Sleep Breath (2011) 15:775780 DOI 10.

1007/s11325-010-0435-3

ORIGINAL ARTICLE

The Serbian version of the Epworth Sleepiness Scale

Ivan Kopitovic & Nikola Trajanovic & Sinisa Prodic & Mirjana Jovancevic Drvenica & Miroslav Ilic & Vesna Kuruc & Marija Kojicic

Received: 19 August 2010 / Revised: 19 October 2010 / Accepted: 22 October 2010 / Published online: 5 November 2010 # Springer-Verlag 2010

Abstract Purpose The Epworth Sleepiness Scale (ESS) is extensively used for evaluating daytime sleepiness in patients with sleep apneahypopnea syndrome (SAHS). The aim of this study was to translate and validate the ESS in the Serbian language. Methods The Serbian version of the ESS (ESSs) was administered to 112 patients with symptoms of sleep disorder breathing referred to Sleep Center of the Institute for Pulmonary Diseases of Vojvodina, Sremska Kamenica, Serbia and 111 healthy controls. Testretest reliability was tested in 19 healthy subjects. Results Patients referred to the Sleep center had significantly higher ESS scores compared to controls (9 vs. 4, p<0.001). The difference was also present for each item separately, excluding item 5. The ESSs scores were significantly higher in patients with severe (median, 13.5; interquartile range (IQR), 10.317.8) compared to moderate (median, 9; IQR, 7.39.5; p=0.005) and mild SAHS (median, 8; IQR, 5.5 9.7; p<0.001). Item analysis demonstrated good internal consistency of the scale (Cronbachs alpha 0.88 in patients and 0.72 in healthy controls). Testretest Spearmans correlation coefficient was 0.68 (p=0.001).
I. Kopitovic (*) : S. Prodic : M. J. Drvenica : M. Ilic : V. Kuruc : M. Kojicic Center for Sleep Medicine, The Institute for Pulmonary Diseases of Vojvodina, Institutski put 4, 21204 Sremska Kamenica, Serbia e-mail: ikopitovic@gmail.com N. Trajanovic Sleep Research Unit, University Health Network, Toronto, Canada

Conclusion The Serbian version of the ESS demonstrated good internal consistency and testretest reliability. The ESSs could be used for both clinical practice and research in Serbian population. Keywords Sleep apnea . Epworth Sleepiness Scale . Validation

Introduction The Epworth Sleepiness Scale (ESS) is a widely used self-reported questionnaire for assessing daytime sleepiness in patients with sleep apneahypopnea syndrome (SAHS). It originated and was initially utilized in English-speaking countries [1]. The ESS measures the probability of falling asleep in eight common situations involving daily activities. Due to its simplicity, high reliability, and internal consistency, the ESS has been used in a clinical setting to estimate the degree of sleep apnea syndrome [2] or assess the treatment effects [3, 4], as well as to screen patients for clinical trials [5]. In addition, the ESS has been shown to predict the drivers risk of being involved in car traffic accidents as a result of the excessive daytime sleepiness [6]. As sleep medicine developed in recent decades, the ESS was translated in various languages and is extensively used in everyday clinical practice. Up to this point, there was no formal validation of a questionnaire for the measurement of excessive daytime sleepiness in the Serbian-speaking population, and, to the best of our knowledge, in other west Balkan languages. This potentially affected a doctrinary development of the

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sleep medicine and research in this part of the world. The aim of the present study is to translate and validate ESS into Serbian language.

excluded. Testretest reliability of the total score was assessed in 19 subjects who completed ESS on two occasions, 1 month apart. Statistical analysis

