Dataset Information

Sleep disturbance is associated with perturbations in immune-inflammatory pathways in oncology outpatients undergoing chemotherapy.

ABSTRACT:

Objective/background

Sleep disturbance is a common problem in patients receiving chemotherapy. Purpose was to evaluate for perturbations in immune-inflammatory pathways between oncology patients with low versus very high levels of sleep disturbance.

Patients/methods

Sleep disturbance was evaluated using the General Sleep Disturbance Scale six times over two cycles of chemotherapy. Latent profile analysis was used to identify subgroups of patients with distinct sleep disturbance profiles. Pathway impact analyses were performed in two independent samples using gene expression data obtained from RNA sequencing (n = 198) and microarray (n = 162) technologies. Fisher's combined probability test was used to identify significantly perturbed pathways between Low versus Very High sleep disturbance classes.

Results

In the RNA sequencing and microarray samples, 59.1% and 51.9% of patients were in the Very High sleep disturbance class, respectively. Thirteen perturbed pathways were related to immune-inflammatory mechanisms (i.e., endocytosis, phagosome, antigen processing and presentation, natural killer cell mediated cytotoxicity, cytokine-cytokine receptor interaction, apoptosis, neutrophil extracellular trap formation, nucleotide-binding and oligomerization domain-like receptor signaling, Th17 cell differentiation, intestinal immune network for immunoglobulin A production, T-cell receptor signaling, complement and coagulation cascades, and tumor necrosis factor signaling).

Conclusions

First study to identify perturbations in immune-inflammatory pathways associated with very high levels of sleep disturbance in oncology outpatients. Findings suggest that complex immune-inflammatory interactions underlie sleep disturbance.

SUBMITTER: Calvo-Schimmel A

PROVIDER: S-EPMC11200329 | biostudies-literature | 2023 Jan

REPOSITORIES: biostudies-literature

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Publications

Sleep disturbance is associated with perturbations in immune-inflammatory pathways in oncology outpatients undergoing chemotherapy.

Calvo-Schimmel Alejandra A Kober Kord M KM Paul Steven M SM Cooper Bruce A BA Harris Carolyn C Shin Joosun J Hammer Marilyn J MJ Conley Yvette P YP Dokiparthi Vasuda V Olshen Adam A Levine Jon D JD Miaskowski Christine C

Sleep medicine 20221121

<h4>Objective/background</h4>Sleep disturbance is a common problem in patients receiving chemotherapy. Purpose was to evaluate for perturbations in immune-inflammatory pathways between oncology patients with low versus very high levels of sleep disturbance.<h4>Patients/methods</h4>Sleep disturbance was evaluated using the General Sleep Disturbance Scale six times over two cycles of chemotherapy. Latent profile analysis was used to identify subgroups of patients with distinct sleep disturbance pr ...[more]

PMID: 36470166

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Project description:BackgroundSleep disturbances, as manifested in insomnia symptoms of difficulties falling asleep or frequent nighttime awakenings, are a strong risk factor for a diverse range of diseases involving immunopathology. Low-grade systemic inflammation has been frequently found associated with sleep disturbances and may mechanistically contribute to increased disease risk. Effects of sleep disturbances on inflammation have been observed to be long lasting and remain after recovery sleep has been obtained, suggesting that sleep disturbances may not only affect inflammatory mediators, but also the so-called specialized pro-resolving mediators (SPMs) that actively resolve inflammation. The goal of this investigation was to test for the first time whether the omega-3 fatty acid-derived D- (RvD) and E-series (RvE) resolvins are impacted by prolonged experimental sleep disturbance (ESD).MethodsTwenty-four healthy participants (12 F, age 20-42 years) underwent two 19-day in-hospital protocols (ESD/control), separated by > 2 months. The ESD protocol consisted of repeated nights of short and disrupted sleep with intermittent nights of undisturbed sleep, followed by three nights of recovery sleep at the end of the protocol. Under the control sleep condition, participants had an undisturbed sleep opportunity of 8 h/night throughout the protocol. The D- and E-series resolvins were measured in plasma using liquid chromatography-tandem mass spectrometry (LC-MS/MS).ResultsThe precursor of the D-series resolvins, 17-HDHA, was downregulated in the ESD compared to the control sleep condition (p <.001 for condition), and this effect remained after the third night of recovery sleep has been obtained. This effect was also observed for the resolvins RvD3, RvD4, and RvD5 (p <.001 for condition), while RvD1 was higher in the ESD compared to the control sleep condition (p <.01 for condition) and RvD2 showed a mixed effect of a decrease during disturbed sleep followed by an increase during recovery sleep in the ESD condition (p <.001 for condition*day interaction). The precursor of E-series resolvins, 18-HEPE, was downregulated in the ESD compared to the control sleep condition (p <.01 for condition) and remained low after recovery sleep has been obtained. This effect of downregulation was also observed for RvE2 (p <.01 for condition), while there was no effect for RvE1 (p >.05 for condition or condition*day interaction). Sex-differential effects were found for two of the D-series resolvins, i.e., RvD2 and RvD4.ConclusionThis first investigation on the effects of experimental sleep disturbance on inflammatory resolution processes shows that SPMs, particularly resolvins of the D-series, are profoundly downregulated by sleep disturbances and remain downregulated after recovery sleep has been obtained, suggesting a longer lasting impact of sleep disturbances on these mediators. These findings also suggest that sleep disturbances contribute to the development and progression of a wide range of diseases characterized by immunopathology by interfering with processes that actively resolve inflammation. Pharmacological interventions aimed at promoting inflammatory resolution physiology may help to prevent future disease risk as a common consequence of sleep disturbances.Trial registrationClinicalTrials.gov NCT02484742.

Dataset Information

Sleep disturbance is associated with perturbations in immune-inflammatory pathways in oncology outpatients undergoing chemotherapy.

Objective/background

Patients/methods

Results

Conclusions

Publications

Sleep disturbance is associated with perturbations in immune-inflammatory pathways in oncology outpatients undergoing chemotherapy.

Similar Datasets

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