The influence of shift work on cognitive functions and oxidative stress

Psychiatry Research 210 (2013) 1219–1225

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The influence of shift work on cognitive functions and oxidative stress Pınar Güzel Özdemir a, Yavuz Selvi b,n, Halil Özkol c, Adem Aydın a, Yasin Tülüce c, Murat Boysan d, Lütfullah Beşiroğlu e a

Yuzuncu Yil University, Faculty of Medicine, Department of Psychiatry, Van, Turkey Department of Psychiatry, SUSAB (Neuroscience Research Unit), Konya, Turkey c Yuzuncu Yil University, Faculty of Medicine, Department of Medical Biology, Van, Turkey d Yuzuncu Yil University, Faculty of Science and Arts, Department of Psychology, Van, Turkey e Katip Celebi University, Faculty of Medicine, Department of Psychiatry, İzmir, Turkey b

art ic l e i nf o

a b s t r a c t

Article history: Received 7 January 2013 Received in revised form 12 June 2013 Accepted 19 September 2013

Shift work influences health, performance, activity, and social relationships, and it causes impairment in cognitive functions. In this study, we investigated the effects of shift work on participants' cognitive functions in terms of memory, attention, and learning, and we measured the effects on oxidative stress. Additionally, we investigated whether there were significant relationships between cognitive functions and whole blood oxidant/antioxidant status of participants. A total of 90 health care workers participated in the study, of whom 45 subjects were night-shift workers. Neuropsychological tests were administered to the participants to assess cognitive function, and blood samples were taken to detect total antioxidant capacity and total oxidant status at 08:00. Differences in anxiety, depression, and chronotype characteristics between shift work groups were not significant. Shift workers achieved significantly lower scores on verbal memory, attention–concentration, and the digit span forward sub-scales of the Wechsler Memory Scale-Revised (WMS-R), as well as on the immediate memory and total learning subscales of the Auditory Verbal Learning Test (AVLT). Oxidative stress parameters were significantly associated with some types of cognitive function, including attention–concentration, recognition, and long-term memory. These findings suggest that night shift work may result in significantly poorer cognitive performance, particularly working memory. & 2013 Elsevier Ireland Ltd. All rights reserved.

Keywords: Antioxidants Cognitive performance Chronobiology Night shift Psychopathology Sleep deprivation

1. Introduction Shift work is an employment schedule designed to maintain service or production through 24 h in the day during the whole week (Pati et al., 2002). Employees assigned into shift groups can alternate across early morning, afternoon or night shifts. Over the last several decades, various conditions in work life such as technological improvement, competitive environments, and social conditions of workers, as well as necessity for service continuation, resulted in a rapid increase in the number of shift workers in labor markets all over the world (Almondes and Araujo, 2009). Hospitals are among the institutions in which the work shift schedules have been widely adopted in order to maintain service day and night (Josten et al., 2003). Shift work has been associated with a number of health problems that have biological, psychological, and sociological aspects. Researchers have shown that shift work leads to negative physiological and psychological outcomes caused by disturbances

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0165-1781/$ - see front matter & 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psychres.2013.09.022

in the biological rhythm. These problems can be listed as immune system disorders, metabolic disturbances, gastrointestinal symptoms, and cardiovascular diseases (Knutsson, 2003; Blachowicz and Letizia, 2006). Shift work also seems to be a potential risk factor for increased psychiatric morbidity such as somatization, anxiety, interpersonal sensitivity, and low quality of life among health workers (Selvi et al., 2010). There is evidence in the literature of the physiological and psychological effects of shift work, including sleep disorders, health problems, disruption to biological rhythm, reduced work efficiency, job dissatisfaction, and social isolation. These effects in a hospital setting can easily be predicted to lead to decreased quality of care and ultimately to higher health care costs (AbuAlRub, 2004; Berger and Hobbs, 2006). Although night-shift work is not rare among healthcare workers, night work is associated with difficulties in performing routine tasks, poor performance, and increased accidents and injuries (Admi et al., 2008). Shift work among hospital nurses is particularly related to shift-work disruption because the shifts change from on to off frequently, and most night shift nurses return immediately to day-activity. Shift working nurses in four hospitals reported being excessively sleepy (Suzuki et al., 2005). In addition,

