Enhanced pain modulation capacity among individuals with borderline personality disorder: A possible mechanism underlying their hypoalgesia.
Journal
European journal of pain (London, England)
ISSN: 1532-2149
Titre abrégé: Eur J Pain
Pays: England
ID NLM: 9801774
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
07
05
2019
revised:
30
10
2019
accepted:
06
11
2019
pubmed:
9
11
2019
medline:
21
11
2020
entrez:
9
11
2019
Statut:
ppublish
Résumé
Ample evidence suggests that individuals with borderline personality disorder (BPD) exhibit hyposensitivity to pain. Since the underlying mechanism of the pain hyposensitivity is unknown, we tested here for the first time whether this hyposensitivity is pain specific or exists also for innocuous sensation, and whether it is associated with enhanced descending pain modulation capabilities. Participants were 55 women; 22 patients with BPD and 33 matched healthy controls. Testing included the measurement of warmth sensation threshold (WST), heat-pain threshold (HPT), pain adaptation, conditioned pain modulation (CPM) and temporal summation of heat-pain (TSP). The level of dissociation was also evaluated. Women with BPD had higher WST and HPT compared with healthy controls. Moreover, women with BPD had greater magnitude of pain adaptation and CPM as well as higher dissociation level compared to controls. In neither the BPD nor the control group did WST and HPT correlate with pain adaptation, CPM or dissociation. In the BPD group only, HPT inversely correlated with the magnitude of TSP. Women with BPD present generalized hyposensitivity to both innocuous and noxious stimuli. Furthermore, women with BPD exhibit more efficient pain inhibition capabilities than healthy controls. While efficient pain modulation may underlie pain hyposensitivity in BPD, both traits may exist independently from each other, or may be moderated by another factor such as dissociation. On the basis of testing pronociceptive and antinociceptive components among individuals with BPD and healthy controls, this study reveals enhanced ability to inhibit pain among woman with borderline personality disorder (BPD) which may underlie hyposensitivity to both noxious and innocuous stimuli and perhaps also self-injurious behaviour among these individuals. The study contributes novel information on possible mechanisms involved in BPD manifestations.
Sections du résumé
BACKGROUND
Ample evidence suggests that individuals with borderline personality disorder (BPD) exhibit hyposensitivity to pain. Since the underlying mechanism of the pain hyposensitivity is unknown, we tested here for the first time whether this hyposensitivity is pain specific or exists also for innocuous sensation, and whether it is associated with enhanced descending pain modulation capabilities.
METHODS
Participants were 55 women; 22 patients with BPD and 33 matched healthy controls. Testing included the measurement of warmth sensation threshold (WST), heat-pain threshold (HPT), pain adaptation, conditioned pain modulation (CPM) and temporal summation of heat-pain (TSP). The level of dissociation was also evaluated.
RESULTS
Women with BPD had higher WST and HPT compared with healthy controls. Moreover, women with BPD had greater magnitude of pain adaptation and CPM as well as higher dissociation level compared to controls. In neither the BPD nor the control group did WST and HPT correlate with pain adaptation, CPM or dissociation. In the BPD group only, HPT inversely correlated with the magnitude of TSP.
CONCLUSIONS
Women with BPD present generalized hyposensitivity to both innocuous and noxious stimuli. Furthermore, women with BPD exhibit more efficient pain inhibition capabilities than healthy controls. While efficient pain modulation may underlie pain hyposensitivity in BPD, both traits may exist independently from each other, or may be moderated by another factor such as dissociation.
SIGNIFICANCE
On the basis of testing pronociceptive and antinociceptive components among individuals with BPD and healthy controls, this study reveals enhanced ability to inhibit pain among woman with borderline personality disorder (BPD) which may underlie hyposensitivity to both noxious and innocuous stimuli and perhaps also self-injurious behaviour among these individuals. The study contributes novel information on possible mechanisms involved in BPD manifestations.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
544-554Informations de copyright
© 2019 European Pain Federation - EFIC®.
Références
Bekrater-Bodmann, R., Chung, B. Y., Richter, I., Wicking, M., Foell, J., Mancke, F., … Flor, H. (2015). Deficits in pain perception in borderline personality disorder: Results from the thermal grill illusion. Pain, 156, 2084-2092. https://doi.org/10.1097/j.pain.0000000000000275
Bernstein, E. M., & Putnam, F. W. (1986). Development, reliability, and validity of a dissociation scale. The Journal of Nervous and Mental Disease, 174, 727-735. https://doi.org/10.1097/00005053-198612000-00004
Bernstein, E., Putnam, F. W., Ross, C. A., Torem, M., Coons, P., Dill, D., … Braun, B. G. (1993). Validity of the Dissociative Experiences Scale in screening for multiple personality disorder: A multicenter study. American Journal of Psychiatry, 150, 1030-1036.
