Pathophysiology and principles of management of the many faces of the acute vaso-occlusive crisis in patients with sickle cell disease

European Journal of Haematology

Volumn 95, Issue 2, 2015, Pages 113-123

  Ballas, Samir K ^a  

^a THOMAS JEFFERSON UNIVERSITY HOSPITAL   (United States)

Author keywords

Central sensitization; Glial activation; N methyl d aspartic acid receptor; Pain; Pharmacogenomics; Sickle cell anemia; Sickle cell disease; Sodium channels; Vaso occlusive crisis

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CYTOCHROME P450; HYDROMORPHONE; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OPIATE; OXYMORPHONE; NARCOTIC ANALGESIC AGENT;

ACUTE DISEASE; ARTICLE; CENTRAL SENSITIZATION; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; GLIA; GLUCURONIDATION; HUMAN; MEMBRANE DEPOLARIZATION; NONHUMAN; PATHOPHYSIOLOGY; PHARMACOGENOMICS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; SENSITIZATION; SICKLE CELL ANEMIA; VASO OCCLUSIVE CRISIS; PAIN; PHARMACOGENETICS;

ANALGESICS, OPIOID; ANEMIA, SICKLE CELL; HUMANS; PAIN; PHARMACOGENETICS;

EID: 84935493549     PISSN: 09024441     EISSN: 16000609     Source Type: Journal    
DOI: 10.1111/ejh.12460     Document Type: Article

References (93)

