One night of total sleep deprivation promotes a state of generalized hyperalgesia: a surrogate pain model to study the relationship of insomnia and pain

Schuh-Hofer, Sigrid; Wodarski, Rachel; Pfau, Doreen B.; Caspani, Ombretta; Magerl, Walter; Kennedy, Jeffrey D.; Treede, Rolf-Detlef

doi:10.1016/j.pain.2013.04.046

Cited by 296Pain Mechanisms and TreatmentsSleep and related disordersSleep and Work-Related Fatigue

One night of total sleep deprivation promotes a state of generalized hyperalgesia: a surrogate pain model to study the relationship of insomnia and pain

Schuh-Hofer, Sigrid, Wodarski, Rachel, Pfau, Doreen B., Caspani, Ombretta, Magerl, Walter, Kennedy, Jeffrey D., Treede, Rolf-Detlef·2013·Pain

DOI 10.1016/j.pain.2013.04.046

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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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Farooqui, S. M., Brock, J. W., & Zhou, J. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02072-1 · Cited by 62 · see citing works
The relationship between selective sleep deprivation, nocturnal jaw‐muscle activity and pain in healthy men
Arima, T., Svensson, P. J., Rasmussen, C., Nielsen, K. D., Drewes, A. M., & Arendt‐Nielsen, L. (2001) · Journal of Oral Rehabilitation · doi:10.1046/j.1365-2842.2001.00687.x · Cited by 62 · see citing works
Sleep deprivation increases brain serotonin turnover in the rat
Asikainen, M., Toppila, J. P., Alanko, L., Ward, D. J., Stenberg, D., & Porkka‐Heiskanen, T. (1997) · Neuroreport · doi:10.1097/00001756-199705060-00006 · Cited by 61 · see citing works
Sleep deprivation decreases μ and δ opioid receptor binding in the rat limbic system
Fadda, P., Tortorella, A. A. V., & Fratta, W. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90489-g · Cited by 59 · see citing works
REM sleep deprivation decreases apomorphine-induced stimulation of locomotor activity but not stereotyped behavior in mice
Asakura, W., Matsumoto, K., Ohta, H., & Watanabe, H. (1992) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(92)90092-x · Cited by 51 · see citing works
Sleep deprivation: Changes of monoamines and acetylcholine in rat brain
Tsuchiya, K., Toru, M., & Kobayashi, T. (1969) · Life Sciences · doi:10.1016/0024-3205(69)90143-x · Cited by 45 · see citing works
Heterogeneous effects of rapid eye movement sleep deprivation on binding to α- and β-adrenergic receptor subtypes in rat brain
Hipólide, D. C., Tufik, S., Raymond, R., & Nóbrega, J. N. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00067-0 · Cited by 45 · see citing works
Disruption of Thermal Perception in a Multiple Sclerosis Patient With Central Pain
Morin, C., Bushnell, M. C., Luskin, M. B., & Craig, A. D. (2002) · Clinical Journal of Pain · doi:10.1097/00002508-200205000-00008 · Cited by 45 · see citing works
Pain-related behavior following REM sleep deprivation in the rat: Influence of peripheral nerve injury, spinal glutamatergic receptors and nitric oxide
Wei, H., Zhao, W., Wang, Y., & Pertovaara, A. (2007) · Brain Research · doi:10.1016/j.brainres.2007.02.040 · Cited by 45 · see citing works
Effect of sleep deprivation on brain serotonin in the rat
Borbély, A. A., Steigrad, P., & Tobler, I. (1980) · Behavioural Brain Research · doi:10.1016/s0166-4328(80)80058-1 · Cited by 42 · see citing works
Melatonin and its precursors′ effects on 131I uptake by the thyroid gland under different photic conditions
PROSPO, N. D. D., Safinski, R. J., Martino, L. J. D., & McGuinness, E. T. (1969) · Life Sciences · doi:10.1016/0024-3205(69)90147-7 · Cited by 41 · see citing works
Nociceptor and age specific effects of REM sleep deprivation induced hyperalgesia
May, M. E., Harvey, M. T., Valdovinos, M. G., Kline, R., Wiley, R. G., & Kennedy, C. H. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.10.005 · Cited by 39 · see citing works
Role of spinal 5-HT receptors in cutaneous hypersensitivity induced by REM sleep deprivation
WEI, H., MA, A., WANG, Y., & Pertovaara, A. (2008) · Pharmacological Research · doi:10.1016/j.phrs.2008.05.007 · Cited by 34 · see citing works
Intrathecal administration of a gap junction decoupler, an inhibitor of Na+–K+–2Cl− cotransporter 1, or a GABAA receptor agonist attenuates mechanical pain hypersensitivity induced by REM sleep deprivation in the rat
Wei, H., Hao, B., Huang, J., Ma, A., Li, X., Wang, Y., & Pertovaara, A. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.09.007 · Cited by 33 · see citing works
Serotonin binding in rat brain: circadian rhythm and effect of sleep deprivation.