Material and methods Translation of ESS into Serbian language The ESS was translated into Serbian language by two clinicians, specialists in Pulmonary medicine. The questionnaire was then administered to ten patients seen at the Sleep center to assure understanding and face validity. Finally, the questionnaire was back-translated from Serbian into English by a bilingual professional interpreter, and the translation was compared with the original version of the ESS. A proper copyright consent from the copyright holder was obtained for the translation and use of the Serbian version of the ESS. Subjects Results A total of 112 subjects who underwent a sleep study at the Institute for Pulmonary Diseases of Vojvodina, Sremska Kamenica, Serbia, a university-affiliated hospital, between June 2006 and September 2009 were assessed. All patients answered the Serbian version of the ESS at their initial outpatient assessment (Appendix). At that time, a complete medical history was taken, and physical examination was performed. The polysomnography (PSG) was performed using SomnoStar, Viasys Healthcare PSG system, measuring electroencephalogram, electrooculogram, electromyogram, arterial oxygen saturation, abdominal and thoracic respiratory movements, oronasal pressure and snoring, and monitoring ECG. Tracings were recorded and analyzed visually. An apnea was defined as complete cessation of airflow for at least 10 s, and hypopnea was defined as a decrease in airflow by more than 50% from baseline for at least 10 s. According to their apneahypopnea index (AHI), patients were divided into three subgroups: severe (AHI>30 per hour), moderate (AHI between 15 and 30 per hour), and mild SAHS (AHI between 5 and 15 per hour) [7]. The study was approved by the Institutional review board who waived the need for informed consent due to an observational study design. Control subjects Control subject included 111 healthy subjects, 25 (23%) males, aged 36 years (interquartile range (IQR), 3147), mainly hospital staff and their relatives who were not involved in shift work. Subjects with sleep problems were Subjects characteristics are presented in Table 1. The patients referred to the Sleep center had significantly higher ESS scores compared to normal subjects (mean, 9; IQR, 612 vs. median 4 IQR 27; p < 0.001). The difference was also present for each item separately, excluding item 5 (Table 2). The ESSs scores were significantly higher in patients with severe (median, 13.5; IQR 10.317.8) compared to moderate (median, 9; IQR, 7.39.5; p=0.005) and mild SAHS (median, 8; IQR 5.59.7; p<0.001). There was no significant difference in ESSs between male and female controls (median, 5; IQR, 28 vs. median 4 IQR 26; p=0.62). Item analysis, internal consistency, and testretest variability The reproducibility was tested in 19 healthy medical workers. No significant differences were found in the total ESS (mean, 3; IQR, 16 vs. mean 2 IQR, 26; p= 0.34), nor for each item, respectively. The Spearmans correlation coefficient was 0.68 (p=0.001). The Cronbachs alpha coefficients for the ESS (Table 3) demonstrated good internal consistency. The Cronbachs alpha coefficient for 112 patients was 0.88 and 0.72 for healthy controls. The ROC curve of the ESS for identification of cases with AHI>5 per hour among 112 patients was 0.85 with a cut-off value of 9, providing best sensitivity and specificity (Fig. 1). An ESS score of 5 has 96% sensitivity and 28% specificity in detecting AHI>5. A continuous data are presented as means and standard deviation for normally distributed data, and median and IQR for non-normally distributed data. Categorical variables are presented as whole numbers and percentages. The comparison of continuous variables was done using Mann Whitney U test. The internal consistency reliability was assessed using a Cronbachs alpha coefficient. The test retest variability was examined by the mean difference of the scores. The performance of the ESS to prioritize polysomnography in patients with suspected sleep apnea was evaluated by plotting receiver operating curve (ROC). A probability of p < 0.05 was considered statistically significant.

Sleep Breath (2011) 15:775780 36 (3141) 86 (77)

777 Table 2 Comparison of ESS scores in patients and normal subjects 4 (27) Patients N=112 1 2 3 4 5 6 7 8 ESS, median, IQR 1 2 1 1 2 0 1 0 9 (12) (12) (01) (12) (13) (01) (12) (01) (612) Normal subjects N=111 0 0 0 0 2 0 0 0 4 (01) (12) (01) (01) (12) (00) (01) (00) (27) p

Normal subjects N=111

167 (161313)

47 (2249) 2 (66) 21(1922) 0 (01.2) 96 (9597) 95 (8696) 0 (00.2)

Psychiatric disease N=3

6(68)

<0.001 <0.001 <0.002 <0.001 0.10 <0.001 <0.001 <0.001 <0.001

412 (344463)

(4359) (22) (2532) (1.443.7) (8895) (7589) (0.373)

All patients

N=112

53 25 28 17.4 93 84 6.6

9 (612)

Periodic limb movement N=4

57 (5365) 3 (75) 23 (2128) 0.7(0.12.5) 95 (9496) 91 (8891) 0.2 (0.10.7)

411(361440)

Discussion
7 (58)

The results of our study indicate good internal consistency and reliability of the Serbian version of Epworth Sleepiness Scale (ESSs) which is comparable to that of other translations regardless of cultural and language differences. The ESS ranges for healthy subjects and for the clinical sample were comparable to findings of Johns et al. [1] as well as a study by Bloch [8]. Similarly to previous validation studies [813] done in other samples, the ESS score in the clinical sample was significantly higher when compared to normal subjects, and the ESS correlated well with the AHI. When examined separately, the difference was significant for all items, with an exception of the fifth item which had the highest mean value in the control group. This is in line with the previous study done in Greek population [9] and probably reflects the custom of taking an afternoon nap, which is often present in Mediterranean countries (siesta) [14]. The Cronbachs alpha was comparable to previously reported data [8, 11, 15], demonstrating good internal consistency. The removal of specific items did not increase the internal consistency. Testretest reliability was acceptable, indicating that the ESSs could reliably be used over time. The ESSs was discriminative of patients with sleep disorder breathing with a cut-off value of 9, demonstrating best sensitivity (71%) and specificity (87%). The values of 5 showed 96% sensitivity in detecting sleep disorder with the negative predictive value of 79%. Sleep apnea syndrome affects 2% of middle-aged women and 4% of middle-aged men [16]. The SAHS syndrome affects individuals on a daily basis by causing excessive daytime sleepiness and neurocognitive deficits [17, 18], and has an important impact on the development of cardiovascular diseases [19], stroke [20], and diabetes [21]. Previous studies demonstrated strong association

