Sex differences in temporal characteristics of descending inhibitory control: an evaluation using repeated bilateral experimental induction of muscle pain

Ge, Hong-You; Madeleine, Pascal; Arendt-Nielsen, Lars

doi:10.1016/j.pain.2004.03.005

Cited by 146Pain Mechanisms and TreatmentsPain Management and Placebo EffectPain Management and Treatment

Sex differences in temporal characteristics of descending inhibitory control: an evaluation using repeated bilateral experimental induction of muscle pain

Ge, Hong-You, Madeleine, Pascal, Arendt-Nielsen, Lars·2004·Pain

DOI 10.1016/j.pain.2004.03.005

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Abstract

Little is known about sex differences in the temporal pattern of descending inhibitory mechanisms, such as descending noxious inhibitory control (DNIC). Sex differences in temporal characteristics of DNIC were investigated by measuring pressure pain thresholds (PPTs) over time in the trapezius muscles (local pain areas) and the posterolateral neck muscles (referred pain areas) following repeated bilateral injection of hypertonic versus isotonic saline into both trapezius muscles. Ten females and 11 males received two consecutive bilateral injections, with 15 min interval, of either 5.8% hypertonic saline (0.5 ml in each side for each bilateral injection) or isotonic saline as a control in a randomized manner. Following hypertonic saline injection, the maximal pain intensities of the first and second bilateral injections were significantly higher in females than in males. The PPTs in the trapezius muscles were significantly lower in females than in males. Significantly higher PPTs (hypoalgesia) in men than in women were shown 15 min after the first bilateral injection, and 7.5 and 15 min after the second bilateral injection in the referred pain areas. Importantly, the second bilateral injection failed to further increase the PPTs for both sexes. These results showed that there were sex differences in temporal characteristics of descending inhibition with long-lasting hypoalgesia in men than in women. Repeated noxious muscular stimuli may inhibit further build-up of DNIC, which…

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Oono, Y., Nie, H., Matos, R. V. L., Wang, K., & Arendt‐Nielsen, L. (2011) · Scandinavian Journal of Pain · doi:10.1016/j.sjpain.2011.05.006 · Cited by 97 · see citing works
Self-citation
Cortical influences on brainstem circuitry responsible for conditioned pain modulation in humans
Youssef, A. M., Macefield, V. G., & Henderson, L. A. (2016) · Human Brain Mapping · doi:10.1002/hbm.23199 · Cited by 95 · see citing works
“Other studies have shown gender differences in CPM magnitude although this difference appears small and can vary depending on experimental methodology [Ge et al., 2004; Popescu et al., 2010; Staud et al., 2003].”
Background
Sex Differences in the Stability of Conditioned Pain Modulation (CPM) among Patients with Chronic Pain
Martel, M. O., Wasan, A. D., & Edwards, R. R. (2013) · Pain Medicine · doi:10.1111/pme.12220 · Cited by 92 · see citing works
Lack of sex differences in modulation of experimental intraoral pain by diffuse noxious inhibitory controls (DNIC)
Baad‐Hansen, L., Poulsen, H. F., Jensen, H. M., & Svensson, P. J. (2005) · Pain · doi:10.1016/j.pain.2005.05.006 · Cited by 90 · see citing works
“A recent study has demonstrated a sex difference in the temporal characteristics of DNIC by repeated tonic trapezius muscle pain (Ge et al., 2004).”
BackgroundResultInfluential
Prevalence of neck and low back pain in community-dwelling adults in Spain: an updated population-based national study (2009/10–2011/12)
Palacios‐Ceña, D., Alonso‐Blanco, C., Hernández‐Barrera, V., Carrasco‐Garrido, P., Jiménez‐García, R., & Fernández‐de‐las‐Peñas, C. (2014) · European Spine Journal · doi:10.1007/s00586-014-3567-5 · Cited by 91 · see citing works
“For instance, biologically, women exhibit less efficient pain habituation and a greater susceptibility to develop temporal summation of chemically-evoked pain [24], and mechanically-evoked pain, [25] as well as less efficient diffuse noxious inhibitory mechanisms [26] than men.”