Wesemann, W., Weiner, N., Rotsch, M., & Schulz, E. (1983) · PubMed · Cited by 33 · see citing works
The Effects of Pain, Gender, and Age on Sleep/Wake and Circadian Rhythm Parameters in Oncology Patients at the Initiation of Radiation Therapy
Buffum, D. G., Koetters, T., Cho, M. H., Macera, L., Paul, S. M., West, C. M., Aouizerat, B. E., Dunn, L. B., Dodd, M. J., Lee, K. A., et al. (2010) · Journal of Pain · doi:10.1016/j.jpain.2010.09.008 · Cited by 32 · see citing works
Modality-specific Somatosensory Changes in a Human Surrogate Model of Postoperative Pain
Fißmer, I., Klein, T., Magerl, W., Treede, R., Zahn, P. K., & Pogatzki-Zahn, E. M. (2011) · Anesthesiology · doi:10.1097/aln.0b013e318219509e · Cited by 30 · see citing works
Sleep Deprivation in the Rat: XVIII. Regional Brain Levels of Monoamines and Their Metabolites
Bergmann, B. M., Seiden, L. S., Landis, C. A., Gilliland, M. A., & Rechtschaffen, A. (1994) · SLEEP · doi:10.1093/sleep/17.7.583 · Cited by 27 · see citing works
Sleepiness does not Modulate Experimental Joint Pain in Healthy Volunteers
Drewes, A. M., Rössel, P., Arendt‐Nielsen, L., Dremstrup, K., Hansen, L. M., Birket‐Smith, L., & Stengaard‐Pedersen, K. (1997) · Scandinavian Journal of Rheumatology · doi:10.3109/03009749709065709 · Cited by 26 · see citing works
Roles of Hypothalamic Subgroup Histamine and Orexin Neurons on Behavioral Responses to Sleep Deprivation Induced by the Treadmill Method in Adolescent Rats
Xu, A., Sakurai, E., Kuramasu, A., Zhang, J., Li, J., Okamura, N., Zhang, D., Yoshikawa, T., Watanabe, T., & Yanai, K. (2010) · Journal of Pharmacological Sciences · doi:10.1254/jphs.10177fp · Cited by 24 · see citing works
Impact of sex on hyperalgesia induced by sleep loss
Araujo, P., Mazaro‐Costa, R., Tufik, S. B., & Andersen, M. L. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.11.003 · Cited by 23 · see citing works
Sleep, pain, fibromyalgia, and chronic fatigue syndrome
Landis, C. A. (2010) · Handbook of clinical neurology · doi:10.1016/b978-0-444-52006-7.00039-3 · Cited by 19 · see citing works
Circadian Rhythm of Serotonin Binding in Rat Brain—II. Influence of Sleep Deprivation and Imipramine
Wesemann, W., Rotsch, M., Schulz, E., & Zöfel, P. (1986) · Chronobiology International · doi:10.3109/07420528609066359 · Cited by 19 · see citing works
Mechanism of noradrenaline-induced stimulation of Na–K ATPase activity in the rat brain: implications on REM sleep deprivation-induced increase in brain excitability
Mallick, B. N., Singh, S., & Singh, A. (2009) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-009-0260-9 · Cited by 15 · see citing works
Regulation of cerebral serotonin binding and metabolism in sleep-deprived rats
Wesemann, W., & Weiner, N. (1982) · Behavioural Brain Research · doi:10.1016/0166-4328(82)90082-1 · Cited by 13 · see citing works
The Effects of Sleep Deprivation and Sleep Recovery on Pain Thresholds of Rats with Chronic Pain
Andersen, M. L., Silva, A., Kawakami, R., & Tufik, S. (2009) · Sleep Science · doi:10.1055/s-0046-1820473 · Cited by 11 · see citing works
Parametric analysis of thermal preference following sleep deprivation in the rat
Harvey, M. T., Kline, R., May, M. E., Roberts, A., Valdovinos, M. G., Wiley, R. G., & Kennedy, C. H. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.08.070 · Cited by 8 · see citing works
Immunomodulatory effects of anti-tumor necrosis factor alpha therapy on synovium in spondylarthropathy: histologic findings in eight patients from an open-label pilot study
Warrington (2001) · Pure Amsterdam UMC · doi:10.1002/1529-0131(200101)44:1 · Cited by 2 · see citing works

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Sorted by citations

Neuropathic pain: an updated grading system for research and clinical practice
Finnerup, N. B., Haroutounian, S., Kamerman, P., Baron, R., Bennett, D. L. H., Bouhassira, D., Cruccu, G., Freeman, R., Hansson, P., Nurmikko, T., et al. (2016) · Pain · doi:10.1097/j.pain.0000000000000492 · Cited by 1,332 · see citing works
Evidence-Based Nonpharmacologic Strategies for Comprehensive Pain Care
Tick, H., Nielsen, A., Pelletier, K. R., Bonakdar, R. A., Simmons, S., Glick, R. M., Ratner, E. F., Lemmon, R., Wayne, P. M., & Zador, V. (2018) · EXPLORE · doi:10.1016/j.explore.2018.02.001 · Cited by 388 · see citing works
“Sleeplessness has been shown experimentally to induce a generalized state of hyperalgesia, a “fibromyalgialike syndrome”.(445) Both pain and pain medications can cause sleep disorders.”