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night-shift work accompanied by extended working time was found to be associated with an increased risk of patient mortality in hospitals (Trinkoff et al., 2011). There are significant associations between neurocognitive deficits and night shift work due to greater losses in total sleep time, sleepiness, and fatigue after working all night (Akerstedt and Wright, 2009; Selvi et al., 2010). Possible mechanisms playing a role in the adverse effects of shift work on cognitive functions have been increasingly recognized. Research has consistently evidenced that sleep deprivation resulting from night shift work seems to be central to the adverse effects in executive functions, attention processes, and working memory (Harrison and Horne, 2000a, 2000b; Kim et al., 2001; Drummond et al., 2001). It has been also demonstrated that sleep-deprived subjects are more prone to underestimate their level of cognitive impairment, whereas individuals in general may overestimate the consequences of deprivation while being only minimally impaired on attention tasks (Dinges et al., 1997; Leproult et al., 2003). Oxidative stress (OS) refers to an imbalance between the systemic secretion of reactive oxygen species and a biological system's ability to detoxify itself or to repair the resulting cell damage through the production of peroxides and free radicals (Punchard and Kelly, 1996). In humans, the brain and neurons are particularly vulnerable to radical-mediated damage (Cui et al., 2004). Reactive oxygen species (ROS) are produced in metabolic and physiological processes, and harmful oxidative reactions may occur in organisms that cannot remove ROS via enzymatic and nonenzymatic antioxidative mechanisms. If the production of free ROS exceeds the system's total antioxidant capacity, then OS occurs (Roenneberg, 2003). OS is known leading to several acute and chronic disorders. It has been well-documented that free oxygen radicals increase in psychiatric disorders such as panic disorder, schizophrenia, and depression, whereas antioxidants such as superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase decrease concomitantly (Ng et al., 2008; Wood et al., 2009). Sleep is central to renovation of the antioxidant defense system. OS resulting from a lack of sleep plays a pivotal role in the development of immune system disorders that have higher prevalence in shift workers (Sharifian et al., 2005). The relationship between insomnia and OS seems to be bidirectional: OS might cause insomnia, and, in turn, insomnia might further accelerate OS (Gulec et al., 2012). This study was designed to investigate the effects of working night shifts on total antioxidant (TAC) and oxidant capacity and to evaluate the correlations between neuropsychological test performance following shifts and the examined variables for each type of working schedule.

2. Methods 2.1. Participants and study design Participants were 90 health care workers, of whom 45 were daytime workers, working at Yüzüncü Yıl University Education and Research Hospital. Inclusion criteria for the study were as follows: not being pregnant, not being under 18 or above 65 years old, not having a history of substance abuse or dependence, no use of medicine for any psychiatric disorders, and having been working in the facility for at least one year. Daytime workers were recruited from the volunteer health workers and nurses who worked during the daytime, and shift workers were selected from health workers and nurses who consistently rotated between 08:00–16:00 and 16:00– 08:00 shifts for 3-week intervals. Individuals who worked during the day shifts or the night shifts were determined by hospital management. Shift workers were selected from employees who volunteered and whose conditions were appropriate for working rotating shifts. Participants in the night shift group were at work during 08:00–16:00 for 3 weeks and then switched to 16:00–08:00 shifts for 3 weeks. Individuals in the night shift group worked 3 days a week and participants in the daytime group worked 5 days a week. All subjects in the shift work group had been on the night schedule for 2 weeks at the time of assessment.