Bingel, U., Herken, W., Teutsch, S., & May, A. (2008). Adaptation to painful stimulation involves the antinociceptive system - a 1-year follow-up of 10 participants. Pain, 140, 393-394.
Bohus, M., Limberger, M., Ebner, U., Glocker, F. X., Schwarz, B., Wernz, M., & Lieb, K. (2000). Pain perception during self-reported distress and calmness in women with borderline personality disorder and self-mutilating behavior. Psychiatry Research, 95, 251-260.
Bungert, M., Koppe, G., Niedtfeld, I., Vollstädt-Klein, S., Schmahl, C., Lis, S., & Bohus, M. (2015). Pain processing after social exclusion and its relation to rejection sensitivity in borderline personality disorder. PLoS ONE, 10, e0133693. https://doi.org/10.1371/journal.pone.0133693
Cardenas-Morales, L., Fladung, A. K., Kammer, T., Schmahl, C., Plener, P. L., Connemann, B. J., & Schonfeldt-Lecuona, C. (2011). Exploring the affective component of pain perception during aversive stimulation in borderline personality disorder. Psychiatry Research, 186, 458-460. https://doi.org/10.1016/j.psychres.2010.07.050
Coghill, R. C., Mayer, D. J., & Price, D. D. (1993). Wide dynamic range but not nociceptive-specific neurons encode multidimensional features of prolonged repetitive heat pain. Journal of Neurophysiology, 69, 703-716. https://doi.org/10.1152/jn.1993.69.3.703
Cullen, K. R., LaRiviere, L. L., Vizueta, N., Thomas, K. M., Hunt, R. H., Miller, M. J., … Schulz, S. C. (2016). Brain activation in response to overt and covert fear and happy faces in women with borderline personality disorder. Brain Imaging and Behavior, 10, 319-331. https://doi.org/10.1007/s11682-015-9406-4
Desbois, C., Le Bars, D., & Villanueva, L. (1999). Organization of cortical projections to the medullary subnucleus reticularis dorsalis: A retrograde and anterograde tracing study in the rat. The Journal of Comparative Neurology, 410, 178-196. https://doi.org/10.1002/(SICI)1096-9861(19990726)410:2<178:AID-CNE2>3.0.CO;2-F
Gescheider, G. A. (1997). Psychophysics: The Fundamentals. London: L. Erlbaum.
Geva, N., & Defrin, R. (2013). Enhanced pain modulation among triathletes: A possible explanation for their exceptional capabilities. Pain, 154, 2317-2323. https://doi.org/10.1016/j.pain.2013.06.031
Granovsky, Y., Nahman-Averbuch, H., Khamaisi, M., & Granot, M. (2017). Efficient conditioned pain modulation despite pain persistence in painful diabetic neuropathy. Pain Reports, 2(3), e592-https://doi.org/10.1097/PR9.0000000000000592
Gruener, H., Zeilig, G., Laufer, Y., Blumen, N., & Defrin, R. (2016). Differential pain modulation properties in central neuropathic pain after spinal cord injury. Pain, 157, 1415-1424. https://doi.org/10.1097/j.pain.0000000000000532
Guan, Y., Borzan, J., Meyer, R. A., & Raja, S. N. (2006). Windup in dorsal horn neurons is modulated by endogenous spinal mu-opioid mechanisms. Journal of Neuroscience, 26(16), 4298-4307.
Hazlett, E. A., Zhang, J., New, A. S., Zelmanova, Y., Goldstein, K. E., Haznedar, M. M., … Chu, K. W. (2012). Potentiated amygdala response to repeated emotional pictures in borderline personality disorder. Biological Psychiatry, 72, 448-456. https://doi.org/10.1016/j.biopsych.2012.03.027
Ji, R. R., & Woolf, C. J. (2001). Neuronal plasticity and signal transduction in nociceptive neurons: Implications for the initiation and maintenance of pathological pain. Neurobiology of Diseases, 8, 1-10. https://doi.org/10.1006/nbdi.2000.0360
Kenshalo, D. R., Leonard, R. B., Chung, J. M., & Willis, W. D. (1979). Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. Journal of Neurophysiology, 42, 1370-1389. https://doi.org/10.1152/jn.1979.42.5.1370
Kluetsch, R. C., Schmahl, C., Niedtfeld, I., Densmore, M., Calhoun, V. D., Daniels, J., … Lanius, R. A. (2012). Alterations in default mode network connectivity during pain processing in borderline personality disorder. Archives of General Psychiatry, 69, 993-1002. https://doi.org/10.1001/archgenpsychiatry.2012.476
Koenig, J., Thayer, J. F., & Kaess, M. (2016). A meta-analysis on pain sensitivity in self-injury. Psychological Medicine, 46(8), 1597-1612.