Background
The effect of sleep deprivation and restriction on mood, emotion, and emotion regulation: three meta-analyses in one
Tomaso, C. C., Johnson, A. B., & Nelson, T. D. (2021) · SLEEP · doi:10.1093/sleep/zsaa289 · Cited by 282 · see citing works
Fibromyalgia: A Critical and Comprehensive Review
Borchers, A. T., & Gershwin, M. E. (2015) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-015-8509-4 · Cited by 279 · see citing works
“sleep deprivation in healthy volunteers [548, 549, 558] or patients with chronic pain [552, 559].”
Background
Effects of acute sleep deprivation on state anxiety levels: a systematic review and meta-analysis
Pires, G. N., Bezerra, A. G., Tufik, S. B., & Andersen, M. L. (2016) · Sleep Medicine · doi:10.1016/j.sleep.2016.07.019 · Cited by 276 · see citing works
Sleep and pain sensitivity in adults
Sivertsen, B., Lallukka, T. M., Petrie, K. J., Steingrímsdóttir, Ó. A., Stubhaug, A., & Nielsen, C. S. (2015) · Pain · doi:10.1097/j.pain.0000000000000131 · Cited by 248 · see citing works
Sleep and pain: recent insights, mechanisms, and future directions in the investigation of this relationship
Babiloni, A. H., Koninck, B. P. D., Beetz, G., Beaumont, L. D., Martel, M. O., & Lavigne, G. J. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02067-z · Cited by 242 · see citing works
Unraveling the evolutionary determinants of sleep
Joiner, W. J. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.068 · Cited by 232 · see citing works
Treatment of central sensitization in patients with chronic pain: time for change?
Nijs, J., Leysen, L., Vanlauwe, J., Logghe, T., Ickmans, K., Polli, A., Malfliet, A., Coppieters, I., & Huysmans, E. (2019) · Expert Opinion on Pharmacotherapy · doi:10.1080/14656566.2019.1647166 · Cited by 225 · see citing works
“increases anxiety state [132,133], while sleep curtailment impairs”
Background
Postoperative sleep disruptions: A potential catalyst of acute pain?
Chouchou, F., Khoury, S., Chauny, J., Denis, R., & Lavigne, G. J. (2013) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2013.07.002 · Cited by 224 · see citing works
Sleep loss and emotion: A systematic review and meta-analysis of over 50 years of experimental research.
Palmer, C. A., Bower, J. L., Cho, K. W., Clementi, M. A., Lau, S., Oosterhoff, B. J., & Alfano, C. A. (2023) · Psychological Bulletin · doi:10.1037/bul0000410 · Cited by 237 · see citing works
Frozen shoulder
Millar, N. L., Meakins, A., Struyf, F., Willmore, E. G., Campbell, A. L., Kirwan, P., Akbar, M., Moore, L. K., Ronquillo, J. C., Murrell, G. A. C., et al. (2022) · Nature Reviews Disease Primers · doi:10.1038/s41572-022-00386-2 · Cited by 208 · see citing works
Sleep Disturbances in Chronic Pain: Neurobiology, Assessment, and Treatment in Physical Therapist Practice
Nijs, J., Maîresse, O., Neu, D., Leysen, L., Danneels, L. A., Cagnie, B. J., Meeus, M., Moens, M., Ickmans, K., & Goubert, D. (2018) · Physical Therapy · doi:10.1093/ptj/pzy020 · Cited by 193 · see citing works
The Pain of Sleep Loss: A Brain Characterization in Humans
Krause, A. J., Prather, A. A., Wager, T. D., Lindquist, M. A., & Walker, M. P. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2408-18.2018 · Cited by 178 · see citing works
“Experiments in humans establish that total (Schuh-Hofer et al., 2013), partial (Faraut et al., 2015), and selective sleep deprivation (Lentz et al., 1999; Roehrs et al., 2006) increase pain, including a lowering of pain thresholds (Schrimpf et al., 2015).”
Background
Decreased alertness due to sleep loss increases pain sensitivity in mice
Alexandre, C., Latrémolière, A., Ferreira, A. N., Miracca, G., Yamamoto, M., Scammell, T. E., & Woolf, C. J. (2017) · Nature Medicine · doi:10.1038/nm.4329 · Cited by 171 · see citing works
Postoperative sleep disorders and their potential impacts on surgical outcomes
Rampes, S., Ma, K., Divecha, Y. A., Alam, A., & Ma, D. (2020) · Journal of Biomedical Research · doi:10.7555/jbr.33.20190054 · Cited by 155 · see citing works
“Pain disrupts sleep, and poor sleep increases pain sensitivity[58].”