Neuropsychological tests were administered to participants by a clinical psychologist at 08:00. This time was deliberately selected for assessing cognitive performance to assess the possible influence of sleep deprivation caused by night shift work as compared to daytime workers, who were assumed to have an ordinary sleep pattern. We primarily investigated differences in cognitive performance and oxidative stress, and the relations between these variables in the group of night-shift workers after the shift probably emerged because of sleep deprivation. Shift workers completed the neuropsychological tests after the night shift, and daytime workers were administered the tests at the start of their work day. The Wechsler Memory Scale, Auditory-Verbal Learning Test, and Stroop Test were administered to the participants to assess cognitive functioning. Each testing session took an average of 45 min. After the assessment, blood samples were obtained with a hemogram tube to identify total antioxidant capacity (TAC) and total oxidant status (TOS). To evaluate the TAC and TOS, the blood samples were stored at  80 1C in the freezer. The study protocol received approval from the Ethics Committee of the Faculty of Medicine, Yüzüncü Yıl University. All participants gave written informed consent after receiving a complete description of the study protocol. The subjects were not paid for their participation.

2.2. Blood sampling and testing Blood samples were collected in order to determine TAC, TOS, and OSI. Between 08:00 and 09:00, 2-ml samples of venous blood were taken from each participant and placed into tubes with ethylenediaminetetraacetic acid. The samples were kept in a cool box, at þ 4 1C, until they were transferred to the laboratory of the Medical Biology Department. The biochemical analyses were performed under the same conditions after preparation of all blood samples. Whole blood samples obtained from each subject were hemolyzed with deionized water. After centrifugation (4000  g for 10 min at þ 4 1C), the pellet was discarded to eliminate cellular debris and the upper supernatant fluid was separated. The supernatant hemolysate was decanted into a clean tube. OS biomarkers (TAC and TOS) in the clear supernatant used for the analysis were measured at this stage. All processes were carried out at þ 4 1C. TOS levels were determined spectrophotometrically (Genesys 10 UV Scanning UV/vis Spectrophotometer) at 530 nm using kits (Erel, 2005). In this new colorimetric method, oxidants presented in the sample oxidize the ferrous ion-odianisidine complex, yielding ferric ion. The oxidation reaction is enhanced by the presence of excess glycerol in the reaction medium. The ferric ion and xylenol orange generate a colored complex. The results are given as micromolar hydrogen peroxide equivalents per liter (mmol H2O2 Equiv./L). TAC levels were measured spectrophotometrically (Genesys 10 UV Scanning UV/vis Spectrophotometer) at 660 nm using kits (Erel, 2004). This method is based on the bleaching of the distinct color of the 2,2′-azino-bis [3-ethylbenzothiazoline6-sulfonic acid] (ABTS) radical cation via the action of antioxidants. The precision of this assay is accurate (lower than 3% error rate). The results are expressed as mmol Trolox Equiv./L. The OSI was used to detect OS. OSI is defined as the ratio of the TOS level to TAC level (Aycicek et al., 2005). Specifically, OSI (arbitrary unit)¼ TOS (mmol H2O2 Equiv./L)/ TAC (mmol Trolox Equiv./L). The unit is arbitrary unit (AU).

2.3. Assessment instruments A sociodemographic questionnaire was developed for this study to assess age, gender, marital status, level of education, years of work, shift-work type, medical history, and family history of psychiatric illness. The Beck Depression Inventory (BDI) is a self-report inventory that measures the severity of the somatic, emotional, cognitive, and motivational symptoms in depression (Beck et al., 1979). The BDI, which includes 21 items, is scored between 0 and 3 for each item. The maximum BDI score is 63 and the minimum score is 0. Total scores of 17 and above indicate possible depression. The BDI was adapted to Turkish by Hisli (1989). The Beck Anxiety Inventory (BAI) is a self-report inventory that measures the frequency of physiological and other symptoms of anxiety experienced during the previous week (Beck et al., 1988). The BAI has 21 items scored between 0 and 3. The items are summed to obtain a total score that can range from 0 to 63 in order to classify anxiety as mild, moderate, or severe. The BAI was translated into Turkish by Ulusoy et al. (1998). The Morningness-Eveningness Questionnaire (MEQ) consists of 19 items pertaining to habitual rising and bed times, preferred times of physical and mental performance, and subjective alertness after rising and before going to bed (Horne and Östberg, 1976). MEQ yields scores ranging from 16 to 86. The Turkish version of the MEQ revealed good psychometric properties (Agargun et al., 2007).