1. Scott RB. Health care priority and sickle cell anemia. JAMA 1970;214:731-4.
2. Prabhakar H, Haywood C Jr, Molokie R. Sickle cell disease in the United States: looking back and forward at 100 years of progress in management and survival. Am J Hematol 2010;85:346-53.
3. Mehari A, Gladwin MT, Tian X, Machado RF, Kato GJ. Mortality in adults with sickle cell disease and pulmonary hypertension. JAMA 2012;307:1254-6.
4. Steinberg MH, McCarthy WF, Castro O, et al. The risks and benefits of long-term use of hydroxyurea in sickle cell anemia: a 17.5 year follow-up. Am J Hematol 2010;85:403-8.
5. Ballas SK, Gupta K, Adams-Graves P. Sickle cell pain: a critical reappraisal. Blood 2012;120:3647-56.
6. Ballas SK. Sickle Cell Pain, 2nd edn. Washington, DC: International Association for the Study of Pain, 2014.
7. Charache S, Terrin ML, Moore RD, Dover GJ, Barton FB, Eckert SV, McMahon RP, Bonds DR. Effect of hydroxyurea on the frequency of painful crises in sickle cell anemia. Investigators of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia. N Engl J Med 1995;332:1317-22.
8. Bille BS. Migraine in school children. A study of the incidence and short-term prognosis, and a clinical, psychological and electroencephalographic comparison between children with migraine and matched controls. Acta Paediatr Suppl 1962;136:1-151.
9. Headache Classification Subcommittee of the International Headache Society. The International Classification of Headache Disorders: 2nd edition. Cephalalgia 2004;24(Suppl 1):9-160.
10. Ballas SK, Lieff S, Benjamin LJ, et al. Definitions of the phenotypic manifestations of sickle cell disease. Am J Hematol 2010;85:6-13.
11. Minniti CP, Eckman J, Sebastiani P, Steinberg MH, Ballas SK. Leg ulcers in sickle cell disease. Am J Hematol 2010;85:831-3.
12. Ballas SK, Talacki CA, Rao VM, Steiner RM. The prevalence of avascular necrosis in sickle cell anemia: correlation with alpha-thalassemia. Hemoglobin 1989;13:649-55.
13. Milner PF, Kraus AP, Sebes JI, Sleeper LA, Dukes KA, Embury SH, Bellevue R, Koshy M, Moohr JW, Smith J. Sickle cell disease as a cause of osteonecrosis of the femoral head. N Engl J Med 1991;325:1476-81.
14. Ballas SK, Darbari DS. Neuropathy, neuropathic pain, and sickle cell disease. Am J Hematol 2013;88:927-9.
15. Okuyucu EE, Turhanoglu A, Duman T, Kaya H, Melek IM, Yilmazer S. Peripheral nervous system involvement in patients with sickle cell disease. Eur J Neurol 2009;16:814-8.
16. Argoff CE, Cole BE, Fishbain DA, Irving GA. Diabetic peripheral neuropathic pain: clinical and quality-of-life issues. Mayo Clin Proc 2006;81(4 Suppl):S3-11.
17. Erbas T, Ertas M, Yucel A, Keskinaslan A, Senocak M. Prevalence of peripheral neuropathy and painful peripheral neuropathy in Turkish diabetic patients. J Clin Neurophysiol 2011;28:51-5.
18. Veves A, Backonja M, Malik RA. Painful diabetic neuropathy: epidemiology, natural history, early diagnosis, and treatment options. Pain Med 2008;9:660-74.
19. Bouhassira D, Attal N, Alchaar H, et al. Comparison of pain syndromes associated with nervous or somatic lesions and development of a new neuropathic pain diagnostic questionnaire (DN4). Pain 2005;114:29-36.
20. Spallone V, Morganti R, D'Amato C, Greco C, Cacciotti L, Marfia GA. Validation of DN4 as a screening tool for neuropathic pain in painful diabetic polyneuropathy. Diabet Med 2012;29:578-85.
21. Bennett M. The LANSS Pain Scale: the Leeds assessment of neuropathic symptoms and signs. Pain 2001;92:147-57.
22. de Moraes Vieira EB, Garcia JB, daSilva AA, Mualem Araujo RL, Jansen RC. Prevalence, characteristics, and factors associated with chronic pain with and without neuropathic characteristics in Sao Luis, Brazil. J Pain Symptom Manage 2012;44:239-51.
23. Kohli DR, Li Y, Khasabov SG, et al. Pain-related behaviors and neurochemical alterations in mice expressing sickle hemoglobin: modulation by cannabinoids. Blood 2010;116:456-65.
24. Hillery CA, Kerstein PC, Vilceanu D, Barabas ME, Retherford D, Brandow AM, Wandersee NJ, Stucky CL. Transient receptor potential vanilloid 1 mediates pain in mice with severe sickle cell disease. Blood 2011;118:3376-83.
25. Fields HL. Pain. New York, NY: McGraw-Hill, 1987.
26. Fishman SM, Ballantyne JC, Rathmell JP. Bonica's Management of Pain, 4th edn. Philadelphia, PA: Walters Kluwer, 2010.
27. Katz N, Ferrrante F. Nociception. In: Ferrante FM, VadeBoncoeur TR, eds. Post Operative Pain Management. New York, NY: Churchill-Livingstone; 1993:17-67.
28. McMahon SB, Koltzenburg M. Wall and Melzack's Textbook of Pain, 5th edn. Philadelphia, PA: Elsevier Churchill Livingstone, 2006.