Background
What is the role of lifestyle behaviour change associated with non-communicable disease risk in managing musculoskeletal health conditions with special reference to chronic pain?
Dean, E., & Söderlund, A. (2015) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-015-0545-y · Cited by 156 · see citing works
“Further, insomnia has been shown to lower a person’s pain threshold and tolerance [41,42], and this is true for people without a health condition [43].”
Background
The effect of sleep deprivation on pain perception in healthy subjects: a meta-analysis
Schrimpf, M., Liegl, G., Boeckle, M., Leitner, A., Geisler, P., & Pieh, C. (2015) · Sleep Medicine · doi:10.1016/j.sleep.2015.07.022 · Cited by 154 · see citing works
“Sleep loss can affect mood states in healthy adolescents [93] and sleep deprivation decreases positive and increases negative mood [58, 94, 95].”
BackgroundInfluential
Chronic exposure to insufficient sleep alters processes of pain habituation and sensitization
Simpson, N. S., Scott‐Sutherland, J., Gautam, S., Sethna, N. F., & Haack, M. (2017) · Pain · doi:10.1097/j.pain.0000000000001053 · Cited by 152 · see citing works
“A single night of sleep loss did not affect temporal summation in humans, but did reduce pain thresholds.(33) However, in a clinical setting, temporal summation of pain increased in patients with osteoarthritis in association with low sleep efficiency.”
Influential
Total sleep deprivation increases pain sensitivity, impairs conditioned pain modulation and facilitates temporal summation of pain in healthy participants
Staffe, A. T., Bech, M. W., Clemmensen, S. L. K., Nielsen, H. T., Larsen, D. B., & Petersen, K. K. (2019) · PLoS ONE · doi:10.1371/journal.pone.0225849 · Cited by 150 · see citing works
Sleep disturbances and severe stress as glial activators: key targets for treating central sensitization in chronic pain patients?
Nijs, J., Loggia, M. L., Polli, A., Moens, M., Huysmans, E., Goudman, L., Meeus, M., Vanderweeën, L., Ickmans, K., & Clauw, D. J. (2017) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2017.1353603 · Cited by 146 · see citing works
“Even low levels of inflammatory cytokines are known to affect brain function [106] which correlates with observations of increased sensitivity to painful stimuli following sleep restriction [100,104,107].”
Background
A prospective analysis of sleep deprivation and disturbance in surgical patients
Dolan, R. D., Huh, J., Tiwari, N., Sproat, T., & Camilleri‐Brennan, J. (2016) · Annals of Medicine and Surgery · doi:10.1016/j.amsu.2015.12.046 · Cited by 126 · see citing works
Rehabilitation management of low back pain – it’s time to pull it all together!
Tousignant‐Laflamme, Y., Martel, M. O., Joshi, A. B., & Cook, C. (2017) · Journal of Pain Research · doi:10.2147/jpr.s146485 · Cited by 126 · see citing works
“…disturbances, 64 that LBP patients reporting sleep problems often report severe back pain, 65–67 and that sleep deprivation triggers hyperalgesia, 68 the presence of sleep disturbances should also be considered as a comorbidity potentially driving other domains, such as nervous system…”
Challenges in postdischarge function and recovery: the case of fast-track hip and knee arthroplasty
Aasvang, E. K., Luna, I. E., & Kehlet, H. (2015) · British Journal of Anaesthesia · doi:10.1093/bja/aev257 · Cited by 120 · see citing works
An Evaluation of Central Sensitization in Patients With Sickle Cell Disease
Campbell, C. M., Moscou-Jackson, G., Carroll, C. P., Kiley, K. B., Haywood, C., Lanzkron, S., Hand, M., Edwards, R. R., & Haythornthwaite, J. A. (2016) · Journal of Pain · doi:10.1016/j.jpain.2016.01.475 · Cited by 114 · see citing works
“These findings are consistent with a growing literature documenting a specific relationship between sleep disturbance and CS indices in clinical pain samples [10;18;42].”
BackgroundResult
The differential effects of sleep deprivation on pain perception in individuals with or without chronic pain: A systematic review and meta-analysis
Chang, J. R., Fu, S.-N., Li, X., Li, S. X., Wang, X., Zhou, Z., Pinto, S. M., Samartzis, D., Karppinen, J. I., & Wong, A. Y. L. (2022) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2022.101695 · Cited by 112 · see citing works
Predicting, preventing and managing persistent pain after breast cancer surgery: the importance of psychosocial factors
Schreiber, K. L., Kehlet, H., Belfer, I., & Edwards, R. R. (2014) · Pain Management · doi:10.2217/pmt.14.33 · Cited by 106 · see citing works
Sex differences in measures of central sensitization and pain sensitivity to experimental sleep disruption: implications for sex differences in chronic pain
Smith, M. T., Remeniuk, B., Finan, P. H., Speed, T. J., Tompkins, D. A., Robinson, M., Gonzalez, K., Bjurström, M. F., & Irwin, M. R. (2018) · SLEEP · doi:10.1093/sleep/zsy209 · Cited by 101 · see citing works
Effects of disturbed sleep on gastrointestinal and somatic pain symptoms in irritable bowel syndrome
Patel, A., Hasak, S., Cassell, B. E., Ciorba, M. A., Vivio, E. E., Kumar, M., Gyawali, C. P., & Sayuk, G. S. (2016) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13677 · Cited by 92 · see citing works
“heat, pressure) following sleep deprivation have been demonstrated in both animal models and healthy subjects.(43) Disruptions in sleep also affect somatic pain syndromes such as fibromyalgia, where sleep complaints and abnormal sleep physiology commonly is detected.”