2.3.1. Neuropsychological tests All subjects were neuropsychologically assessed in a standard procedure by the same clinical psychologist. The clinical psychologist performed a battery of three different neuropsychological tests to all subjects with routinized procedures. These tests are identified below respectively.

P.G. Özdemir et al. / Psychiatry Research 210 (2013) 1219–1225 The Wechsler Memory Scale-Revised (WMS-R) is the final version in which edits were many in many aspects; this scale was first developed by Wechsler (1987) in 1945 (D'Elia et al., 1989). WMS-R is the most comprehensive and, from the psychometric perspective, the most advanced memory test. The test is administered individually with 13 subtests with a total of 21 points. In our study, we performed all subtests of WMS-R to determine attention–concentration, visual and verbal memory, delayed recall, mental control, and general memory of the subjects. The Auditory Verbal Learning Test (AVLT) measures different aspects of verbal memory components such as immediate, delayed and free recall, learning rate, retroactive interference, and recognition in adults. This test includes 15 unrelated words. These words are read to the subject at 1-s intervals, and the subject is then asked to repeat remembered words. This procedure aims to evaluate immediate memory and continuity of attention. In this way, learning ability of the subject is evaluated. If a test loses its validity for whatever reason, there is a second list of words available. In our study, we administered the second list at the end of the shifts in order to decrease the effect of learning. AVLT was originally developed by Rey (1964) and later modified by authors from several countries, where the test has been recognized as a useful tool for diagnosing memory disturbances. The study of the Turkish validity and reliability of the AVLT was done by Öktem (1992). The Stroop Color-Word Interference Test-TBAG Form (SCWT) was developed by Stroop in 1935 as an experiment task (Stroop, 1935). This test assesses response inhibition and measures the ability to shift perceptual the set in accordance with changing demands. It also measures inhibition of habitual behavior patterns and behaving in an unusual manner. The Stroop test also assesses the informationprocessing rate, the parallel processing of attended and non-attended stimuli, and

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attention (Spreen and Strauss, 1991). This test was adapted and standardized for the Turkish population by MacLeod (1992). 2.4. Statistical analysis First, descriptive statistics were computed. Comparisons of cognitive functions between participants who were in the daytime work group and in the shift work group were run with the use of analysis of variance. With respect to effect size, eta values were computed. The statistical significance threshold was held at p o 0.05.

3. Results The average age of the 90 participants was 27.59 74.41 years. The gender distribution was 44 males and 46 females. The level of education was as follows: elementary (4.4%; n ¼4), secondary (25.6%, n ¼23), and university (70.0%, n¼ 63) education. Approximately half of the sample was single (52.22%, n ¼47); the other half of the sample was married (43.33%, n ¼39), and a small proportion of the participants were widowed (2.22%, n ¼2) or divorced (2.22%, n ¼2). The working duration of participants was 5.5 74.06 years.

Table 1 Comparisons of depression, anxiety and chronotypical characteristics between groups. Groups Day shift

Beck Depression Inventory Beck Anxiety Inventory Morningness-Eveningness Questionnaire

Night shift

Mean

S.D.

Mean

S.D.

F (1, 88)

P

η2

10.71 10.56 49.38

6.89 8.42 8.21

11.11 13.20 51.18

8.80 11.60 8.71

0.058 1.532 1.018

0.811 0.219 0.316

0.001 0.017 0.011

P values are indicated in italic type and significant P values are indicated in bold italic type.

Table 2 Comparison of cognitive functions between work shift groups with analysis of variance. Groups Day shift

Night shift P

η

4.046 0.001 7.223 0.071 3.692 5.359 0.752 3.903 2.290

0.047 0.981ns 0.009 0.791ns 0.058ns 0.023 0.388ns 0.051ns 0.134ns

0.21 0.01 0.28 0.03 0.20 0.24 0.09 0.21 0.16

1.61 10.64 0.53 1.40 1.33 0.30 0.39 1.97 0.62

7.038 6.876 0.538 2.410 2.064 1.000 9.514 12.263 0.732

0.009 0.010 0.465ns 0.124ns 0.154ns 0.320ns 0.003 0.001 0.395ns

0.27 0.27 0.08 0.16 0.15 0.11 0.31 0.35 0.09

7.48 1.57 1.31

0.271 3.282 0.026

0.604ns 0.073ns 0.871ns

0.06 0.19 0.02

Mean

S.D.