Background
Sex differences in experimental measures of pain sensitivity and endogenous pain inhibition
Goodin, B. R., Bulls, H. W., Freeman, E. L., Robbins, M. T., Anderson, A., & Ness, T. J. (2015) · Journal of Pain Research · doi:10.2147/jpr.s84607 · Cited by 90 · see citing works
Overview of orofacial pain: epidemiology and gender differences in orofacial pain
Shinal, R. M., & Fillingim, R. B. (2007) · Dental Clinics of North America · doi:10.1016/j.cden.2006.09.004 · Cited by 80 · see citing works
Intensity Dependence of Auditory-Evoked Cortical Potentials in Fibromyalgia Patients: A Test of the Generalized Hypervigilance Hypothesis
Carrillo‐de‐la‐Peña, M. T., Vallet, M., Pérez, M. I., & Gómez‐Perretta, C. (2006) · Journal of Pain · doi:10.1016/j.jpain.2006.01.452 · Cited by 86 · see citing works
Evidence of diffuse noxious inhibitory controls (DNIC) elicited by cold noxious stimulation in patients with provoked vestibulodynia
Johannesson, U., de Boussard, C. N., Jansen, G. B., & Bohm‐Starke, N. (2006) · Pain · doi:10.1016/j.pain.2006.10.022 · Cited by 84 · see citing works
“For a deeper understanding of other noxious modalities, the tourniquet (Bouhassira et al., 2003) and hypertonic saline injections (Ge et al., 2004) could be used.”
Background
Sex differences and hormonal modulation of deep tissue pain
Traub, R. J., & Ji, Y. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.07.002 · Cited by 83 · see citing works
“Correspondingly, the pressure pain threshold increased in men, but not women, in an area of referred pain (Ge et al., 2004; Ge et al., 2006).”
Background
Gender differences in pain modulation evoked by repeated injections of glutamate into the human trapezius muscle
Ge, H., Madeleine, P., & Arendt‐Nielsen, L. (2004) · Pain · doi:10.1016/j.pain.2004.09.041 · Cited by 80 · see citing works
“Females have a lower pressure pain threshold (PPT) in the trapezius muscle than males but no such gender differences exists in posterolateral neck muscles and masseter muscles in the present and previous studies (Ge et al., 2004; Svensson et al., 2003).”
BackgroundResultSelf-citation
Spatial and temporal aspects of muscle hyperalgesia induced by nerve growth factor in humans
Andersen, H., Arendt‐Nielsen, L., Svensson, P. J., Danneskiold‐Samsøe, B., & Graven‐Nielsen, T. (2008) · Experimental Brain Research · doi:10.1007/s00221-008-1531-5 · Cited by 81 · see citing works
“This result is in contrast to other studies where women produced higher VAS pain scores than men to hypertonic saline injection ( Ge et al. 2004; Stohler et al. 2001).”
ResultSelf-citation
Analysis of Meaningful Conditioned Pain Modulation Effect in a Pain-Free Adult Population
Locke, D., Gibson, W., Moss, P., Munyard, K., Mamotte, C. D. S., & Wright, A. (2014) · Journal of Pain · doi:10.1016/j.jpain.2014.09.001 · Cited by 81 · see citing works
Delayed onset muscle soreness in neck/shoulder muscles
Nie, H., Kawczyński, A., Madeleine, P., & Arendt‐Nielsen, L. (2005) · European Journal of Pain · doi:10.1016/j.ejpain.2004.12.009 · Cited by 81 · see citing works
“It appears that women are more sensitive to pain and incline to report greater pain to experimental muscle pain conditions (Ge et al., 2004; Riley et al., 1998).”
BackgroundSelf-citation
The nociceptive withdrawal reflex: Normative values of thresholds and reflex receptive fields
Neziri, A. Y., Andersen, O. K., Petersen‐Felix, S., Radanov, B. P., Dickenson, A. H., Scaramozzino, P., Arendt‐Nielsen, L., & Curatolo, M. (2009) · European Journal of Pain · doi:10.1016/j.ejpain.2009.04.010 · Cited by 80 · see citing works
“The influence of age seems to be strongly dependent on the stimulus modality (Gibson and Farrell, 2004; Lautenbacher et al., 2005).”
