Poor sleep quality

Is poor sleep quality associated with poor neurocognitive outcome in cancer survivors? A systematic review

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Abstract

Purpose

Cancer-related neurocognitive impairment and poor sleep are prevalent in cancer survivors and have a negative impact on their quality of life. This systematic review studies the association between sleep disturbance and neurocognitive functioning, as well as the potential positive effects of sleep interventions on neurocognitive functioning in cancer survivors. In addition, we aimed at determining the potential positive effects of sleep interventions on neurocognitive functioning in this population.

Methods

Following PRISMA guidelines for reporting systematic reviews and meta-analyses, a comprehensive PubMed, Embase, PsycINFO, and CINAHL search was performed. Inclusion criteria were adult cancer survivors, self-reported or objective measures of neurocognitive functioning and sleep quality, or reports on the association between sleep and neurocognitive functioning.

Results

Of the 4,547 records retrieved, 17 studies were retained for this review. Twelve studies were correlational, and five reported on interventions aimed at improving sleep quality. All studies that included self-reported neurocognitive functioning found that poorer sleep was associated with worse neurocognitive functioning. In four out of eight studies, poorer sleep was associated with objective neurocognitive impairment. Three out of five interventional studies showed neurocognitive functioning improved with improved sleep.

Conclusions

While poor sleep in cancer survivors is associated with self-reported neurocognitive impairment, the association between poor sleep and objective neurocognitive impairment is less evident.

Implications for Cancer Survivors

It is important that care providers are aware of the association between sleep and neurocognitive functioning and that improving sleep quality can be a way to decrease neurocognitive impairment in cancer survivors.

Discussion

This review aimed at examining the association between sleep and neurocognitive functioning in cancer survivors. Multiple factors contribute to the development of sleep disturbances in cancer patients and survivors, such as neurotoxicity of the treatment, pain, and psychological symptoms [4, 55]. These factors are also associated with neurocognitive impairment, implying a possible relationship between sleep and neurocognitive functioning in cancer survivors as well. This is also in line with a survey among cancer survivors, where chemotherapy was strongly associated with lower self-reported neurocognitive functioning and more self-reported sleep difficulties [1].

We found limited evidence that in cancer survivors, sleep quality and quantity are associated with objective neurocognitive functioning (oNCF). Verbal memory/functioning seemed strongest associated with sleep disturbances, with one study suggesting that increased sleep duration is associated with better verbal functioning [37] and another study concluding that cancer survivors with insomnia performed worse on verbal episodic memory when compared to survivors who were good sleepers [34]. One out of three studies investigating the correlation between PSQI score and neuropsychological test performance found a significant correlation with the domains of learning, memory, attention, and executive function [43]. It is not clear why these correlations were not found in the other two studies, but an explanation might be that these studies used a less extensive test battery than the study by Van Dyk [43]. Also, these studies used the separate standardized test scores as a measure of oNCF instead of domain scores. In other populations (self-reported), sleep quality is also associated with oNCF; although similar to cancer research, there is great variability in the tests that are used [56, 57]. One recent study found that in memory clinic patients, only objective sleep measurements, and not self-reported, were associated with oNCF [58]. Unfortunately, only one of the included studies used an accelerometer, and this study found no association between oNCF and sleep [35].

Overall, there was heterogeneity of the neuropsychological tests used in the different papers, making it difficult to compare outcome measures. Furthermore, some studies used just a small number of tests, while others used an elaborate test battery. If only specific neurocognitive domains are impacted by sleep disturbances, a summarized score might not be sensitive enough. Further research is necessary to be able to confirm the association with the domains reported in this review.

All studies with self-reported neurocognitive functioning (sr-NCF) as an outcome measure were evidential for a positive association between sleep disturbances and self-reported neurocognitive impairment. Studies comparing cancer survivors with and without insomnia found evidence that insomnia was associated with poorer sr-NCF [34, 39, 41]. It is not possible to identify which other sleep-related factors are specifically associated with sr-NCF, since some studies used total scores of the PSQI, while others also reported subscales. Overall, the findings suggest that improving sleep quality could be a way to decrease sr-NCF.

The finding that poor sleep seems mostly associated with self-reported and not objective neurocognitive impairment might indicate that instead of causing neurocognitive impairment, sleep is associated with the impression that a patient has neurocognitive impairment. This is similar to findings in other patient groups and healthy populations [59, 60]. Previous research has shown that sr-NCF is also associated with symptoms of anxiety depression, quality of life, and fatigue [61, 62]. It has been shown that sleep and sr-NCF are part of a psychological symptom cluster in oncological patients [63]. It is likely that poor sleep increases fatigue and sr-NCF, while symptoms of anxiety and depression can lead to poorer sleep. This would also suggest that interventions aimed at improving sleep could benefit the whole symptom cluster.

The studies included in this review suggest that sleep interventions might indeed improve sr-NCF, but more research is needed. One study that found an effect of treatments targeting sleep problems used the self-reported neurocognitive functioning scale of the EORTC QLQ-C30 as an outcome measure. This scale consists of (only) two questions, one regarding memory and one regarding concentration. Although the improvement on this scale is encouraging, it would still be important to study the effect of sleep interventions on sr-NCF with more extensive outcome measures. Furthermore, the interventions in all five studies were all very different. More research is necessary before we can conclude whether these interventions could be effective in decreasing sr-NCF. Future interventional sleep studies are recommended to include at least a measure of sr-NCF.