Kraus, A., Esposito, F., Seifritz, E., Di Salle, F., Ruf, M., Valerius, G., … Schmahl, C. (2009). Amygdala deactivation as a neural correlate of pain processing in patients with borderline personality disorder and cooccurrent posttraumatic stress disorder. Biological Psychiatry, 65, 819-822. https://doi.org/10.1016/j.biopsych.2008.10.028
Krause-Utz, A., Elzinga, B. M., Oei, N. Y., Paret, C., Niedtfeld, I., Spinhoven, P., … Schmahl, C. (2014). Amygdala and dorsal anterior cingulate connectivity during an emotional working memory task in borderline personality disorder patients with interpersonal trauma history. Frontiers in Human Neuroscience, 8, 848. https://doi.org/10.3389/fnhum.2014.00848
Krause-Utz, A., Frost, R., Winter, D., & Elzinga, B. M. (2017). Dissociation and alterations in brain function and structure: Implications for borderline personality disorder. Current Psychiatry Reports, 19, 6-28. https://doi.org/10.1007/s11920-017-0757-y
Krause-Utz, A., Oei, N. Y., Niedtfeld, I., Bohus, M., Spinhoven, P., Schmahl, C., & Elzinga, B. M. (2012). Influence of emotional distraction on working memory performance in borderline personality disorder. Psychological Medicine, 42, 2181-2192. https://doi.org/10.1017/S0033291712000153
Krause-Utz, A., Winter, D., Schriner, F., Chiu, C. D., Lis, S., Spinhoven, P., … Elzinga, B. M. (2018). Reduced amygdala reactivity and impaired working memory during dissociation in borderline personality disorder. European Archives of Psychiatry and Clinical Neuroscience, 268, 401-415. https://doi.org/10.1007/s00406-017-0806-x
Krüger, O., Shiozawa, T., Kreifelts, B., Scheffler, K., & Ethofer, T. (2015). Three distinct fiber pathways of the bed nucleus of the stria terminalis to the amygdala and prefrontal cortex. Cortex, 66, 60-68. https://doi.org/10.1016/j.cortex.2015.02.007
Lanius, R. A., Vermetten, E., Loewenstein, R. J., Brand, B., Schmahl, C., Bremner, J. D., & Spiegel, D. (2010). Emotion modulation in PTSD: Clinical and neurobiological evidence for a dissociative subtype. American Journal of Psychiatry, 167, 640-647. https://doi.org/10.1176/appi.ajp.2009.09081168
Le Bars, D. (2002). The whole body receptive field of dorsal horn multireceptive neurones. Brain Research. Brain Research Reviews, 40, 29-44. https://doi.org/10.1016/S0165-0173(02)00186-8
Leichsenring, F., Leibing, E., Kruse, J., New, A. S., & Leweke, F. (2011). Borderline personality disorder. Lancet, 377, 74-84. https://doi.org/10.1016/S0140-6736(10)61422-5
Ludäscher, P., Bohus, M., & Lieb, K. (2007). Elevated pain thresholds correlate with dissociation and aversive arousal in women with borderline personality disorder. Psychiatry Research, 149, 291-296.
Ludäscher, P., Greffrath, W., Schmahl, C., Kleindienst, N., Kraus, A., Baumgartner, U., … Bohus, M. (2009). A cross-sectional investigation of discontinuation of self-injury and normalizing pain perception in women with borderline personality disorder. Acta Psychiatrica Scandinavica, 120, 62-70.
Ludäscher, P., Valerius, G., Stiglmayr, C., Mauchnik, J., Lanius, R. A., Bohus, M., & Schmahl, C. (2010). Pain sensitivity and neural processing during dissociative states in women with borderline personality disorder with and without comorbid posttraumatic stress disorder: A pilot study. Journal of Psychiatry and Neuroscience, 35, 177.