BackgroundSelf-citation
Generalized expansion of nociceptive reflex receptive fields in chronic pain patients
Neziri, A. Y., Haesler, S., Petersen‐Felix, S., Müller, M. D., Arendt‐Nielsen, L., Manresa, J. A. B., Andersen, O. K., & Curatolo, M. (2010) · Pain · doi:10.1016/j.pain.2010.09.017 · Cited by 79 · see citing works
Self-citation
Central hyperexcitability as measured with nociceptive flexor reflex threshold in chronic musculoskeletal pain: A systematic review
Lim, E. C. W., Sterling, M. M., Stone, A., & Vicenzino, B. (2011) · Pain · doi:10.1016/j.pain.2011.03.033 · Cited by 77 · see citing works
The effects of DNIC-type inhibition on temporal summation compared to single pulse processing: Does sex matter?
Lautenbacher, S., Miriam Kunz, A., & Burkhardt, S. (2008) · Pain · doi:10.1016/j.pain.2008.09.019 · Cited by 74 · see citing works
“There have been some reports of this kind before [2,6,23,24,28], which counterbalance roughly in number the studies in which women were found to have less efficient DNIC [ 7 ,8,11,32,33].”
BackgroundResult
Sex and pain perception and analgesia.
Palmeira, C. C. D. A., Ashmawi, H. A., & Posso, I. D. P. (2011) · Revista Brasileira de Anestesiologia · doi:10.1016/s0034-7094(11)70091-5 · Cited by 73 · see citing works
Computer work and self-reported variables on anthropometrics, computer usage, work ability, productivity, pain, and physical activity
Madeleine, P., Vangsgaard, S., Andersen, J. H., Ge, H., & Arendt‐Nielsen, L. (2013) · BMC Musculoskeletal Disorders · doi:10.1186/1471-2474-14-226 · Cited by 71 · see citing works
“The reported differences in musculoskeletal pain frequency, intensity, and spreading are well in line with the known gender differences in pain perception [29-32].”
BackgroundResultSelf-citation
Fatigue-enhanced hyperalgesia in response to muscle insult: Induction and development occur in a sex-dependent manner
Gregory, N. S., Gibson-Corley, K. N., Frey‐Law, L., & Sluka, K. A. (2013) · Pain · doi:10.1016/j.pain.2013.07.047 · Cited by 67 · see citing works
Factors affecting – And relationships between – Different modes of endogenous pain modulation in healthy volunteers
Treister, R., Eisenberg, E., Gershon, E., Haddad, M., & Pud, D. (2009) · European Journal of Pain · doi:10.1016/j.ejpain.2009.10.005 · Cited by 60 · see citing works
“Many studies have demonstrated more efficient DNIC like-effect in men than in women (Staud et al., 2003; Ge et al., 2004; Serrao et al., 2004; Granot et al., 2008), whereas one trial showed more efficient DNIC like-effect in women than in men (Bragdon et al., 2002).”
Result
Prevalence of chronic head, neck and low back pain and associated factors in women residing in the autonomous region of Madrid (Spain)
Jiménez-Sánchez, S., Fernández-de-las-Peñas, C., Carrasco-Garrido, P., Hernández-Barrera, V., Alonso-Blanco, C., Palacios-Ceña, D., & Jiménez-García, R. (2012) · Gaceta Sanitaria · doi:10.1016/j.gaceta.2011.10.012 · Cited by 59 · see citing works
Descending pain modulation and its interaction with peripheral sensitization following sustained isometric muscle contraction in fibromyalgia
Ge, H. Y., Nie, H., Graven‐Nielsen, T., Danneskiold‐Samsøe, B., & Arendt‐Nielsen, L. (2011) · European Journal of Pain · doi:10.1016/j.ejpain.2011.06.008 · Cited by 57 · see citing works
“This may be related to a less efficient descending inhibition in older rather than younger subjects (Riley et al., 2010) and female gender (Arendt-Nielsen et al., 2008; Ge et al., 2004).”