To make future studies more comparable, it is recommended that they use similar measures for NCF and sleep. To measure oNCF, it is generally recommended to use the test battery from the International Cognition and Cancer Task Force, potentially supplemented by other tests [64]. The tests in this battery have been specifically selected for their ability to measure oNCF in cancer. However, since most studies found no association between sleep and performance on these tests, it is important to continue research into which tests could be more sensitive to detect possible oNCF changes associated with sleep in cancer survivors at all.

In terms of measuring sr-NCF, the neurocognitive functioning scale of the EORTC QLQ-C30 is sufficient to indicate whether a patient reports complaints. Nevertheless, to describe change over time or the effect of treatment, a more elaborate questionnaire such as the FACT-Cog might be more suitable to be able to specify which sleep factors are most strongly associated with sr-NCF. The Pittsburgh Sleep Quality Index was the most frequently used measure of sleep. The PSQI could be recommended as a measure of sleep quality although, when necessary, it is recommended to add an objective measure for the quantity and quality of sleep, since patients’ reported sleep issues are often not confirmed by objective measurements [65].

This systematic review is the first one assessing the association between sleep and neurocognitive functioning in cancer survivors. One limitation of this review is that most studies consisted of a breast cancer population. This over-representation of breast cancer survivors makes the findings less generalizable to other cancer types, because of possible differences in treatment and the effect of the tumour on sleep and NCF. Another limitation is the exclusion of studies with cancer patients who are still undergoing treatment, leading to exclusion of (longitudinal) studies that had measurements pre- and post-cancer treatment. Both neurocognitive impairment and sleep issues are more often reported during, compared to after treatment, suggesting that a subgroup of patients recovers over time, while some survivors experience these issues long term.

In clinical practice, it is important that care providers are aware of the association between NCF and sleep and that treating poor sleep can be a way to decrease NCI in cancer survivors who report these issues.

The results of this review suggest that sleep and neurocognitive functioning are associated in cancer patients, with most evidence for an association with sr-NCF. Further research is necessary to be able to establish the effect of sleep interventions on sr-NCF, but particularly of oNCF.

Poor sleep quality linked to higher type 1 diabetes distress in young adults

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Young adults with type 1 diabetes have more diabetes distress symptoms with shorter sleep time, lower sleep efficiency and higher sleep variability, according to a study published in The Science of Diabetes Self-Management and Care.

“When an individual has inadequate sleep quantity or quality, a functional deficit occurs between the amygdala and ventral anterior cingulate cortex, resulting in decreased mood, a heightened response to negative stimuli and altered inhibitory function,” Stephanie Griggs, PhD, RN, assistant professor at the Frances Payne Bolton School of Nursing and faculty associate at the Schubert Center for Child Studies at Case Western Reserve University, told Healio. “Sleep extension has restorative benefits, normalizes inhibitory function and suppresses amygdala hyperactivity, thereby resulting in fewer or no emotional or physical symptoms.”

Stephanie Griggs, PhD, RN
Griggs is an assistant professor at the Frances Payne Bolton School of Nursing and faculty associate at the Schubert Center for Child Studies at Case Western Reserve University.

Griggs and colleagues conducted a cross-sectional study enrolling 46 young adults aged 18 to 30 years with type 1 diabetes for at least 6 months and no other major health problems (mean age, 22.3 years; 67.4% women; 84.8% non-Hispanic white). Participants with obstructive sleep apnea or working night shift were excluded. Adults wore the Spectrum Plus device on their wrist to measure sleep-wake data. Sleep quality was assessed through the 19-item Pittsburgh Sleep Quality Index. The 17-item Diabetes Distress Scale measured diabetes emotional stress, and diabetes symptoms were measured with the 34-item Diabetes Symptom Checklist – Revised. The 8-item PROMIS version 1.0 questionnaire measured general emotional distress. Each participant wore a Dexcom G4 continuous glucose monitor or shared data from their own device during the study. Clinical and demographic data were collected through electronic medical records.

Of the study cohort, 54.3% slept fewer than 7 hours per night. The cohort had a mean sleep quality score of 5.91, with a score of greater than 5 signifying poor sleep quality.

Moderate emotional distress was reported by 30.4% of the cohort, and 41.3% met the criteria for moderate diabetes distress. Females reported having more hypoglycemia symptoms (P = .001) and fatigue symptoms (P =.008) compared with males.

Having a shorter total sleep time (r = –.32; P = .032), longer sleep onset latency (r = .36; P = .014) and worse sleep efficiency (r = –.35; P = .018) were associated with greater diabetes emotional distress. The associations remained significant after adjusting for sex and BMI. High sleep variability was associated with more neurologic pain symptoms (r = .32; P = .028). Longer sleep onset latency was associated with more psychological cognitive symptoms (r = .37; P = .012), more hyperglycemia symptoms (r = .33; P = .024) and a higher total symptom burden (r = .3 P = .042).

“Promoting sleep through extension and decreasing variability may help mitigate diabetes symptoms,” Griggs said. “Diabetes and primary care providers should routinely assess sleep health and address diabetes management issues that may be interfering with nocturnal sleep, such as nocturnal hyperglycemia or hypoglycemia.”

Griggs said future researchers should clarify the directionality of the associations between sleep duration and the timing of symptoms, and whether promoting sleep mitigates diabetes symptoms over time.