Deconstructing Pain in Sickle Cell Disease: Sickling, Sensitivity and Centralization
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1 Deconstructing Pain in Sickle Cell Disease: Sickling, Sensitivity and Centralization Deepika S. Darbari, MD Children s National Medical Center Associate Professor of Pediatrics George Washington University School of Medicine and Health Sciences Washington DC 1
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3 Outline Pain phenotypes in sickle cell disease Chronic sickle cell disease pain represents end-organ damage Clinical phenotype vs. mechanistic classification of pain in SCD Mechanisms responsible for transition from acute to chronic pain (sickling of red cells, pain sensitivity and sensitization) Areas for future research
4 Many complications of sickle cell Pain is the most common problem African Tribal names: - Chwechweechwe (relentless perpetual chewing) - Adep (beaten up) - HemKom (body biting) Akinsheye et al. Blood 2011
5 Impact of pain in sickle cell disease Quality of life of patients and their caregivers Financial burden: Direct cost : Admissions and treatment of VOC» over 75,000 hospitalizations» over $475 million in 2004» over 1.1 billion Indirect cost : Lost productivity, missed work or school days Steiner and Miller hcup-us.ahrq.gov
6 Pain in SCD starts early Acute Pain (Dactylitis) 5 cardinal signs of acute inflammation : rubor (redness), calor (increased heat), tumor (swelling), dolor (pain), and functio laesa (loss of function) Ischemia- reperfusion physiology (reperfusion injury)
7 Increasing age: a risk factor for pain Darbari. J Pediatrics 2012
8 Chronic SCD pain: End organ damage
9 Chronic SCD pain vs. vaso-occlusive crises Smith et al Annals Int Med 2008
10 Chronic persistent pain of SCD Chronic (> 3 months) pain is common Starts in adolescents and young adult years Objective signs +/- ( AVN/ leg ulcer)/ vs. self report Comorbidities (poor sleep, anxiety, depression) Often poor response to standard therapy Underlying mechanisms: Unclear but may be related to recurrent VOC, neuropathic pain, neuroplasticity of central / peripheral nervous system altered pain processing/ perception
11 Mechanisms of pain Woolf JCI 2010
12 Acute VOC: Ischemia/Reperfusion injury 1. Ischemia induced tissue injury caused by interruption of vascular supply. 2. Reperfusion associated with resolution of occlusion and resupply of oxygen inflammatory phase systemic inflammation remote organ injury/ multi-organ dysfunction syndrome Cells involved Sickle RBC Platelets Neutrophils Monocytes Endothelial cells Mast cells Molecules/mediators Pro-inflammatory cytokines through the NF-kB pathway (TNFa, IL, endothelin-1, PG E2. Chemokines Coagulation cascade HMGB
13 Mechanisms of pain Woolf JCI 2010
14 Acute to chronic pain : A Multi level and multiple cellular processes Latremoliere and Woolf. J Pain. 2009
15 Patients with SCD are more sensitive to nociceptive stimulus Brandow. A J Hematol 2013
16 Altered pain processing in SCD Non invasive FMRI methodology An excellent tool for imaging pain, objective measure Resting state functional connectivity correlates to the time course of blood-oxygen level dependent (BOLD) MRI signal changes between various brain regions Provides insight into functionally interconnected brain networks that play role in pain (Correlation vs. anti-correlation; pronociceptive vs. antinociceptive areas) 16
17 Brain networks relevant to pain processing Salience network (SLN): Key hub of pain processing. Provides a neural representation of painful sensory stimuli, which then interacts with other brain regions for additional, elaborated processing of that information. Includes bilateral primary and secondary somatosensory areas (S1 and S2), primary motor cortex (M1), and the sensory motor area (SMA). The (A) salience network (SLN) and (B) default mode networks of the brain shown to be relevant to centralized pain. Default Mode Network (DMN): Engaged in self-referential thinking. Deactivates with task. Includes the inferior parietal lobule, the posterior cingulate cortex, precuneus, areas of the medial frontal gyri, the hippocampal formation, and the posterior lateral temporal cortex. 17
18 High pain burden and altered pain processing in SCD Low Pain group (Upper Panel): Greater negative DMN connectivity (anti-correlation) with pro-nociceptive area (insula) High Pain group (Lower Panel): Greater anti-correlation of salience network and antinociceptive area (perigenual ant cingulate) Darbari et al. J Pain 2015
19 High pain burden and altered pain processing in SCD High pain group: Greater pronociceptive connectivity (Panel A) Greater connectivity between pro-nociceptive structures such as the insula and secondary somatosensory cortex. Greater connectivity between DMN regions and pro-nociceptive pain structures Low pain group: Greater antinociceptive connectivity (Panel B) Greater connectivity between the primary somatosensory cortex and subgenual ACC (an antinociceptive region of the cingulate) (associated with endogenous analgesic mechanisms) Darbari et al. J Pain 2015
20 Hemoglobin F and connectivity patterns Non transfused patients in low pain group: High HbF was associated with greater anti-correlation Beneficial between the secondary connectivity somatosensory with cortex and precuneus. Hb F (Less pro-nociceptive connectivity) High HbF was What associated comes with greater connectivity first? between the SLN and the perigenual Pain or anterior cingulate. protective (Greater anti-nociceptive influences connectivity) Darbari et al. J Pain 2015
21 Sickle cell pain mechanisms Underlying mechanism Pain characteristics Peripheral (nociceptive) Inflammation or mechanical damage of tissues Throbbing, sharp, pounding, dull Local Peripheral neuropathic/ sensitization Damage or dysfunction of peripheral nerves Burning, heavy sensation, or numbness along the path of the affected nerve. Allodynia and hyperalgesia Central neuropathic/ sensitization Altered central pain processing Hyperalgesia/allodynia Diffuse pain Response to therapy Classic examples NSAID, opioid responsive Osteoarthritis Rheumatoid arthritis Acute SCD VOC Pain Responds to both peripheral and centrally acting pharmacological therapies, gabapentinoids Diabetic neuropathic pain Post-herpetic Chronic neuralgia SCD Pain Responsive to neuroactive compounds Fibromyalgia, IBS, TMJD, Tension headache Chronic SCD Pain Darbari Eur J Haem 2014
22 Proposed model of acute to chronic trnasition of SCD pain Nociceptive intermittent pain phenotype Neuroplasticity of brain Disease Environmental Genetics Alexander BJH 2004 Modified from Kato et al. Blood Reviews, 2007c Darbari Eur J Haem 2014 Chronic persistent pain phenotype
23 Summary Sickle cell pain mechanisms are unique Chronic sickle cell pain is common and represent end organ damage associated with SCD Transition from acute to chronic pain is a multi level and multiple cellular processes Etiology of chronic SCD pain is complex and is modified by protective/ risk factors Longitudinal studies are needed to understand chronic SCD pain
24 Acknowledgments Children and patients with sickle cell disease Children s National Medical Center, Washington, DC: Gilbert Vezina Iordanis Evangelou Nadja Kadom Nneka Okoye Juan Carlos Arroyo National Institutes of Health, NHLBI, Bethesda, MD: James Taylor Chronic Pain and Fatigue Research Center, University of Michigan at Ann Arbor: Richard E. Harris Daniel J. Clauw Johnson P. Hampson Eric Ichesco 24
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