BackgroundSelf-citation
Gender‐specific differences in electromyographic changes and perceived pain induced by experimental muscle pain during sustained contractions of the upper trapezius muscle
Ge, H., Arendt‐Nielsen, L., Farina, D., & Madeleine, P. (2005) · Muscle & Nerve · doi:10.1002/mus.20410 · Cited by 55 · see citing works
Self-citation
Gender Differences in Pain Severity, Disability, Depression, and Widespread Pressure Pain Sensitivity in Patients with Fibromyalgia Syndrome Without Comorbid Conditions
Castro-Sánchez, A. M., Matarán-Peñarrocha, G. A., López-Rodríguez, M. M., Lara-Palomo, I. C., Arendt-Nielsen, L., & Fernández-de-las-Peñas, C. (2012) · Pain Medicine · doi:10.1111/j.1526-4637.2012.01523.x · Cited by 69 · see citing works
Self-citation
Temporal changes in cortical activation during distraction from pain: A comparative LORETA study with conditioned pain modulation
Moont, R., Crispel, Y., Lev, R., Pud, D., & Yarnitsky, D. (2011) · Brain Research · doi:10.1016/j.brainres.2011.11.056 · Cited by 54 · see citing works
Evaluation of Anti-Hyperalgesic and Analgesic Effects of Two Benzodiazepines in Human Experimental Pain: A Randomized Placebo-Controlled Study
Vuilleumier, P. H., Besson, M. J., Desmeules, J. A., Arendt‐Nielsen, L., & Curatolo, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0043896 · Cited by 53 · see citing works
Self-citation
Psychophysical testing of spatial and temporal dimensions of endogenous analgesia: conditioned pain modulation and offset analgesia
Honigman, L., Yarnitsky, D., Sprecher, E., & Weissman‐Fogel, I. (2013) · Experimental Brain Research · doi:10.1007/s00221-013-3580-7 · Cited by 51 · see citing works
“…mostly demonstrate that males exhibit more efficient EA magnitudes, for example, in stress-induced analgesia, and, specifically, in different CPM paradigms and OA (Staud et al. 2003; Ge et al. 2004; Quiton and Greenspan 2007; Granot et al. 2008; Weissman-Fogel et al. 2008; Niesters et al. 2011b).”
BackgroundResult
Effects of muscle fatigue induced by low-level clenching on experimental muscle pain and resting jaw muscle activity: gender differences
Torisu, T., Wang, K., Svensson, P. J., Laat, A. D., Fujii, H., & Arendt‐Nielsen, L. (2006) · Experimental Brain Research · doi:10.1007/s00221-006-0497-4 · Cited by 50 · see citing works
“Further, gender diVerences have been described in the endogenous pain control system ( Ge et al. 2004 ), and e.g.”
BackgroundSelf-citation
Effect of persistent monoarthritis of the temporomandibular joint region on acute mustard oil-induced excitation of trigeminal subnucleus caudalis neurons in male and female rats
Bereiter, D. A., Okamoto, K., & Bereiter, D. F. (2005) · Pain · doi:10.1016/j.pain.2005.05.013 · Cited by 49 · see citing works
“Reduced ability to recruit endogenous pain inhibitory mechanisms in women may contribute to chronic TMD (Bragdon et al., 2002), fibromyalgia (Staud et al., 2003), and deep neck muscle pain (Ge et al., 2004).”