29. Wall PD, Melzack R. Textbook of Pain, 3rd edn. New York, NY: Churchill Livingstone, 1994.
30. Southall MD, Li T, Gharibova LS, Pei Y, Nicol GD, Travers JB. Activation of epidermal vanilloid receptor-1 induces release of proinflammatory mediators in human keratinocytes. J Pharmacol Exp Ther 2003;304:217-22.
31. Strichartz G. Beyond neurons: the complex sources of pain transduction. Pain 2010;148:180-1.
32. Cousins MJ, John J. Bonica distinguished lecture. Acute pain and the injury response: immediate and prolonged effects. Reg Anesth 1989;14:162-79.
33. Cousins MJ. Acute post operative pain. In: Wall PD, Melzack R, eds. Textbook of Pain, 3rd edn. New York, NY: Churchill Livingstone; 1994:357-85.
34. Levin J, Taiwo Y. Inflammatory pain. In: Wall PD, Melzack R, eds. Textbook of Pain, 2nd edn. New York, NY: Churchill Livingstone; 1994:45-56.
35. Cox JJ, Reimann F, Nicholas AK, et al. An SCN9A channelopathy causes congenital inability to experience pain. Nature 2006;444:894-8.
36. Black JA, Nikolajsen L, Kroner K, Jensen TS, Waxman SG. Multiple sodium channel isoforms and mitogen-activated protein kinases are present in painful human neuromas. Ann Neurol 2008;64:644-53.
37. Breedlove SM, Watson NV. Biological Psychology: An Introduction to Behavioral, Cognitive, and Clinical Neuroscience, 7th edn. Sunderland, MA: Sinauer Associates, Inc; 2013.
38. Uprety D, Baber A, Foy M. Ketamine infusion for sickle cell pain crisis refractory to opioids: a case report and review of literature. Ann Hematol 2014;93:769-71.
39. Tawfic QA, Faris AS, Kausalya R. The role of a low-dose ketamine-midazolam regimen in the management of severe painful crisis in patients with sickle cell disease. J Pain Symptom Manage 2014;47:334-40.
40. McCance-Katz EF. (R)-methadone versus racemic methadone: what is best for patient care? Addiction 2011;106:687-8.
41. Inturrisi CE. Pharmacology of methadone and its isomers. Minerva Anestesiol 2005;71:435-7.
42. Hahnenkamp K, Durieux ME, Hahnenkamp A, Schauerte SK, Hoenemann CW, Vegh V, Theilmeier G, Hollmann MW. Local anaesthetics inhibit signalling of human NMDA receptors recombinantly expressed in Xenopus laevis oocytes: role of protein kinase C. Br J Anaesth 2006;96:77-87.
43. Furutani K, Kohno T. Local anesthetics inhibit NMDA-mediated glutamatergic transmission in spinal dorsal horn neurons. Masui 2011;60(Suppl):S151-8.
44. Gronwald C, Vegh V, Hollmann MW, Hahnenkamp A, Garaj V, Hahnenkamp K. The inhibitory potency of local anesthetics on NMDA receptor signalling depends on their structural features. Eur J Pharmacol 2012;674:13-9.
45. Busse S, Brix B, Kunschmann R, Bogerts B, Stoecker W, Busse M. N-methyl-d-aspartate glutamate receptor (NMDA-R) antibodies in mild cognitive impairment and dementias. Neurosci Res 2014;85:58-64.
46. Shim JH. Clinical application of α2-δ ligand. Hanyang Med Rev 2011;31:55-62.
47. Leipold E, Liebmann L, Korenke GC, et al. A de novo gain-of-function mutation in SCN11A causes loss of pain perception. Nat Genet 2013;45:1399-404.
48. Yang Y, Wang Y, Li S, et al. Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia. J Med Genet 2004;41:171-4.
49. Dib-Hajj SD, Rush AM, Cummins TR, Hisama FM, Novella S, Tyrrell L, Marshall L, Waxman SG. Gain-of-function mutation in Nav1.7 in familial erythromelalgia induces bursting of sensory neurons. Brain 2005;128:1847-54.
50. Halfor B. Human genetic studies point drug makers to a specific sodium channel target for painkillers. C & EN. 2014; (March 14).
51. Yale SH, Nagib N, Guthrie T. Approach to the vaso-occlusive crisis in adults with sickle cell disease. Am Fam Physician 2000;61:1349-56, 63-4.
52. McClish DK, Smith WR, Dahman BA, Levenson JL, Roberts JD, Penberthy LT, Aisiku IP, Roseff SD, Bovbjerg VE. Pain site frequency and location in sickle cell disease: the PiSCES project. Pain 2009;145:246-51.
53. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009;10:895-926.
54. Woolf CJ. Evidence for a central component of post-injury pain hypersensitivity. Nature 1983;306:686-8.
55. Woolf CJ. Generation of acute pain: central mechanisms. Br Med Bull 1991;47:523-33.
56. Woolf CJ. Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology 2007;106:864-7.
57. Restak R. Optimizing Brain Fittness. Chantilly, VA: The Great Courses, 2011.
58. Hsieh MM, Kang EM, Fitzhugh CD, Link MB, Bolan CD, Kurlander R, Childs RW, Rodgers GP, Powell JD, Tisdale JF. Allogeneic hematopoietic stem-cell transplantation for sickle cell disease. N Engl J Med 2009;361:2309-17.