Ludäscher, P., von Kalckreuth, C., Parzer, P., Kaess, M., Resch, F., Bohus, M., … Brunner, R. (2015). Pain perception in female adolescents with borderline personality disorder. European Child and Adolescent Psychiatry, 24, 351-357. https://doi.org/10.1007/s00787-014-0585-0
Magerl, W., Burkart, D., Fernandez, A., Schmidt, L. G., & Treede, R. D. (2012). Persistent antinociception through repeated self-injury in women with borderline personality disorder. Pain, 153, 575-584.
Mainero, C., Boshyan, J., & Hadjikhani, N. (2011). Altered functional magnetic resonance imaging resting-state connectivity in periaqueductal gray networks in migraine. Annals of Neurology, 70, 838-845. https://doi.org/10.1002/ana.22537
Naoum, J., Kleindienst, N., Baumgärtner, U., Willis, F., Mancke, F., Treede, R. D., … Schmahl, C. (2018). Effects of a painful stimulus on stress regulation in male patients with borderline personality disorder: A pilot study. Journal of Personality Disorders, 23, 1-19.
Neugebauer, V. (2007). The amygdala: Different pains, different mechanisms. Pain, 127, 1-2. https://doi.org/10.1016/j.pain.2006.10.004
Niedtfeld, I., Kirsch, P., Schulze, L., Herpertz, S. C., Bohus, M., & Schmahl, C. (2012). Functional connectivity of pain-mediated affect regulation in Borderline Personality Disorder. PLoS ONE, 7, e33293. https://doi.org/10.1371/journal.pone.0033293
Niedtfeld, I., Schulze, L., Kirsch, P., Herpertz, S. C., Bohus, M., & Schmahl, C. (2010). Affect regulation and pain in borderline personality disorder: A possible link to the understanding of self-injury. Biological Psychiatry, 68, 383-391. https://doi.org/10.1016/j.biopsych.2010.04.015
Niedtfeld, I., Schulze, L., Krause-Utz, A., Demirakca, T., Bohus, M., & Schmahl, C. (2013). Voxel-based morphometry in women with borderline personality disorder with and without comorbid posttraumatic stress disorder. PLoS ONE, 8, e65824. https://doi.org/10.1371/journal.pone.0065824
Ossipov, M. H., Morimura, K., & Porreca, F. (2014). Descending pain modulation and chronification of pain. Current Opinion in Supportive and Palliative Care, 8, 143-151.
Pavony, M. T., & Lenzenweger, M. F. (2014). Somatosensory processing and borderline personality disorder: Pain perception and a signal detection analysis of proprioception and exteroceptive sensitivity. Personality Disorders, 5, 164-171. https://doi.org/10.1037/per0000017
Prossin, A. R., Love, T. M., Koeppe, R. A., Zubieta, J. K., & Silk, K. R. (2010). Dysregulation of regional endogenous opioid function in borderline personality disorder. American Journal of Psychiatry, 167, 925-933. https://doi.org/10.1176/appi.ajp.2010.09091348
Reitz, S., Kluetsch, R., Niedtfeld, I., Knorz, T., Lis, S., Paret, C., … Schmahl, C. (2015). Incision and stress regulation in borderline personality disorder: Neurobiological mechanisms of self-injurious behavior. British Journal of Psychiatry, 207, 165-172.
Ruocco, A. C., Amirthavasagam, S., Choi-Kain, L. W., & McMain, S. F. (2013). Neural correlates of negative emotionality in borderline personality disorder: An activation-likelihood estimation meta-analysis. Biological Psychiatry, 73, 153-160. https://doi.org/10.1016/j.biopsych.2012.07.014
Russ, M. J., Campbell, S. S., Kakuma, T., Harrison, K., & Zanine, E. (1999). EEG theta activity and pain insensitivity in self-injurious borderline women. Psychiatry Research, 89, 201-214.
Russ, M. J., Roth, S. D., Lerman, A., Kakuma, T., Harrison, K., Shindledecker, R. D., … Mattis, S. (1992). Pain perception in self-injurious women with borderline personality disorder. Biological Psychiatry, 32, 501-511.
Sandkuhler, J., Chen, J. G., Cheng, G., & Randic, M. (1997). Low-frequency stimulation of afferent A delta-fibers induces long-term depression at primary afferent synapses with substantia gelatinosa neurons in the rat. Journal of Neuroscience, 17, 6483-6491.