Background
Pain threshold and intensity in rheumatic patients: correlations with the Hamilton Depression Rating scale
Bagnato, G., Andres, I. D., Sorbara, S., Verduci, E., Corallo, G., Ferrera, A., Morgante, S., Roberts, W. N., & Bagnato, G. (2014) · Clinical Rheumatology · doi:10.1007/s10067-013-2477-y · Cited by 48 · see citing works
Neurobiology of estrogen status in deep craniofacial pain
Bereiter, D. A., & Okamoto, K. (2011) · International review of neurobiology · doi:10.1016/b978-0-12-385198-7.00010-2 · Cited by 46 · see citing works
Symptoms and Physiological Responses to Prolonged, Repeated, Low‐Level Tooth Clenching in Humans
Takeuchi, T., Arima, T., Ernberg, M. M., Yamaguchi, T., Ohata, N., & Svensson, P. J. (2015) · Headache The Journal of Head and Face Pain · doi:10.1111/head.12528 · Cited by 41 · see citing works
Conditioned pain modulation is affected by occlusion cuff conditioning stimulus intensity, but not duration
Smith, A. D., & Pedler, A. R. (2017) · European Journal of Pain · doi:10.1002/ejp.1093 · Cited by 40 · see citing works
“There is significant variability in the magnitude of CPM (Imai et al., 2016; Kennedy et al., 2016), which may relate to age, sex (Edwards et al., 2003; Ge et al., 2004; Magerl et al., 2010) and other variables.”
Background
Individual variability and sex differences in conditioned pain modulation and the impact of resilience, and conditioning stimulus pain unpleasantness and salience
Firouzian, S., Osborne, N. R., Cheng, J. C., Kim, J. A., Bosma, R. L., Hemington, K. S., Rogachov, A., & Davis, K. D. (2020) · Pain · doi:10.1097/j.pain.0000000000001863 · Cited by 40 · see citing works
Body Mass Index and Its Influence on Chronic Low Back Pain in the Spanish Population: A Secondary Analysis from the European Health Survey (2020)
Lucha-López, M. O., Hidalgo-García, C., Monti-Ballano, S., Márquez-Gonzalvo, S., Ferrández-Laliena, L., Müller-Thyssen-Uriarte, J., & Lucha-López, A. C. (2023) · Biomedicines · doi:10.3390/biomedicines11082175 · Cited by 48 · see citing works
“Hormonal mechanisms [16], increased sensitivity to pain [17] and less competent pain inhibitory mechanism [18] have been highlighted as the biological factors behind the higher prevalence of low back pain in woman.”
Background
Postneedling soreness after deep dry needling of a latent myofascial trigger point in the upper trapezius muscle: Characteristics, sex differences and associated factors
Martín‐Pintado‐Zugasti, A., Fernández, Á. L. R., & Fernández‐Carnero, J. (2016) · Journal of Back and Musculoskeletal Rehabilitation · doi:10.3233/bmr-150630 · Cited by 39 · see citing works
“In these studies women reported higher levels of pain in the VAS compared to men following the injection of hypertonic saline [31,32] or glutamate [33].”
Pain in workers with shoulder impingement syndrome: an assessment using the DASH and McGill pain questionnaires
Camargo, P. R., Haik, M. N., Filho, R., Mattiello, S. M., & Salvini, T. F. (2007) · Brazilian Journal of Physical Therapy · doi:10.1590/s1413-35552007000200012 · Cited by 39 · see citing works
Central pain mechanisms following combined acid and capsaicin perfusion of the human oesophagus
Brock, C., Andresen, T., Frøkjær, J. B., Gale, J. D., Olesen, A. E., Arendt‐Nielsen, L., & Drewes, A. M. (2009) · European Journal of Pain · doi:10.1016/j.ejpain.2009.05.013 · Cited by 38 · see citing works
“Apart from spinal hyperexcitability pain perception is influenced by brainstem nuclei, which projects to dorsal horn neurons causing either enhanced facilitation or inhibition (Ren and Dubner, 2002; Millan, 2002; Gebhart, 2004).”
Self-citation
Influence of oral contraceptives on endogenous pain control in healthy women
Rezaii, T., & Ernberg, M. M. (2010) · Experimental Brain Research · doi:10.1007/s00221-010-2246-y · Cited by 36 · see citing works
“Many studies have shown that endogenous pain inhibition is less potent in women than in men (Staud et al. 2003; Ge et al. 2004, 2005; Serrao et al. 2004), which oVers a possible explanation to why many long-lasting pain conditions are more prevalent in women (Berkley 1997; Dao and LeResche 2000).”