Background
Chronic Widespread Back Pain is Distinct From Chronic Local Back Pain: Evidence From Quantitative Sensory Testing, Pain Drawings, and Psychometrics
Gerhardt, A., Eich, W., Janke, S., Leisner, S., Treede, R.-D., & Tesarz, J. (2016) · The Clinical Journal of Pain · doi:10.1097/ajp.0000000000000300 · Cited by 91 · see citing works
Self-citation
What to call the amplification of nociceptive signals in the central nervous system that contribute to widespread pain?
Woolf, C. J. (2014) · Pain · doi:10.1016/j.pain.2014.07.021 · Cited by 89 · see citing works
“Does it represent a disease state or is it at the extreme of the normal variance in pain threshold due to genetic polymorphisms [3] or sleep deprivation [7]; might it be due to widely distributed peripheral sensitization or disseminated ectopic firing in a small-fiber neuropathy [8], or the consequence of anatomical c…”
Background
Who is healthy? Aspects to consider when including healthy volunteers in QST-based studies—a consensus statement by the EUROPAIN and NEUROPAIN consortia
Gierthmühlen, J., Enax‐Krumova, E., Attal, N., Bouhassira, D., Cruccu, G., Finnerup, N. B., Haanpää, M., Hansson, P. T., Jensen, T. S., Freynhagen, R., et al. (2015) · Pain · doi:10.1097/j.pain.0000000000000227 · Cited by 89 · see citing works
Individual Variation in Pain Sensitivity and Conditioned Pain Modulation in Acute Low Back Pain: Effect of Stimulus Type, Sleep, and Psychological and Lifestyle Factors
Klyne, D. M., Moseley, G. L., Sterling, M. M., Barbe, M. F., & Hodges, P. W. (2018) · Journal of Pain · doi:10.1016/j.jpain.2018.02.017 · Cited by 88 · see citing works
The Association between Sleep and Chronic Spinal Pain: A Systematic Review from the Last Decade
Looveren, E. V., Bilterys, T., Munneke, W., Cagnie, B. J., Ickmans, K., Maîresse, O., Malfliet, A., Baets, L. D., Nijs, J., Goubert, D., et al. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10173836 · Cited by 87 · see citing works
“Longitudinal and experimental research has affirmed that disturbed sleep causes generalized hyperalgesia and reduced endogenous pain inhibition in healthy subjects [19,20].”
Background
Sleep Loss in the Hospitalized Patient and Its Influence on Recovery From Illness and Operation
Hillman, D. R. (2021) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000005323 · Cited by 85 · see citing works
Psychosocial factors and risk of chronic widespread pain: An 11-year follow-up study—The HUNT study
Mundal, I. P., Gråwe, R. W., Bjø‌rngaard, J. H., Linaker, O. M., & Fors, E. A. (2014) · Pain · doi:10.1016/j.pain.2014.04.033 · Cited by 80 · see citing works
Effects of experimental sleep deprivation on anxiety-like behavior in animal research: Systematic review and meta-analysis
Pires, G. N., Bezerra, A. G., Tufik, S. B., & Andersen, M. L. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.028 · Cited by 79 · see citing works
Are Signs of Central Sensitization in Acute Low Back Pain a Precursor to Poor Outcome?
Klyne, D. M., Moseley, G. L., Sterling, M. M., Barbe, M. F., & Hodges, P. W. (2019) · Journal of Pain · doi:10.1016/j.jpain.2019.03.001 · Cited by 80 · see citing works
Effects of Preoperative Anxiety on Postoperative Outcomes and Sleep Quality in Patients Undergoing Laparoscopic Gynecological Surgery
Gu, X., Zhang, Y., Wei, W., & Zhu, J. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12051835 · Cited by 78 · see citing works
Sleep features and central sensitization symptoms in primary headache patients
de Tommaso, M., Delussi, M. D., Vecchio, E., Sciruicchio, V., Invitto, S., & Livrea, P. (2014) · The Journal of Headache and Pain · doi:10.1186/1129-2377-15-64 · Cited by 77 · see citing works
“Sleep deprivation causes hyperalgesia in normal controls [20], while further case- control studies may clarify if the sleep time threshold for central sensitization symptoms development may be lower in primary headache in respect to controls.”
