The influence of desynchronised circadian rhythm on emotional contagion and reactivity: A comparative study

INTRODUCTION

The impact of sleep deprivation on cognitive processes has sparked considerable interest owing to its comorbidity with various neurological, mood and psychiatric disorders.^[1] However, despite the growing prevalence of behavioural disturbances associated with sleep disruption, this area has received limited scientific attention.

Examining the effects of altered sleep patterns on neurological functions holds particular relevance for health-care professionals, as their ability to concentrate, maintain attention and regulate emotions is critical for optimal patient care.

Among the health-care workforce, nurses represent the largest contingent, accounting for approximately 50% of hospital personnel.^[2] It is worth noting that nurses who work night shifts endure sleep deprivation due to the extended duration of their work hours. Furthermore, the demanding nature of their professional responsibilities exposes them to physical and mental chronic stress.

These aforementioned factors render nurses particularly susceptible to sleep disruption, leading to adverse effects on their physical and emotional well-being. Involvement in shift work disrupts their circadian rhythms, further exacerbating the risk of physiological and psychological disturbances.^[3] Commensurately, these individuals are more prone to developing sleep disorders, experiencing daytime drowsiness and exhibiting reduced performance in their work. Moreover, the psychological stress generated within the occupational environment significantly impairs their overall quality of life.^[4]

There is evidence that sleep deprivation can affect memory, with emotional memory being more susceptible to disruption than neutral memory.^[5,6] This disparity likely stems from the crucial role of sleep in facilitating the long-term consolidation of emotional memory.^[7] Studies have demonstrated that sleep deprivation can engender heightened activity within the amygdala, specifically in response to negative stimuli, indicating a potential augmentation of the amygdala’s reactivity to negative emotions during sleep deprivation.^[8,9] However, other studies have shown that sleep deprivation can also lead to faster response times to positive stimuli, suggesting that the effects of sleep deprivation on emotional reactivity may be more complex.^[10]

Emotional contagion refers to the phenomenon where one person’s emotions and related behaviours can influence and spread to others within a social or interpersonal context.^[11] Partial sleep deprivation led to reduced activity in the fusiform gyrus when processing angry faces and lower ratings of happiness for all stimuli.^[12]

Working 12-h shifts has been associated with reduced empathy and heightened burnout, with females exhibiting higher rates of exhaustion-related burnout symptoms.^[13]

A study by Medic et al. explains that short-term disruption of sleep is associated with increased stress responsivity, somatic problems, reduced quality of life, emotional distress, mood disorders and other mental health problems, cognition, memory, and performance deficits, and behaviour problems in otherwise healthy individuals.^[14]

There is an apparent contradiction within the existing research. While it is widely accepted that sleep deprivation impairs physiological bodily processes, there is a dearth of definitive evidence in the literature regarding the specific impact of acute sleep deprivation on emotional reactivity. The conflicting nature of the data mandated the conduct of this study.

MATERIAL AND METHODS

1. Study design: A comparative study

2. Sampling technique: Purposive

3. Sample size estimation = 72

4. Sample size estimation - Expected reduction-(mean) = d = 13.4

   • SD = 48 = σ

   • Power = 80%

   • α error= 0.05;

   • One-sided Zα = 1.65 and β error = 0.2;

   • n = ([Zα + Zβ] σ/d²) = 71.64 = 72

5. Source of data: The study population included 72 (4^th year) nursing students aged 21–23 who worked night shifts (8 p.m.–8 a.m.) at KLE Hospital.

6. Inclusion and Exclusion Criteria for Experiment Group [Table 1].

   Table 1: Inclusion and exclusion criteria for experiment group

   (4th year) Nursing students doing night shifts (8 pm–8 am)	H/O prior sleep disorders
   Aged 21–23 years Both genders were recruited	Having H/O diabetes or other major illness H/O alcohol consumption or tobacco chewing
   At least 12 h of sleep deprivation.	H/O any psychiatric illness or any medication affecting sleep (e.g.- Cetirizine)

   H/O: History of

7. Exclusion Criteria for the control group [Table 2].

   Table 2: Exclusion criteria for the control group

   H/O daytime napping H/O social media addiction H/O habitual night-time phone use H/O gadget addiction H/O prior, sleep disorders and insomnia Having H/O diabetes or other major illness H/O alcohol consumption or tobacco chewing H/O any psychiatric illness or any medication affecting sleep (e.g.- Cetirizine)

   H/O: History of

8. Study Flow-chart [Figure 1].

   

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   Figure 1:

   Study flowchart. PSQI: Pittsburgh sleep quality index, SSS: Stanford sleepiness scale, HADS: Hospital anxiety and depression scale, HRV: Heart rate variability.

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The control population consisted of 72 age- and gender-matched day-shift working students.