Background
Inter-Individual Differences Explain More Variance in Conditioned Pain Modulation Than Age, Sex and Conditioning Stimulus Intensity Combined
Graeff, P., Itter, A., Wach, K., & Ruscheweyh, R. (2021) · Brain Sciences · doi:10.3390/brainsci11091186 · Cited by 36 · see citing works
Changes of Hypertonic Saline–Induced Masseter Muscle Pain Characteristics, by an Infusion of the Serotonin Receptor Type 3 Antagonist Granisetron
Christidis, N., Ioannidou, K., Milosevic, M. M., Segerdahl, M., & Ernberg, M. M. (2008) · Journal of Pain · doi:10.1016/j.jpain.2008.05.002 · Cited by 34 · see citing works
Effect of low-frequency deep brain stimulation on sensory thresholds in Parkinson's disease
Belasen, A., Rizvi, K., Gee, L. E., Yeung, P., Prusik, J., Ramirez‐Zamora, A., Hanspal, E. K., Paiva, P., Durphy, J., Argoff, C. E., et al. (2016) · Journal of neurosurgery · doi:10.3171/2016.2.jns152231 · Cited by 33 · see citing works
Zentrale Schmerzverarbeitung bei chronischem Rückenschmerz
Giesecke, T., Gracely, R. H., Clauw, D. J., NACHEMSON, A. K., Duck, M., Sabatowski, R., Gerbershagen, H. U., Williams, D. A., & Petzke, F. W. (2006) · Der Schmerz · doi:10.1007/s00482-006-0473-8 · Cited by 39 · see citing works
“Unterschiede in der Schmerzverarbeitung bei Männern und Frauen wurden beschrieben [14].”
Background
Reliability of the conditioned pain modulation paradigm across three anatomical sites
Nuwailati, R., Curatolo, M., LeResche, L., Ramsay, D. S., Spiekerman, C. F., & Drangsholt, M. T. (2019) · Scandinavian Journal of Pain · doi:10.1515/sjpain-2019-0080 · Cited by 30 · see citing works
Lack of Gender and Age Differences in Pain Measurements Following Exercise in People with Chronic Whiplash-Associated Disorders
Ickmans, K. (2017) · Pain Physician · doi:10.36076/ppj.20.5.e829 · Cited by 29 · see citing works
Bilateral, wide-spread, mechanical pain sensitivity in children with frequent episodic tension-type headache suggesting impairment in central nociceptive processing
Fernández‐de‐las‐Peñas, C., Fernández-Mayoralas, D. M., Ortega‐Santiago, R., Ambite‐Quesada, S., Crujera, A. G., & Fernández‐Jaén, A. (2010) · Cephalalgia · doi:10.1177/0333102410362806 · Cited by 27 · see citing works
“It is known that women have less efficient pain habituation, greater susceptibility to the development of temporal summation of chemical (43), mechanical (44), and therma (45) pain, and less efficient diffuse noxious inhibitory pathways (46,47) than males.”
Background
Characterization of pain syndromes in patients with neuromyelitis optica
Valério, F., Apóstolos‐Pereira, S. L., Sato, D. K., Callegaro, D., Lucato, L. T., Barboza, V. R., da Silva, V. A., Galhardoni, R., Rodrigues, A. L. D. L., Teixeira, M. J., et al. (2020) · European Journal of Pain · doi:10.1002/ejp.1608 · Cited by 24 · see citing works
Noxious counterirritation in patients with advanced osteoarthritis of the knee reduces MCC but not SII pain generators: A combined use of MEG and EEG
Hauck, M. (2008) · Journal of Pain Research · doi:10.2147/jpr.s3996 · Cited by 23 · see citing works
“Our dipole reconstruction results with N1 and P2 components generated in SII and MCC, respectively, is consistent with numerous studies examining pain evoked brain potentials and ﬁ elds (Bromm and Lorenz 1998; Treede et al 1999; Hauck et al 2006).”