Influential
The Role of Sex in Sleep Deprivation Related Changes of Nociception and Conditioned Pain Modulation
Eichhorn, N., Treede, R., & Schuh‐Hofer, S. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.09.044 · Cited by 78 · see citing works
“Similar to our previous observations (Schuh-Hofer et al., 2013) none of the study participants complained of spontaneous bodily pain after one night of TSD.”
BackgroundResultInfluential
Napping Reverses Increased Pain Sensitivity Due to Sleep Restriction
Faraut, B., Léger, D., Medkour, T., Dubois, A., Bayon, V., Chennaoui, M., & Perrot, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117425 · Cited by 75 · see citing works
Nucleus accumbens mediates the pronociceptive effect of sleep deprivation: the role of adenosine A2A and dopamine D2 receptors
Sardi, N. F., Tobaldini, G., de Morais, R. N., & Fischer, L. (2017) · Pain · doi:10.1097/j.pain.0000000000001066 · Cited by 72 · see citing works
Sleep Fragmentation Hypersensitizes Healthy Young Women to Deep and Superficial Experimental Pain
Iacovides, S., George, K., Kamerman, P. R., & Baker, F. C. (2017) · Journal of Pain · doi:10.1016/j.jpain.2017.02.436 · Cited by 71 · see citing works
Pain in children and adolescents with cerebral palsy – a cross-sectional register study of 3545 individuals
Eriksson, E., Hägglund, G., & Alriksson‐Schmidt, A. I. (2020) · BMC Neurology · doi:10.1186/s12883-019-1597-7 · Cited by 70 · see citing works
The Neuroinflammatory Etiopathology of Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS)
Glassford, J. A. G. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00088 · Cited by 68 · see citing works
“Glucocorticoid deficiencies∗∗ are associated with interrupted nociceptive modulation, for example via the disruption of neuroendocrine-mediated glial activation mechanisms (Schwartzman, 2012).”
Background
The Pronociceptive Effect of Paradoxical Sleep Deprivation in Rats: Evidence for a Role of Descending Pain Modulation Mechanisms
Tomim, D. H., Pontarolla, F. M., Bertolini, J. F., Arase, M., Tobaldini, G., Lima, M. M. S., & Fischer, L. (2015) · Molecular Neurobiology · doi:10.1007/s12035-014-9059-0 · Cited by 66 · see citing works
Sleep and Children with Cerebral Palsy: A Review of Current Evidence and Environmental Non-Pharmacological Interventions
Dutt, R., Roberts, M. R., & Brown, C. A. (2015) · Children · doi:10.3390/children2010078 · Cited by 64 · see citing works
“Pain is known to interfere with sleep and there is evidence that the relationship may be bi-directional such that sleep deprivation increases the severity of pain experience and increased pain interferes with sleep [15].”
Background
Influence of sleep problems and co-occurring musculoskeletal pain on long-term prognosis of chronic low back pain: the HUNT Study
Skarpsno, E. S., Mork, P. J., Nilsen, T. I. L., & Nordstoga, A. L. (2019) · Journal of Epidemiology & Community Health · doi:10.1136/jech-2019-212734 · Cited by 63 · see citing works
Presentation and management of chronic pain
Rajapakse, D., Liossi, C., & Howard, R. F. (2014) · Archives of Disease in Childhood · doi:10.1136/archdischild-2013-304207 · Cited by 62 · see citing works
Sleep Disturbance and Chronic Widespread Pain
McBeth, J., Wilkie, R., Bedson, J., Chew-Graham, C. A., & Lacey, R. J. (2015) · Current Rheumatology Reports · doi:10.1007/s11926-014-0469-9 · Cited by 59 · see citing works
Analgesic Effect of Perioperative Escitalopram in High Pain Catastrophizing Patients after Total Knee Arthroplasty
Lunn, T. H., Frøkjær, V. G., Hansen, T. B., Kristensen, P. W., Lind, T., & Kehlet, H. (2015) · Anesthesiology · doi:10.1097/aln.0000000000000597 · Cited by 61 · see citing works
Insomnia severity and its relationship with demographics, pain features, anxiety, and depression in older adults with and without pain: cross-sectional population-based results from the PainS65+ cohort
Dragioti, E., Levin, L., Bernfort, L., Larsson, B. K., & Gerdle, B. U. C. (2017) · Annals of General Psychiatry · doi:10.1186/s12991-017-0137-3 · Cited by 63 · see citing works
Sleep restriction alters plasma endocannabinoids concentrations before but not after exercise in humans
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Background
Leveraging healthcare utilization to explore outcomes from musculoskeletal disorders: methodology for defining relevant variables from a health services data repository
Rhon, D. I., Clewley, D. J., Young, J. L., Sissel, C. D., & Cook, C. E. (2018) · BMC Medical Informatics and Decision Making · doi:10.1186/s12911-018-0588-8 · Cited by 59 · see citing works
Role of Glia in the Regulation of Sleep in Health and Disease
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Effect of sleep loss on pain—New conceptual and mechanistic avenues
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“IL-17 directly causes pain (Pinto et al., 2010) by sensitizing nociceptors (Segond von Banchet et al., 2013), while the pro-nociceptive effects of IL-22 are possibly indirectly mediated by neutrophil recruitment (Pinto et al., 2015).”
