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One night of total sleep deprivation promotes a state of generalized hyperalgesia: A surrogate pain model to study the relationship of insomnia and pain
Abstract
Sleep disturbances are highly prevalent in chronic pain patients. Understanding their relationship has become an important research topic since poor sleep and pain are assumed to closely interact. To date, human experimental studies exploring the impact of sleep disruption/deprivation on pain perception have yielded conflicting results. This inconsistency may be due to the large heterogeneity of study populations and study protocols previously used. In addition, none of the previous studies investigated the entire spectrum of nociceptive modalities. To address these shortcomings, a standardized comprehensive quantitative sensory protocol was used in order to compare the somatosensory profile of 14 healthy subjects (6 female, 8 male, 23.5 ± 4.1 year; mean ± SD) after a night of total sleep deprivation (TSD) and a night of habitual sleep in a cross-over design. One night of TSD significantly increased the level of sleepiness (P<0.001) and resulted in higher scores of the State Anxiety Inventory (P<0.01). In addition to previously reported hyperalgesia to heat (P<0.05) and blunt pressure (P<0.05), study participants developed hyperalgesia to cold (P<0.01) and increased mechanical pain sensitivity to pinprick stimuli (P<0.05) but no changes in temporal summation. Paradoxical heat sensations or dynamic mechanical allodynia were absent. TSD selectively modulated nociception, since detection thresholds of non-nociceptive modalities remained unchanged. Our findings show that a single night of TSD is able to induce generalized hyperalgesia and to increase State Anxiety scores. In the future, TSD may serve as a translational pain model to elucidate the pathomechanisms underlying the hyperalgesic effect of sleep disturbances.
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“Exerciseinduced elevations of endocannabinoid levels have been proposed to account partially for anxiolytic (Tantimonaco et al., 2014;Fuss et al., 2015), anti-nociceptive (Galdino et al., 2014) and neuroprotective (Hill et al., 2010a) properties of exercise, which are all responses that instead are affected in a negative direction by sleep loss (e.g.Roy-Byrne et al., 1986;Schuh-Hofer et al., 2013;”
From Sleep restriction alters plasma endocannabinoids concentrations before but not after exercise in humans (2016) · cites this paper as Schuh-Hofer et al., 2013
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Postoperative Sleep Disturbances
Hillman, D. R. (2017) · Advances in Anesthesia · doi:10.1016/j.aan.2017.07.001 · Cited by 43
Disabling low back pain associated with night shift duration: sleep problems as a potentiator
Takahashi, M., Matsudaira, K., & Shimazu, A. (2015) · American Journal of Industrial Medicine · doi:10.1002/ajim.22493 · Cited by 41
“All data were selfreported, and it is desirable to assess sleep using an objective method such as wrist actigraphy, even in a subsample [Schuh-Hofer et al., 2013; Alsaadi et al., 2014a].”
MethodNeurobiological mechanisms underlying the sleep-pain relationship in adolescence: A review
Christensen, J., Noel, M. E., & Mychasiuk, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.11.006 · Cited by 44
Night-shift work is associated with increased pain perception
Matre, D., Knardahl, S., & Nilsen, K. B. (2017) · Scandinavian Journal of Work Environment & Health · doi:10.5271/sjweh.3627 · Cited by 41
Akodu, A. K., & Akindutire, O. M. (2018) · The Korean journal of pain · doi:10.3344/kjp.2018.31.3.199 · Cited by 40
Park, S. J., Yoon, D. M., Yoon, K. B., Moon, J. A., & Kim, S. H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0163132 · Cited by 39
“Specifically, insomnia causes a hyperalgesic status with a low pain threshold, and this effect remains even after controlling other psychological symptoms [8,30].”
BackgroundHagenauer, M. H., Crodelle, J. A., Piltz, S. H., Toporikova, N., Ferguson, P. F. B., & Booth, V. (2017) · Association for Women in Mathematics series · doi:10.1007/978-3-319-60304-9_1 · Cited by 39
Li, Y., Ge, J., Luo, Y., Xu, W., Wang, J., Lazarus, M., Hong, Z., Qu, W., & Huang, Z. (2019) · Pain · doi:10.1097/j.pain.0000000000001725 · Cited by 36
Ghafouri, M., Teymourzadeh, A., Nakhostin-Ansari, A., Sepanlou, S. G., Dalvand, S., Moradpour, F., Bavarsad, A. H., Boogar, S. S., Dehghan, M., Ostadrahimi, A., et al. (2022) · Annals of Medicine and Surgery · doi:10.1016/j.amsu.2022.103243 · Cited by 36
The Influence of Sleep Disturbance on Chronic Pain
Li, M. T., Robinson, C. L., Ruan, Q. Z., Surapaneni, S., & Southerland, W. A. (2022) · Current Pain and Headache Reports · doi:10.1007/s11916-022-01074-2 · Cited by 47
The Pain and Movement Reasoning Model: Introduction to a simple tool for integrated pain assessment
Jones, L. E., & O’Shaughnessy, D. (2014) · Manual Therapy · doi:10.1016/j.math.2014.01.010 · Cited by 37
Vinstrup, J., Jakobsen, M. D., Calatayud, J., Jay, K., & Andersen, L. L. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00968 · Cited by 37
“Extending these findings, 1 night of total sleep deprivation has been shown to induce a state of generalized hyperalgesia and mood changes associated with increased anxiety levels (4).”
