory factor analysis extracted three main factors (“physical symptoms”, “emotional distress”, and “headache/jaw symptoms”)”. Please clarify and correct this.

2. In Table 4, test-retest reliability, were the ICC values shown for each item resulted from the remaining items after deletion of that item? If that is the case, this should be explained in the footnote of the table for clarity. The same explanation should also be applied in Table 6 for the internal consistency.

3. The number of participants for pilot testing of the Chinese CSI-9 is 10 in the Discussion section (line 453) while this is reported to be 6 in the Methods section (line 164). Please clarify and correct this.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: TSANG Chi-Chung Raymond

**********

PLoS One. 2023 Mar 16;18(3):e0282419. doi: 10.1371/journal.pone.0282419.r004

Author response to Decision Letter 1

3 Jan 2023

Manuscript ID: PONE-D-22-25986

Title: Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center study

Name of Journal: PLoS One

Response to Reviewers’ comments

Dear Editor PhD. Fatih Özden:

Thank you for carefully considering our manuscript! We are grateful for your response and overall positive feedback. After carefully reviewing the comments made by Reviewer 1, we have modified the manuscript, providing a full context to the study.

We hope that you now find the revised manuscript suitable for publication and look forward to contributing to your journal. We believe that the revised manuscript would be of interest to your readership.

Please do not hesitate to contact me in case of any questions or concerns regarding the current manuscript.

Best regards,

Dong-feng Liang

Reviewer #1

Reviewer #1: Most of the issues have been addressed by the authors, except the following:

Response: The Reviewer is right. It was added as a footnote to Tables 4 and 6.

Response: We thank the Reviewer for pointing out that discrepancy. It was corrected in the Discussion. It was six.

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PLoS One. doi: 10.1371/journal.pone.0282419.r005

Decision Letter 2

Fatih Özden

9 Jan 2023

PONE-D-22-25986R2Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center studyPLOS ONE

Dear Dr. Liang,

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6. Review Comments to the Author

Reviewer #1: All the concerns have been addressed except the criteria of model fit indices for the cofirmatory factor analysis (CFA) and their citation are missing in the Methods - Validity Assessment section. The authors should provide this information to allow readers to evaluate the model fit of the one-factor model from the CFA.

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Reviewer #1: Yes: Raymond CC Tsang

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PLoS One. 2023 Mar 16;18(3):e0282419. doi: 10.1371/journal.pone.0282419.r006

Author response to Decision Letter 2

13 Feb 2023

Manuscript ID: PONE-D-22-25986R2

Title: Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center study

Name of Journal: PLoS One

Response to Reviewers’ comments

Dear Editor PhD. Fatih Özden:

Please do not hesitate to contact me in case of any questions or concerns regarding the current manuscript.

Best regards,

Dong-feng Liang

Reviewer #1

All the concerns have been addressed except the criteria of model fit indices for the confirmatory factor analysis (CFA) and their citation are missing in the Methods - Validity Assessment section. The authors should provide this information to allow readers to evaluate the model fit of the one-factor model from the CFA. Response: We thank the Reviewer. It was added in the Methods section.

Revised version: The indices used to determine the model fit were: chi-square degrees of freedom (�2/df), goodness-of-fit index (GFI), adjusted goodness-of-fit index (AGFI), comparative fit index (CFI), Tucker-Lewis Coefficient (TLI) and root mean square error of approximation (RMSEA). A model with �2/df<3, RMSEA<0.08, GFI>0.90, CFI>0.90, and TLI>0.90 suggested a good fit [reference].

Reference: Qiu H, Huang C, Liu Q, Jiang L, Xue Y, Wu W, Huang Z, Xu J. Reliability and validity of the Healthy Fitness Measurement Scale Version 1.0 (HFMS V1.0) in Chinese people. BMJ Open. 2021 Dec 7;11(12):e048269.

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PLoS One. doi: 10.1371/journal.pone.0282419.r007

Decision Letter 3

Fatih Özden

15 Feb 2023

Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center study

PONE-D-22-25986R3

Dear Dr. Liang,

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Fatih Özden, PhD

Academic Editor

PLOS ONE

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Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0282419.r008

Acceptance letter

Fatih Özden

7 Mar 2023

PONE-D-22-25986R3

Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: a single-center study

Dear Dr. Liang:

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Data

(XLSX)

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S1 Table. Answers to part B of the Chinese 9-item central sensitization inventory.

(DOCX)

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S2 Table. Answers to part A of the Chinese 9-item central sensitization inventory.

(DOCX)

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Data Availability Statement

All relevant data are within the paper and its Supporting Information files.

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Cross-cultural adaptation and validation of the Chinese version of the short-form of the Central Sensitization Inventory (CSI-9) in patients with chronic pain: A single-center study

Dongfeng Liang

Xiangli Yu

Xiaojie Guo

Jie Zhang

Ronghuan Jiang

Roles

Abstract

Introduction

Methods

Study participants

Study design

Development of the Chinese CSI-9

Data collection

Validity assessment

Reliability assessment

Measurement error

Floor and ceiling effects

Exploratory analysis of the utility of the Chinese CSI-9 as a screening tool for CS

Statistical analysis

Results

Cross-cultural adaptation of the CSI-9 into Chinese

Baseline characteristics of the study participants

Table 1. Baseline data.

Structural validity

Table 2. Structural validity of the Chinese central sensitization inventory.

Construct validity

Table 3. Construct validity in the overall sample (n = 290).

Test-retest reliability

Table 4. Test-retest reliability (two-way random-effects model).

CSS-related disorders

Measurement error

Fig 1. Bland-Altman plots for evaluating measurement error.

Criterion validity

Table 5. Criterion validity in the overall sample (n = 290).

Internal consistency

Table 6. Internal consistency.

Discriminatory analysis

Floor and ceiling effects

Exploratory analysis of the utility of the Chinese CSI-9 as a screening tool for CS

Table 7. Utility of the Chinese 9-item Central Sensitization Inventory in the diagnosis of central sensitization.

Discussion

Conclusion

Supporting information

Data Availability

Funding Statement

References

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Fatih Özden

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Author response to Decision Letter 0

Decision Letter 1

Fatih Özden

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Author response to Decision Letter 1

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Fatih Özden

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Author response to Decision Letter 2

Decision Letter 3

Fatih Özden

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Acceptance letter

Fatih Özden

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

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