Background
Disturbed body perception, reduced sleep, and kinesiophobia in subjects with pregnancy-related persistent lumbopelvic pain and moderate levels of disability: An exploratory study
Beales, D. J., Lutz, A., Thompson, J. A., Wand, B. M., & O’Sullivan, P. (2015) · Manual Therapy · doi:10.1016/j.math.2015.04.016 · Cited by 55 · see citing works
Pain matters for central sensitization: sensory and psychological parameters in patients with fibromyalgia syndrome
Rehm, S., Sachau, J., Hellriegel, J., Forstenpointner, J., Jacobsen, H. B., Harten, P., Gierthmühlen, J., & Baron, R. (2021) · PAIN Reports · doi:10.1097/pr9.0000000000000901 · Cited by 53 · see citing works
The association between sleep quality, preoperative risk factors for chronic postoperative pain and postoperative pain intensity 12 months after knee and hip arthroplasty
Larsen, D. B., Laursen, M. B., Simonsen, O. H., Arendt‐Nielsen, L., & Petersen, K. K. (2021) · British Journal of Pain · doi:10.1177/20494637211005803 · Cited by 53 · see citing works
The effect of sleep restriction on laser evoked potentials, thermal sensory and pain thresholds and suprathreshold pain in healthy subjects
Ødegård, S. S., Omland, P. M., Nilsen, K. B., Stjern, M., Gravdahl, G. B., & Sand, T. (2014) · Clinical Neurophysiology · doi:10.1016/j.clinph.2014.12.011 · Cited by 52 · see citing works
Relationships of sleep disturbance, intestinal microbiota, and postoperative pain in breast cancer patients: a prospective observational study
Yao, Z., Zhao, B.-C., Yang, X. Y., Lei, S.-H., Jiang, Y.-M., & Liu, K. (2020) · Sleep And Breathing · doi:10.1007/s11325-020-02246-3 · Cited by 49 · see citing works
“Preliminary research with healthy participants has shown that disturbed sleep can induce generalized hyperalgesia [9, 10], supporting the hypothesis regarding Zhi-Wen Yao and Bing-Cheng Zhao contributed equally to this work.”
Result
Disrupted Sleep Is Associated With Altered Pain Processing by Sex and Ethnicity in Knee Osteoarthritis
Petrov, M. E. R., Goodin, B. R., Cruz‐Almeida, Y., King, C., Glover, T. L., Bulls, H. W., Herbert, M. S., Sibille, K. T., Bartley, E. J., Fessler, B. J., et al. (2015) · Journal of Pain · doi:10.1016/j.jpain.2015.02.004 · Cited by 49 · see citing works
“In Figure 1, the simple slopes were plotted, but not the true intercepts on the original temporal summation response scale (1-100) because the sleep parameters and the interaction terms were centered.”
Background
Pain and Distraction According to Sensory Modalities: Current Findings and Future Directions
Bascour–Sandoval, C., Salgado, S., Milán, E. G., Fernández‐Gómez, J., Michael, G. A., & Galvéz-García, G. (2019) · Pain Practice · doi:10.1111/papr.12799 · Cited by 46 · see citing works
Interplay among pain intensity, sleep disturbance and emotion in patients with non-specific low back pain
Sribastav, S. S., He, P., Jun, L., Li, Z., Fuxin, W., Jianru, W., Hui, L., Hua, W., & Zheng, Z. (2017) · PeerJ · doi:10.7717/peerj.3282 · Cited by 48 · see citing works
“The pain has been reported to have a bidirectional relationship with sleep; pain hinders sleep while sleep disturbance may decrease pain thresholds and the mental capacity to manage pain (Schuh-Hofer et al., 2013).”
Background
Provoked vestibulodynia: current perspectives
Henzell, H., Berzins, K. N., & Langford, J. (2017) · International Journal of Women s Health · doi:10.2147/ijwh.s113416 · Cited by 45 · see citing works
MicroRNA-19b predicts widespread pain and posttraumatic stress symptom risk in a sex-dependent manner following trauma exposure
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Musculoskeletal pain is associated with restless legs syndrome in young adults
Hoogwout, S. J., Paananen, M. V., Smith, A. J., Beales, D. J., O’Sullivan, P. B., Straker, L. M., Eastwood, P. R., McArdle, N., & Champion, D. (2015) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-015-0765-1 · Cited by 43 · see citing works
“High prevalence of sleep disruption has been reported in chronic MSK pain [35] and experimental studies in animals [36] and humans [37] have shown that sleep disruption can induce musculoskeletal sensitization and lower pain thresholds.”