Widespread Sensory Hypersensitivity Is Not a Feature of Chronic Headache in Elders
Uthaikhup, S., Sterling, M. M., & Jull, G. A. (2009) · Clinical Journal of Pain · doi:10.1097/ajp.0b013e3181a38f88 · Cited by 22 · see citing works
“Sex was used as a covariate in the analyses as its influence on pain perception has been documented in previous studies.(35,36) Nonparametric analysis was used for the TPTs because the data were not normally distributed.”
Method
Effect of heterotopic noxious conditioning stimulation on electrical and pressure pain thresholds in two different anatomical regions
Rosén, A., Feldreich, A., Dabirian, N., & Ernberg, M. M. (2008) · Acta Odontologica Scandinavica · doi:10.1080/00016350802169111 · Cited by 21 · see citing works
“It could be argued that the sample size was too small for such differences to be detected, although previous studies have shown gender differences in pain modulation with even fewer subjects [10,11,15].”
Result
Proprioception: The Forgotten Sixth Sense
Kaya, D. (2015) · Cited by 21 · see citing works
Influence of Polymorphisms in the HTR3A and HTR3B Genes on Experimental Pain and the Effect of the 5-HT3 Antagonist Granisetron
Jounger, S. L., Christidis, N., Hedenberg‐Magnusson, B., List, T., Svensson, P., Schalling, M., & Ernberg, M. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0168703 · Cited by 21 · see citing works
Individual Differences in Opioid Efficacy for Chronic Noncancer Pain
Riley, J. L., & Hastie, B. A. (2008) · Clinical Journal of Pain · doi:10.1097/ajp.0b013e31816c6654 · Cited by 21 · see citing works
Sexo e percepção da dor e analgesia
Palmeira, C. C. D. A., Ashmawi, H. A., & Posso, I. D. P. (2011) · Brazilian Journal of Anesthesiology · doi:10.1590/s0034-70942011000600014 · Cited by 18 · see citing works
Conditioned pain modulation in rodents can feature hyperalgesia or hypoalgesia depending on test stimulus intensity
Tansley, S. N., MacIntyre, L., Diamond, L., Sotocinal, S. G., George, N. C., Meluban, L., Austin, J., Coderre, T. J., Martin, L. J., & Mogil, J. S. (2018) · Pain · doi:10.1097/j.pain.0000000000001454 · Cited by 19 · see citing works
Painful conditioning stimuli of the craniofacial region evokes diffuse noxious inhibitory controls in men and women.
Wang, K., Svensson, P. J., Sessle, B. J., Cairns, B. E., & Arendt‐Nielsen, L. (2010) · PubMed · Cited by 17 · see citing works
Self-citation
Directed attention alters the temporal activation patterns of back extensors during trunk flexion–extension in individuals with chronic low back pain
Butler, H. L., Larivière, C., Hubley‐Kozey, C. L., & Sullivan, M. J. L. (2010) · European Spine Journal · doi:10.1007/s00586-010-1403-0 · Cited by 17 · see citing works
“In fact, intramuscular injections of algesic substances results in greater pain ratings in women than men providing robust support for the hypothesis that women are more sensitive to muscle pain [10, 14–17].”