RESULTS

The findings of our study demonstrate that female nurses with sleep deprivation (SD) have a lower overall sleep quality score (PSQI Global score: 12 ± 7.6) compared to daytime controls (7 ± 4.8). SD female nurses exhibit signs of sleepiness (3.66 ± 0.24), while SD male nurses show higher levels of anxiety (8 ± 1.1) on the HADS questionnaire compared to daytime controls. During the emotional contagion task for affective facial recognition, SD female nurses display heightened responses to negative emotions such as anger (4 ± 11.12) and fear (4.2 ± 9.0) compared to controls. They also show reduced responsiveness to positive emotions (happy) in SD (1.5 ± 11) compared to daytime controls (2.5 ± 10.2), whereas no significant changes are observed among male SD nurses and controls. When examining HRV in relation to negative emotions, specifically anger, SD female nurses exhibit lower parasympathetic activity (characterised by reduced RMSSD: 39 ± 7.0) compared to controls (51 ± 12.46), while no statistically significant differences are observed among male counterparts. Notably, there are no significant differences in emotions such as surprise and disgust between SD individuals and controls in both genders.

1. Sociodemographic details [Table 3]

   Table 3: Sociodemographic details.

   Age	• 21–23 years
   Gender	• Females (SD=44; Controls=44) and • Males (SD=28; Controls=28)
   Qualifications	• Nursing students doing shift work at KLE’s Hospital and Research Centre
   Hours of actual sleep (SLEEP LOG)	• Average 4–5 h of daytime sleep in shift workers (nurses) as compared to 8 hours of night-time sleep in the control population working in day hours.
   Substance abuse such as smoking and alcohol	• Neither population
   History of endocrine disorders.	• Nil

   SD: Sleep deprived, KLE: Karnataka Lingayat Education Society

2. Comparison of sleep indices using the PSQI questionnaire among shift workers and controls – [Table 4]

   Table 4: Comparison of sleep indices using PSQI questionnaire among shift workers and controls.

   PSQI	SD females (n=44)	SD males (n=28)	Control females (n=44)	Control males (n=28)	P-value
   Subjective sleep quality	1.8±8	1.5±6	2±7.9	1±0.8	0.01*
   Sleep latency	2.8±12	2.4±2.5	1.2±10	1.3±2	0.7
   Sleep duration	2±6.7	1.6±7.2	1.8±5.5	0.9±1.1	0.78
   Sleep efficiency	2.8±6.5	1.99±3	1.5±4.3	1.33±5	0.5
   Sleep disturbances	2.2±7.9	2±4.3	0.8±7.7	0.63±4.4	0.2
   Daytime disturbances	2±2.3	1.85±2.11	1.1±3.11	1±2.33	0.1
   Global score	12±7.6	12.34±5.4	7±4.8	7.24±6	0.04*

   *Statistically significant, P<0.05, SD: Sleep deprived, PSQI: Pittsburgh Sleep Quality Index

3. Comparison of sleepiness using SSS in sleep-deprived females and males – [Graph 1]

   

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   Graph 1:

   Comparison of sleepiness using Stanford sleepiness scale in SD females and males. *Statistically significant, P < 0.05 (SD: Sleep deprived, C: Control).

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4. Comparison of anxiety and depression among sleep-deprived and control groups – [Graph 2]

   

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   Graph 2:

   Comparison of anxiety and depression among SD and controls. *Statistically significant, P < 0.05. The data are in mean with standard deviation. (HADS: Hospital anxiety and depression scale, SD: Sleep deprived, C: Control).

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5. Comparison of autonomic reactivity among sleep-deprived and controls – [Graph 3]

   

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   Graph 3:

   Comparison of autonomic reactivity among sleep deprived and controls. The test used to determine P-value is student t-test. *Statistically significant, P < 0.05 (HRV: Heart rate variability, RMSSD: Root mean square of the successive differences, SD: Sleep deprived, C: Controls).

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6. Comparison of emotional reactivity (arousal) and vagal outflow (RMSSD) using facial affective tasks among sleep-deprived and controls (Females) – [Table 5]

   Table 5: Comparison of emotional reactivity (arousal) and vagal outflow (RMSSD) using facial affective task among SD and Cs (females).

   Emotional reactivity	Females SD	Females C	P-value
   1) Happy	1.5±11	2.5±10.2	0.002*
   RMSSD	56±4.32	50±4.32	0.01*
   2) Sad	2±7.4	3.2±6.7	0.04*
   RMSSD	48±8.89	49±1.76	0.12
   3) Fear	4.2±9.0	3.1±7.7	0.05*
   RMSSD	41±7.18	51±1.21	0.01*
   4) Disgust	3±13	3.2±12.8	0.2
   RMSSD	48±4.45	49±3.12	0.9
   5) Surprise	3±12.9	2.8±9.7	0.1
   RMSSD	47±5.61	50±4.32	0.7
   6) Anger	4±11.12	3±11.9	0.001*
   RMSSD	39±7.0	51±12.46	0.05*

   *Statistically significant, P<0.05, RMSSD: Root mean square of the successive differences, SD: Sleep deprived, C: Controls

7. Comparison of emotional reactivity (arousal) and vagal outflow (RMSSD) using facial affective tasks among sleep-deprived and controls (Males) – [Table 6].