BackgroundImpact of Sleep Deprivation in the Neurological Intensive Care Unit: A Narrative Review
Chang, V. A., Owens, R. L., & LaBuzetta, J. N. (2019) · Neurocritical Care · doi:10.1007/s12028-019-00795-4 · Cited by 42
Rouhi, S., Topcu, J., Egorova, N., & Jordan, A. S. (2023) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2023.101835 · Cited by 33
Rhon, D. I. (2019) · Pain Physician · doi:10.36076/ppj/2019.22.e351 · Cited by 33
Conditioned pain modulation is not decreased after partial sleep restriction
Matre, D., Andersen, M. R., Knardahl, S., & Nilsen, K. B. (2015) · European Journal of Pain · doi:10.1002/ejp.741 · Cited by 34
“…Kundermann et al., 2004b; Chhangani et al., 2009; Smith et al., 2009; Tiede et al., 2010; Ablin et al., 2013; Schestatsky et al., 2013; Schuh-Hofer et al., 2013) and by cross-sectional studies indicating associations between pain and sleep problems (Edwards et al., 2008; Sivertsen et al., 2009).”
BackgroundSardi, N. F., Lazzarim, M. K., Guilhen, V. A., Marcílio, R. S., Natume, P., Watanabe, T., Lima, M. M. S., Tobaldini, G., & Fischer, L. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.06.022 · Cited by 35
“The mechanisms by which sleep loss increases pain sensitivity (Alexandre et al., 2017; Nascimento et al., 2007; Okifuji and Hare, 2011; Sardi et al., 2018; Schuh-Hofer et al., 2013; Tomim et al., 2016) and the prevalence of pain conditions (Mork and Nilsen, 2012; Paul-Savoie et al.”
BackgroundCoregulation of sleep-pain physiological interplay by orexin system: An unprecedented review
Ahmadi‐Soleimani, S. M., Mianbandi, V., Azizi, H., Azhdari‐Zarmehri, H., Ghaemi-Jandabi, M., Abbasi-Mazar, A., Mohajer, Y., & Darana, S. P. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112650 · Cited by 32
Experimental Sleep Restriction Facilitates Pain and Electrically Induced Cortical Responses
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Poor Sleep Is a Risk Factor for Low-Back Pain among Healthcare Workers: Prospective Cohort Study
Vinstrup, J., Jakobsen, M. D., & Andersen, L. L. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17030996 · Cited by 29
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Ding, W., Yang, L., Shi, E., Kim, B., Low, S. A., Hu, K., Gao, L., Chen, P., Ding, W. Y., Borsook, D., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42283-6 · Cited by 29
Fibromyalgia Symptoms and Cirrhosis
Rogal, S. S., Bielefeldt, K., Wasan, A. D., Szigethy, E., Lotrich, F. E., & DiMartini, A. F. (2014) · Digestive Diseases and Sciences · doi:10.1007/s10620-014-3453-3 · Cited by 29
“Disordered sleep is a hallmark of both hepatic encephalopathy and fibromyalgia, with sleep disturbances thought to predispose people to more severe pain [6, 7].”
Scheinfeld, N. S. (2013) · Dermatology Online Journal · doi:10.5070/d31911020616 · Cited by 28
Metadata
- Authors
- Schuh-Hofer, S., Wodarski, R., Pfau, D. B., Caspani, O., Magerl, W., Kennedy, J. D., & Treede, R.-D.
- Affiliations
- Eli Lilly (United States) (US)
- Heidelberg University (DE)
- Venue
- Pain
- Published
- 2013-09
- Volume
- 154
- Issue
- 9
- Pages
- 1613-1621
- ISSN
- 0304-3959 (ISSN-L)
- OpenAlex
- W2094084202
- Cited by
- 296
- References
- 109
- Citations by year
- 2026: 17 · 2025: 26 · 2024: 18 · 2023: 27 · 2022: 27 · 2021: 22 · 2020: 21 · 2019: 23 · 2018: 18 · 2017: 20 · 2016: 23 · 2015: 30 · 2014: 19 · 2013: 5
- FWCI
- 17.83
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Pain (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Commission
- Innovative Medicines Initiative
- Topics
- Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and related disorders
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- total sleep deprivation, hyperalgesia, insomnia, pain perception, nociception, quantitative sensory testing, mechanical allodynia, state anxiety, sleepiness
- MeSH terms
- Adult, Anxiety, Female, Humans, Hyperalgesia, Male, Pain, Pain Measurement, Physical Stimulation, Sleep Deprivation, Pain Threshold, Cross-Over Studies, Young Adult, Pain Perception
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