Background
Sex-related differences in experimental pain sensitivity in subjects with painful or painless neuropathy after surgical repair of traumatic nerve injuries
Miclescu, A. A., Gkatziani, P., Granlund, P., Butler, S. H., & Gordh, T. (2022) · PAIN Reports · doi:10.1097/pr9.0000000000001033 · Cited by 16 · see citing works
“For instance, in some studies, male patients expressed more effective descending inhibition quantified by conditioned pain modulation (CPM).(7,8,13,34,39) In other studies, no sex differences(3,52) or more”
Changes in the Spatiotemporal Expression of Local and Referred Pain Following Repeated Intramuscular Injections of Hypertonic Saline: A Longitudinal Study
Rubin, T. K., Henderson, L. A., & Macefield, V. G. (2010) · Journal of Pain · doi:10.1016/j.jpain.2009.11.007 · Cited by 15 · see citing works
Individual differences in conditioned pain modulation are associated with functional connectivity within the descending antinociceptive pathway
Li, J. Z., Mills, E. P., Osborne, N. R., Cheng, J. C., Sanmugananthan, V. V., El‐Sayed, R., Besik, A., Kim, J. A., Bosma, R. L., Rogachov, A., et al. (2024) · Pain · doi:10.1097/j.pain.0000000000003478 · Cited by 14 · see citing works
“Although some studies in healthy subjects show a higher proportion of women exhibiting inhibitory CPM when compared with men, 31,33,35,84 other studies did not find any sex differences in the CPM. 55,69,71,78,79 A recent review highlighted that despite there being a known sexual dichotomy, there…”
Optimizing the early phase development of new analgesics by human pain biomarkers
Arendt-Nielsen, L., & Hoeck, H. C. (2011) · Expert Review of Neurotherapeutics · doi:10.1586/ern.11.147 · Cited by 14 · see citing works
Self-citation

Experimental muscle pain impairs descending inhibition
Arendt‐Nielsen, L., Sluka, K. A., & Nie, H. (2008) · Pain · doi:10.1016/j.pain.2008.09.027 · Cited by 142 · see citing works
Self-citation
Hypoalgesia in the Referred Pain Areas After Bilateral Injections of Hypertonic Saline Into the Trapezius Muscles of Men and Women: A Potential Experimental Model of Gender-Specific Differences
Ge, H., Madeleine, P., Cairns, B. E., & Arendt‐Nielsen, L. (2005) · Clinical Journal of Pain · doi:10.1097/01.ajp.0000149799.01123.38 · Cited by 55 · see citing works
Self-citation
Sex-related differences in descending norepinephrine and serotonin controls of spinal withdrawal reflex during intramuscular saline induced muscle nociception in rats
Lei, J., Jin, L., Zhao, Y., Sui, M.-Y., Huang, L., Tan, Y.-X., Chen, Y.-K., & You, H. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.01.004 · Cited by 43 · see citing works
Gender differences in pain modulation evoked by repeated injections of glutamate into the human trapezius muscle
Ge, H., Madeleine, P., & Arendt‐Nielsen, L. (2004) · Pain · doi:10.1016/j.pain.2004.09.041 · Cited by 80 · see citing works
Self-citation
Gender differences in pain modulation by diffuse noxious inhibitory controls: a systematic review
Popescu, A., LeResche, L., Truelove, E. L., & Drangsholt, M. T. (2010) · Pain · doi:10.1016/j.pain.2010.05.013 · Cited by 265 · see citing works

Authors: Ge, H.-Y., Madeleine, P., & Arendt-Nielsen, L.
Affiliations: Aalborg University (DK)
ORCID: Madeleine, Pascal
Venue: Pain
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2004-07
Volume: 110
Issue: 1
Pages: 72-78
ISSN: 0304-3959 (ISSN-L)
DOI: 10.1016/j.pain.2004.03.005
OpenAlex: W1982175970
Cited by: 146
References: 46
Citations by year: 2025: 9 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 4 · 2017: 4 · 2016: 7 · 2015: 7 · 2014: 6 · 2013: 9 · 2012: 6
FWCI: 4.32
Type: journal article
Language: en
Open access: closed
Locations: Pain (publishedVersion)
PubMed (publishedVersion)
VBN Forskningsportal (Aalborg Universitet) (submittedVersion)
Topics: Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
Life Sciences › Neuroscience › Cognitive Neuroscience › Pain Management and Placebo Effect
Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
Keywords: sex differences, pressure pain threshold, trapezius, referred pain, hypertonic saline injection, hypoalgesia, descending pain inhibition, descending facilitation, descending pain modulation
MeSH terms: Adult, Female, Humans, Injections, Intramuscular, Male, Neural Inhibition, Pain, Pressure, Saline Solution, Hypertonic, Sex Characteristics, Case-Control Studies, Pain Threshold, Muscle, Skeletal

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Sex differences in temporal characteristics of descending inhibitory control: an evaluation using repeated bilateral experimental induction of muscle pain

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