Sanislow, C. A., Grilo, C. M., Morey, L. C., Bender, D. S., Skodol, A. E., Gunderson, J. G., … McGlashan, T. H. (2002). Confirmatory factor analysis of DSM-IV criteria for borderline personality disorder: Findings from the collaborative longitudinal personality disorders study. American Journal of Psychiatry, 159, 284-290. https://doi.org/10.1176/appi.ajp.159.2.284
Schloss, N., Shabes, P., Kuniss, S., Willis, F., Treede, R. D., Schmahl, C., & Baumgärtner, U. (2019). Differential perception of sharp pain in patients with borderline personality disorder. European Journal of Pain, 23(8), 1448-1463. https://doi.org/10.1002/ejp.1411
Schmahl, C., & Baumgärtner, U. (2015). Pain in borderline personality disorder. In D. P. Finn & E. Leonard Brian (Eds.), Pain in Psychiatric Disorders. Mod Trends Pharmacopsychiatry, Vol. 30 (pp. 166-175). Basel: Karger Publishers.
Schmahl, C., Bohus, M., Esposito, F., Treede, R. D., Di Salle, F., Greffrath, W., … Seifritz, E. (2006). Neural correlates of antinociception in borderline personality disorder. Archives of General Psychiatry, 63, 659-666. https://doi.org/10.1001/archpsyc.63.6.659
Schmahl, C., Herpertz, S. C., Bertsch, K., Ende, G., Flor, H., Kirsch, P., … Bohus, M. (2014). Mechanisms of disturbed emotion processing and social interaction in borderline personality disorder: State of knowledge and research agenda of the German Clinical Research Unit. Borderline Personal Disord Emot Dysregul, 1, 12. https://doi.org/10.1186/2051-6673-1-12
Schmahl, C., Meinzer, M., Zeuch, A., Fichter, M., Cebulla, M., Kleindienst, N., … Bohus, M. (2010). Pain sensitivity is reduced in borderline personality disorder, but not in posttraumatic stress disorder and bulimia nervosa. The World Journal of Biological Psychiatry, 11, 364-371. https://doi.org/10.3109/15622970701849952
Schmahl, C. G., Vermetten, E., Elzinga, B. M., & Bremner, J. D. (2004). A positron emission tomography study of memories of childhood abuse in borderline personality disorder. Biological Psychiatry, 55, 759-765. https://doi.org/10.1016/j.biopsych.2003.11.007
Schulze, L., Domes, G., Kruger, A., Berger, C., Fleischer, M., Prehn, K., … Herpertz, S. C. (2011). Neuronal correlates of cognitive reappraisal in borderline women with affective instability. Biological Psychiatry, 69, 564-573.
Silberschmidt, A., Lee, S., Zanarini, M., & Schulz, S. C. (2015). Gender differences in borderline personality disorder: Results from a multinational, clinical trial sample. Journal of Personality Disorders, 29, 828-838. https://doi.org/10.1521/pedi_2014_28_175
Villanueva, L., Bouhassira, D., & Le Bars, D. (1996). The medullary subnucleus reticularis dorsalis (SRD) as a key link in both the transmission and modulation of pain signals. Pain, 67, 231-240. https://doi.org/10.1016/0304-3959(96)03121-1
Villemure, C., & Bushnell, M. C. (2009). Mood influences supraspinal pain processing separately from attention. Journal of Neuroscience, 29, 705-715. https://doi.org/10.1523/JNEUROSCI.3822-08.2009
Weissman-Fogel, I., Dror, A., & Defrin, R. (2015). Temporal and spatial aspects of experimental tonic pain: Understanding pain adaptation and intensification. European Journal of Pain, 19, 408-418. https://doi.org/10.1002/ejp.562
Willis, F., Kuniss, S., Kleindienst, N., Naoum, J., Reitz, S., Boll, S., … Schmahl, C. (2017). The role of nociceptive input and tissue injury on stress regulation in borderline personality disorder. Pain, 158, 479-487.
Wingenfeld, K., Spitzer, C., Rullkötter, N., & Löwe, B. (2010). Borderline personality disorder: Hypothalamus pituitary adrenal axis and findings from neuroimaging studies. Psychoneuroendocrinology, 35, 154-170.
Yarnitsky, D. (2010). Conditioned pain modulation (the diffuse noxious inhibitory control-like effect): Its relevance for acute and chronic pain states. Current Opinion in Anaesthesiology, 23, 611-615. https://doi.org/10.1097/ACO.0b013e32833c348b
You, D. S., & Meagher, M. W. (2017). Association Between Borderline Personality Features and Temporal Summation of Second Pain: A Cross-Sectional Study. Behavioral Medicine, 43, 208-217.
Youssef, A. M., Macefield, V. G., & Henderson, L. A. (2016). Pain inhibits pain; human brainstem mechanisms. NeuroImage, 124, 54-62. https://doi.org/10.1016/j.neuroimage.2015.08.060