   Table 6: Comparison of emotional reactivity (arousal) and vagal outflow (RMSSD) using facial affective tasks among sleep deprived and controls (males).

   Emotional reactivity	Males SD	Males C	P-value
   1) Happy	2.8±8.1	3±6.7	1.112
   RMSSD	54±18.23	60±17.9	0.875
   2) Sad	2±11.3	2.8±14.9	0.7
   RMSSD	56±11.15	58±12	0.12
   3) Fear	3.2±5.5	2.3±5.7	0.9
   RMSSD	56±13.41	57±11.3	0.5
   4) Disgust	2.5±9.8	2.8±3.6	0.2
   RMSSD	58±13.11	59±12.7	0.4
   5) Surprise	2.4±22	2.8±25	0.1
   RMSSD	53±15.17	59±16.71	0.1
   6) Anger	2.4±4.8	2.7±5.9	0.11
   RMSSD	53±14.8	54±15.32	0.9

   RMSSD: Root mean square of the successive differences, SD: Sleep deprived, C: Controls, Statistically significant P = <0.05.

DISCUSSION

In our study, the mean age of the participants was 22 years, and the shift work duration was 12 h.

The results of the PSQI showed that 67% of the nurses had poor sleep quality (global score 12, subcomponent scores around 2). A study by Gómez-García et al. in Spain reported a deteriorated PSQI score in nurses with night shifts compared to nurses with day shifts, indicating deteriorated sleep quality among night shift workers.^[19] As part of the health-care system, where shift work is a necessary hazard, nursing staff experience sleepiness and discomfort in their work environment. This reduces the quality of healthcare delivery to patients and increases the risk of occupational errors.

The results of our SSS showed that female nurses had a slightly lower score (3.16 ± 0.24) than male nurses (3.66 ± 0.50). Although this difference was not statistically significant, this could be due to the greater sensitivity of female psychological status to stress.^[20]

The results of the HADS questionnaire showed that female shift workers had significantly higher anxiety levels (8 ± 1.1) than controls (6.73 ± 0.16). However, no gender differences were found for depression. Our nursing staff was relatively young, and they may have been more anxious because they had not yet developed coping strategies. The unpredictability of the work schedule and the seriousness of the patients’ conditions may also have been contributing factors.

Our findings also revealed blunted vagal outflow as indicated by the RMSSD values. Sleep deprivation leads to a decrease in vagal innervation activity and an increase in sympathetic activity. Goff et al. have provided an explanation for this phenomenon, stating that the body’s regulatory mechanisms are designed to prevent sudden surges in sympathetic activity during the waking state. However, sleep deprivation disrupts this regulatory balance and results in greater fluctuations in autonomic activity.^[21]

The AFRT results showed that nurses engaged in night shifts exhibited heightened arousal for negative valence emotions, such as anger (4 ± 13.1) and fear (4.2 ± 9.0). These results are consistent with studies that have shown that sleep deprivation, with <5 h of sleep per night, increases emotional disturbance.^[22]

In line with our results, a study conducted by Bauducco et al. discovered that adolescents who obtained inadequate amounts of sleep were more prone to engaging in norm-breaking behaviour, as well as displaying increased hostility and anger.^[23] This further supports the notion that compromised sleep duration has detrimental effects on emotional regulation and behavioural functioning.

Studies have shown that sleep deprivation can lead to increased amygdala activity in response to both negative and positive stimuli.^[24] This is because sleep deprivation weakens the connectivity between the amygdala and prefrontal areas of the brain, including the medial prefrontal cortex. This disruption can lead to hyperactivity toward emotional stimuli and a decrease in the ability to regulate emotional responses.^[25]

Even a single episode of total sleep deprivation has been linked with greater subjective reports of anxiety, anger and stress in response to mildly stressful situations. This is likely because the amygdala is involved in both emotions and sleep architecture. When the amygdala is hyperactive, it can lead to heightened responses to negative stimuli, even when those stimuli are not particularly threatening.

By weakening the connectivity between the amygdala and prefrontal cortex, sleep deprivation can lead to increased reactivity to emotional stimuli and a decrease in the ability to regulate emotional responses, resulting in negative consequences, including increased anxiety, anger and stress.

CONCLUSION

Our study found that even a solitary episode of acute sleep deprivation manifested as deteriorated sleep patterns in sleep workers. Female shift workers were more likely to experience anxiety than their male counterparts.

The subjects showed heightened emotional reactivity to negative valence emotions, such as anger and fear. Besides, they exhibited blunted emotional reactivity to positive valence emotions, such as happiness and sadness. There was no significant change in response to neutral valence emotions, such as surprise or disgust.

The HRV measurements suggested that even sleep deprivation can lead to sympathetic overactivity. This is consistent with previous research that has shown that sleep deprivation can lead to sympathetic overactivity.