Background
Associates of Insomnia in People with Chronic Spinal Pain: A Systematic Review and Meta-Analysis
Bilterys, T., Siffain, C. N., Maeyer, I. D., Looveren, E. V., Maîresse, O., Nijs, J., Meeus, M., Ickmans, K., Cagnie, B. J., Goubert, D., et al. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10143175 · Cited by 43 · see citing works
Are Changes in Sleep Quality/Quantity or Baseline Sleep Parameters Related to Changes in Clinical Outcomes in Patients With Nonspecific Chronic Low Back Pain?
Chang, J. R., Wang, X., Lin, G., Samartzis, D., Pinto, S. M., & Wong, A. Y. L. (2021) · Clinical Journal of Pain · doi:10.1097/ajp.0000000000001008 · Cited by 42 · see citing works
Review of self-reported instruments that measure sleep dysfunction in patients suffering from temporomandibular disorders and/or orofacial pain
Sommer, I., Lavigne, G. J., & Ettlin, D. A. (2014) · Sleep Medicine · doi:10.1016/j.sleep.2014.07.023 · Cited by 44 · see citing works
“4 deprivation) or poor sleep quality may induce pain hypersensitivity, exacerbate pain responses, and alter mood states without clearly understood pathomechanisms [50,53,89,95].”
Background
Can we improve pain and sleep in elderly individuals with transcranial direct current stimulation? – Results from a randomized controlled pilot study
Harvey, M.-P., Lorrain, D., Martel, M., Bergeron-Vézina, K., Houde, F., Seguin, M., & Léonard, G. (2017) · Clinical Interventions in Aging · doi:10.2147/cia.s133423 · Cited by 42 · see citing works
Postoperative Sleep Disturbances
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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 · see citing works
“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].”
Method
Neurobiological 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 41 · see citing works
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 · see citing works
The effect of stabilization exercise on pain-related disability, sleep disturbance, and psychological status of patients with non-specific chronic low back pain
Akodu, A. K., & Akindutire, O. M. (2018) · The Korean journal of pain · doi:10.3344/kjp.2018.31.3.199 · Cited by 40 · see citing works
Factors Associated with Higher Reported Pain Levels in Patients with Chronic Musculoskeletal Pain: A Cross-Sectional, Correlational Analysis
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 · see citing works
“Specifically, insomnia causes a hyperalgesic status with a low pain threshold, and this effect remains even after controlling other psychological symptoms [8,30].”
Background
The Modulation of Pain by Circadian and Sleep-Dependent Processes: A Review of the Experimental Evidence
Hagenauer, 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 · see citing works
High cortical delta power correlates with aggravated allodynia by activating anterior cingulate cortex GABAergic neurons in neuropathic pain mice
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 · see citing works
Prevalence and predictors of low back pain among the Iranian population: Results from the Persian cohort study
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 · see citing works
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 42 · see citing works
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 36 · see citing works
Association of Stress and Musculoskeletal Pain With Poor Sleep: Cross-Sectional Study Among 3,600 Hospital Workers
Vinstrup, J., Jakobsen, M. D., Calatayud, J., Jay, K., & Andersen, L. L. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00968 · Cited by 36 · see citing works
“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).”
Background
Impact 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 37 · see citing works
The impact of sleep disturbance on pain perception: A systematic review examining the moderating effect of sex and age
Rouhi, S., Topcu, J., Egorova, N., & Jordan, A. S. (2023) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2023.101835 · Cited by 33 · see citing works
Comorbid Insomnia and Sleep Apnea are Associated with Greater Downstream Health Care Utilization and Chronic Opioid Use after Arthroscopic Hip Surgery
Rhon, D. I. (2019) · Pain Physician · doi:10.36076/ppj/2019.22.e351 · Cited by 33 · see citing works
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 · see citing works
“…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).”
Background
Chronic sleep restriction increases pain sensitivity over time in a periaqueductal gray and nucleus accumbens dependent manner
Sardi, 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 33 · see citing works
“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.”
Background
Coregulation 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 · see citing works
Experimental Sleep Restriction Facilitates Pain and Electrically Induced Cortical Responses
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The joint effect of insomnia symptoms and lifestyle factors on risk of self-reported fibromyalgia in women: longitudinal data from the HUNT Study
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Linking Nonrestorative Sleep and Activity Interference Through Pain Catastrophizing and Pain Severity: An Intraday Process Model Among Individuals With Fibromyalgia
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The Impact of Sleep Disturbances on Endogenous Pain Modulation: A Systematic Review and Meta-Analysis
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Biopsychosocial factors should be considered when evaluating central sensitization in axial spondyloarthritis
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Poor Sleep Is a Risk Factor for Low-Back Pain among Healthcare Workers: Prospective Cohort Study
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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)
ORCID: Wodarski, Rachel
Caspani, Ombretta
Magerl, Walter
Kennedy, Jeffrey D.
Treede, Rolf-Detlef
Venue: Pain
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2013-09
Volume: 154
Issue: 9
Pages: 1613-1621
ISSN: 0304-3959 (ISSN-L)
DOI: 10.1016/j.pain.2013.04.046
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 › 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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One night of total sleep deprivation promotes a state of generalized hyperalgesia: a surrogate pain model to study the relationship of insomnia and pain

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