Mean

S.D.

The Wechsler Memory Scale-Revised Verbal memory Visual memory Attention/concentration Delayed recall Mental control Digit span forward Digit span backward Digit span total General memory performance

90.24 31.36 15.36 64.31 5.02 6.27 4.07 10.33 121.60

14.71 9.41 2.02 14.62 0.97 1.18 0.78 1.67 20.51

84.31 31.40 14.13 63.51 4.53 5.71 3.89 9.60 115.71

13.24 7.98 2.28 13.88 1.41 1.10 1.13 1.85 16.15

The Auditory Verbal Learning Test Immediate memory Total learning score The highest learning score Long term memory Recognition Total number of recall Consistency of recall Repeats Priority-recency effect

6.98 133.29 14.96 13.42 1.58 15.00 1.00 4.09 2.44

1.88 9.50 0.30 1.45 1.45 0.00 0.00 1.49 0.84

6.00 127.71 14.89 12.96 2.00 14.96 0.82 5.38 2.58

26.29 0.18 0.98

9.05 0.49 1.29

25.38 0.62 1.02

The Stroop Color Word Interference Test Stroop 5 duration Stroop 5 error Stroop 5 corrected response

P values are indicated in italic type and significant P values are indicated in bold italic type.

F (1, 88)

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The BDI, BAI, and MEQ scores were compared between day and night shift groups by using analysis of variance, and no significant differences between groups were found. Findings are presented in Table 1. Cognitive functions of the participants were assessed by the WMS-R, the AVLT and the Stroop Color Word Interference Test. Daytime work and shift work groups were compared by analysis of variance. Eta values were also computed. In the analyses, daytime working staff scored significantly higher in the verbal memory, attention–concentration, and the digit

span forward subscales of the WMS-R. The AVLT-immediate memory and AVLT-total learning score of the daytime-working staff were significantly higher than the shift-working staff. On the other hand, participants in the shift work group displayed significantly higher scores in the consistency of recall and the repeats subscales of the AVLT than participants in the daytime work group. No significant differences between the two groups were found in the Stroop Color Word Interference Test sub-scales. These results are listed in Table 2.

Table 3 Comparison of oxidative stress parameters between work shift groups with analysis of variance. Groups Day shift

Total oxidant status Total antioxidant capacity Oxidative stress index

Night shift

Mean

S.D.

Mean

S.D.

F (1, 88)

P

η2

158.50 20.83 0.78

34.45 3.81 0.22

166.75 20.14 0.88

28.49 4.72 0.24

1.534 0.580 3.908

0.219 0.448 0.051

0.017 0.007 0.043

P values are indicated in italic type and significant P values are indicated in bold italic type.

Fig. 1. Regression scatter plots for day shift group.

P.G. Özdemir et al. / Psychiatry Research 210 (2013) 1219–1225

We compared the TOS, TAC, and OSI between groups by the use of the analysis of variance. As given in Table 3, differences in the TOS and TAC between groups were not significant and the OSI is on the border of significance. To assess the relationships of cognitive function with TOS, TAC, and OSI, the Pearson product-moment correlation coefficients were computed within groups. For the daytime shift group, TOS was reversely associated with the Wechsler Digit Span total scale (r ¼  0.31, p o 0.05). The AVLT priority-recency effect scale scores positively linked to the TAC (r ¼0.32, p o 0.05) and negatively linked to the OSI (r ¼ 0.32, p o 0.05). Regression scatter plots are presented in Fig. 1. For the night shift group, TAC was significantly associated with the AVLT recognition scale (r ¼ 0.35, p o 0.05) and the Wechsler attention/concentration scales (r ¼ 0.30, p o 0.05), whereas TAC was reversely associated with the AVLT long-term memory scale scores (r ¼  0.37, p o 0.05). The OSI also linked to the AVLT long-term memory scale scores (r ¼0.30, p o 0.05) and the AVLT consistency of recall scale scores (r ¼ 0.31, p o 0.05). Regression scatter plots are presented in Fig. 2. We also computed Pearson product-moment correlation coefficients by groups between the Morningness-Eveningness Questionnaire and neuropsychological test scores. A negative correlation between the Stroop-5 corrected response scale and MEQ scores in the shift-work group was found. This can be interpreted as evening-type night shift workers achieving lower scores on the Stroop-5 corrected response scale (r ¼  0.38, p o 0.01). Correlations of TOS, TAC, and OSI with MEQ scores were also run by groups, and no significant linkages were found.