326 (241356) 391 (307466) 445 (368484) 441 (398472)

(4063) (19) (2427) (01.4) (9496) (8993) (00.4)

Insomnia

N=21

(5156) (45) (2328) (0.54) (9496) (8891) (0.14)

55 4 26 0.5 95 92 0.1

Primary snoring N=11

Central sleep apnea N=3

(3377) (0) (2330) (1766) (8395) (6786) (297)

54 5 24 1.3 94 89 0.3

Table 1 Patients and normal subjects characteristics

Obstructive sleep apnea N=70

(4258) (16) (2734) (1858) (8593) (6784) (786)

42 0 25 22 93 85 5

Age (years), median, IQR Gender (F), n (%) BMI (kg/m2), median, IQR AHI (per hour), median, IQR Average SaO2, median, IQR Lowest SaO2(%), median, IQR Percentage of time with Sao2 less than 90% (s) median, IQR Total sleep time (min), median, IQR ESS, median, IQR

52 11 30 30 91 80 25

12 (815)

7 (217)

6 (511)

5 (38)

778 Table 3 Item analysis of the Serbian version of ESS Item number Patients, n=112 MeanSD 1 2 3 4 5 6 7 8 1.40.9 1.80.8 0.80.9 1.60.9 1.71 0.50.8 1.50.7 0.60.9 10.05.2 Cronbachs alpha 0.86 0.86 0.87 0.87 0.87 0.87 0.86 0.86 0.88

Sleep Breath (2011) 15:775780 Normal subjects, n=111 MeanSD 0.620.77 1.120.98 0.450.75 0.720.91 1.501.07 0.090.32 0.490.77 0.040.23 5.03.65 Cronbachs alpha 0.66 0.65 0.69 0.72 0.71 0.70 0.69 0.72 0.72

between obstructive sleep apnea and motor vehicle accidents [6, 22]. Over the past decades, sleep medicine has been rapidly evolving in developed countries, however, the advance of sleep medicine in low-income and in-transition countries is hampered by lack of education and trained specialists in the field. Also, the lack of awareness by the healthcare providers is one of the main causes that majority of patients remain undiagnosed and untreated. We believe that the translation of Epworth Sleepiness Scale is one of the important steps that could help improve sleep medicine in this part of the world.

This study has several limitations. The study groups were unbalanced in terms of age and gender. This was due to a fact that the majority of referred patients were middleaged men, while the controls were healthy hospital staff, mostly female nurses. However, this was unlikely to influence the results since there was no association between age, gender, and ESSs scores in the control group. Some studies [23, 24] suggested that socioeconomic status could influence daytime sleepiness, but majority of validation studies failed to account for this. In our study, the detailed data on socioeconomic status were not routinely collected. The healthy controls did not have polysomnography performed; nevertheless, control group criteria excluded patients with known comorbidities and sleep impairment. As in previous validation studies, the testretest was determined solely in healthy controls and should be tested in patients with sleep disorders as well. Finally, no other test measuring sleep propensity was available for concurrent validity. The advantages of ESS include simplicity and a good performance in assessing daily sleep propensity, in contrast to other tests such as the Multiple Sleep Latency Test or the Maintenance of Wakefulness Test that are more costly and time-consuming. In conclusion, the Serbian version of the ESS demonstrated good internal consistency and reproducibility despite cultural, social, and language differences. The easily administrable ESSs could be used for assessment of daytime sleepiness in the local population and is a valuable tool in everyday clinical practice and research.

Acknowledgments MK and IK designed the research and drafted the manuscript. SP, MD, and MI collected the data. MK and IK analyzed the data, and NT and VK revised the manuscript. Fig. 1 Receiver operating characteristics curve (ROC) of the Serbian version of the Epworth Sleepiness Scale (ESSs) in detecting patients with AHI>5 ROC=0.85 Declaration of interest The authors declare that they have no conflict of interest.

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Appendix

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