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4. Discussion In this study, our aim was to evaluate the effects of night shift work on cognitive functions in terms of attention, memory, learning, and remembering, and to investigate the associations between cognitive functions and oxidative stress parameters by groups of shift and non-shift workers in hospital. The study is a preliminary one that addresses both cognitive functions and oxidative parameters together among night shift workers. Additionally, workers' anxiety, depression, and chronobiological characteristics were assessed. No significant differences between groups were found in depression, anxiety, or chronobiological characteristics of the participants. Differences between groups were also not significant in OS parameters. However, there were significant differences in cognitive functioning between groups. Few studies have examined the influence of chronotype on the ability to cope with shift work schedules, but the results were not unequivocal. A study conducted in a sample of nurses found that evening-type participants were more likely to report sleep problems in the day shift, but there were no substantial effects of chronotype on sleep quality in the night shift (Newey and Hood, 2004). Another study investigating the relationships between OS and chronotypes suggested that differences between chronotypes in both oxidant and antioxidant levels were not significant (Selvi et al., 2011). In line with the previous studies, there were no significant deviations on the MEQ scores between the two groups. This may be because of the triweekly change of shift patterns among shift-working employees. Moreover, relations between oxidative stress parameters and morningness-eveningness scores were not significant in either group.

Fig. 2. Regression scatter plots for night shift group.

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Sharifian et al. (2005) noted that total plasma antioxidant capacities were lower in night-shift workers, and researchers emphasized that night shift can act as an oxidative stressor. However, Aytac et al. (2007) reported no significant effects of 24-h sleep deprivation on oxidant and antioxidant levels in a sample of nurses. As seen in the literature, there have been mixed findings concerning the connection between OS and shift work. In these studies, duration of shift work was not controlled and inconsistent results may be related to variation in the longevity of working shifts. In the current study, findings were partially compatible with the previous studies in the night shift work group did not significantly display oxidative distress indicated by the TOS, TAC, and OSI. Notably, the significance level for the OSI was very close to the critical value, and unsubstantial differences between the groups seem to be related to inadequate sample size. Although a number of studies have reported a variety of adverse biological, psychological, and social outcomes of night-shift work and other atypical work schedules among employees, very few studies have systematically investigated the effects of night- and day-shift work on alertness and cognitive performance. Research has consistently evidenced that sleep deprivation is significantly associated with deteriorations in memory performance (Harrison and Horne, 2000b; Pilcher and Huffcutt, 1996). Sleep deprivation was found to be significantly associated with verbal memory deficits (Turner et al., 2007). Mu et al. (2005) showed that, in a neuroimaging study, sleep deprivation deficits were not predominantly caused by prefrontal cortex dysfunction, and the parietal cortex and other parts of the brain involving in verbal working memory exhibited vulnerability as well. The verbal memory scale of the WMS-R evaluates the ability to encode and store information in the verbal domain. Lower scores in the verbal memory domain represent poor functioning in information storage and retrieval deficits, related to working memory deficits to an extent. Consistent with the literature, night-shift individuals exhibited poorer performance compared to day-shift individuals. Digit span tests in the WMS combine two skills: repetition of digits in the same order as they are spoken by the tester, and repetition of digits in the reverse order. Poor performance on digit span scales is of unusual diagnostic significance, particularly for suspected brain dysfunction. Repetition of digits is especially revealing in individuals who have difficulty sustaining concentration during problem-solving, an important component of working memory. The scale also measures attention and concentration (Lichtenberger et al., 2002; Kaufman and Lichtenberger, 2006). The WMS-R subtests of digit span and attention/concentration scores of night-shift workers were significantly lower than day-shift workers. Negative effects of sleep deprivation on working memory (Chee and Choo, 2004; Chee et al., 2006; Chee and Chuah, 2008) and attention (Thomas et al., 2000; Drummond et al., 2001; Lim et al., 2007) have been well-elaborated. Machi et al. (2012) reported that short-term memory was the cognitive domain most likely to decline in emergency-center physicians during shift work. Sarıcaoglu et al. (2005) compared the effect of day- and nightshift working on the attention and anxiety levels of a group of anesthesia assistants. There were 15 day-shift and 18 night-shift residents who performed the Rey Auditory Verbal Learning Test, Visual, Aural Digit Span Test, and the State Trait Anxiety Inventory before and after shifts. This study revealed that following night shift, workers were more impaired on measures of cognitive functions. However, Petru et al. (2005) conducted a comparative study of 44 drivers, one group working permanently in the daytime and the other group working 1 week at night and 1 week in the daytime. This study did not find significant differences in terms of cognitive and psychomotor performance. The Rey Auditory Learning Scale is an instrument developed primarily to assess short-term memory skills. The immediate memory scale refers to the number of correct words said by the

subject in the first trial. Total learning score is the total number of correct words said by the subject in 10 trials. The repeats scale refers to the number of attempts required for the subject to be able to say precisely all of the words in the list. Consistency of recall refers to the consistency across trials. All these scales are good indicators of working memory (Teruya et al., 2009). AVLT is a test used in our study to investigate differences on verbal learning and memory performance among shift-work and non-shift-work participants. According to the results, immediate memory scores and total learning scores were significantly lower among night-shift workers compared to day-shift workers. Night shift workers needed more repetitions to learn the word list compared to the daytime workers. Moreover, scores of consistency on the recall scale among daytime workers were greater than night-shift workers. Consistency on recall of items includes forming meaningful connections between words and shows that the individual maintains the same learning strategy. It appeared from our study that sleep deprivation caused by night shift work significantly influenced working memory performance rather than long-term memory. In the present study, the correlations of OSI, TOS, and TAC parameters with cognitive functions were also assessed in both groups separately. In the day-shift group, TOS was reversely associated with the Wechsler digit span scale. The AVLT priority-recency effect subscale scores positively linked to TAC, and negatively linked to OSI. In the night-shift group, TAC was significantly associated with the AVLT recognition sub-scale and the Wechsler attention–concentration sub-scales; whereas TAC was reversely associated with the AVLT long-term memory and AVLT consistency of recall subscale scores. In particular, the negative association between TAC and longterm memory performance was quite striking, and needs further investigation. This seems to be a compensatory mechanism for sleep deprivation among night-shift workers. As we know, OS is important in the pathogenesis of Alzheimer's disease and cognitive decline (Liu et al., 2003). Nonetheless, OS remains a biologic hypothesis in the pathogenesis of cognitive decline; further research is needed to assess the compassing of oxidant capacity and antioxidant status and their roles in preventing cognitive decline. As far as we know, our study is a preliminary one, drawing attention to the correlation between circadian rhythm and cognitive functions related to shift work and OS. In addition, this research has some limitations. This study was conducted in a single center and the sample size was relatively small. We did not use a repeated-measure experimental design to assess changes in cognitive performance and OS parameters before and after the shifts. We assessed cognitive performance and oxidative stress at 08:00 to test the differences that emerged because of sleep deprivation by comparing to a control group working during the daytime. However, we made assessments at only one time point in the morning and did not make reassessments after the daytime work; this means that we have not controlled the possible effects of fatigue caused by working. We thought that if the participants worked at least 1 year, they would have adapted to the shift. Finally, we did not obtain information with sleep diaries, and the diet schedules of participants were not assessed, which may be confounding factors to an extent. Some variables including caffeine or tobacco use may impact performance on working memory tests; we did not control our analyses for these variables.

5. Conclusions As a result of our study, we found that cognitive functions of daytime healthcare workers were better than night-shift healthcare workers. The relationships between OS and cognitive process are still uncertain and open to interpretation among night-shift

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