59. Miller G. Neuroscience. The dark side of glia. Science 2005;308:778-81.
60. Watkins LR, Maier SF. Glia: a novel drug discovery target for clinical pain. Nat Rev Drug Discov 2003;2:973-85.
61. Rolan P, Hutchinson M, Johnson K. Ibudilast: a review of its pharmacology, efficacy and safety in respiratory and neurological disease. Expert Opin Pharmacother 2009;10:2897-904.
62. Rolan P, Gibbons JA, He L, Chang E, Jones D, Gross MI, Davidson JB, Sanftner LM, Johnson KW. Ibudilast in healthy volunteers: safety, tolerability and pharmacokinetics with single and multiple doses. Br J Clin Pharmacol 2008;66:792-801.
63. Hollenberg PF. Characteristics and common properties of inhibitors, inducers, and activators of CYP enzymes. Drug Metab Rev 2002;34:17-35.
64. Smith HS. Opioid metabolism. Mayo Clin Proc 2009;84:613-24.
65. Bertilsson L, Lou YQ, Du YL, Liu Y, Kuang TY, Liao XM, Wang KY, Reviriego J, Iselius L, Sjoqvist F. Pronounced differences between native Chinese and Swedish populations in the polymorphic hydroxylations of debrisoquin and S-mephenytoin. Clin Pharmacol Ther 1992;51:388-97.
66. Evans DA, Mahgoub A, Sloan TP, Idle JR, Smith RL. A family and population study of the genetic polymorphism of debrisoquine oxidation in a white British population. J Med Genet 1980;17:102-5.
67. Heiskanen T, Olkkola KT, Kalso E. Effects of blocking CYP2D6 on the pharmacokinetics and pharmacodynamics of oxycodone. Clin Pharmacol Ther 1998;64:603-11.
68. Janssen Pharmaceuticals Inc. Duragesic [Fentanyl Transdermal System]. US Full Prescribing Information. Titusville, NJ: Janssen Pharmaceuticals Inc., 2012.
69. Purdue Pharma LP. OxyContin [Oxycodone Hydrochloride Tablet Extended Release]. US Full Prescribing Information. Stamford, CT: Purdue Pharma LP, 2013.
70. Crettol S, Deglon JJ, Besson J, Croquette-Krokar M, Hammig R, Gothuey I, Monnat M, Eap CB. ABCB1 and cytochrome P450 genotypes and phenotypes: influence on methadone plasma levels and response to treatment. Clin Pharmacol Ther 2006;80:668-81.
71. Foster DJ, Somogyi AA, Bochner F. Methadone N-demethylation in human liver microsomes: lack of stereoselectivity and involvement of CYP3A4. Br J Clin Pharmacol 1999;47:403-12.
72. Li Y, Kantelip JP, Gerritsen-van Schieveen P, Davani S. Interindividual variability of methadone response: impact of genetic polymorphism. Mol Diagn Ther 2008;12:109-24.
73. Totah RA, Allen KE, Sheffels P, Whittington D, Kharasch ED. Enantiomeric metabolic interactions and stereoselective human methadone metabolism. J Pharmacol Exp Ther 2007;321:389-99.
74. Wang JS, DeVane CL. Involvement of CYP3A4, CYP2C8, and CYP2D6 in the metabolism of (R)- and (S)-methadone in vitro. Drug Metab Dispos 2003;31:742-7.
75. Daly AK, Brockmoller J, Broly F, et al. Nomenclature for human CYP2D6 alleles. Pharmacogenetics 1996;6:193-201.
76. Crews KR, Gaedigk A, Dunnenberger HM, Klein TE, Shen DD, Callaghan JT, Kharasch ED, Skaar TC. Clinical Pharmacogenetics Implementation Consortium (CPIC) guidelines for codeine therapy in the context of cytochrome P450 2D6 (CYP2D6) genotype. Clin Pharmacol Ther 2012;91:321-6.
77. Neafsey P, Ginsberg G, Hattis D, Sonawane B. Genetic polymorphism in cytochrome P450 2D6 (CYP2D6): population distribution of CYP2D6 activity. J Toxicol Environ Health B Crit Rev 2009;12:334-61.
78. Brousseau DC, McCarver DG, Drendel AL, Divakaran K, Panepinto JA. The effect of CYP2D6 polymorphisms on the response to pain treatment for pediatric sickle cell pain crisis. J Pediatr 2007;150:623-6.
79. Joly P, Gagnieu MC, Bardel C, Francina A, Pondarre C, Martin C. Genotypic screening of the main opiate-related polymorphisms in a cohort of 139 sickle cell disease patients. Am J Hematol 2012;87:534-6.
80. Shord SS, Cavallari LH, Gao W, Jeong HY, Deyo K, Patel SR, Camp JR, Labott SM, Molokie RE. The pharmacokinetics of codeine and its metabolites in Blacks with sickle cell disease. Eur J Clin Pharmacol 2009;65:651-8.
81. Kilpatrick GJ, Smith TW. Morphine-6-glucuronide: actions and mechanisms. Med Res Rev 2005;25:521-44.
82. van Dorp EL, Romberg R, Sarton E, Bovill JG, Dahan A. Morphine-6-glucuronide: morphine's successor for postoperative pain relief? Anesth Analg 2006;102:1789-97.
83. Crawford MW, Galton S, Naser B. Postoperative morphine consumption in children with sickle-cell disease. Paediatr Anaesth 2006;16:152-7.
84. Dampier CD, Setty BN, Logan J, Ioli JG, Dean R. Intravenous morphine pharmacokinetics in pediatric patients with sickle cell disease. J Pediatr 1995;126:461-7.
85. Wienkers LC, Heath TG. Predicting in vivo drug interactions from in vitro drug discovery data. Nat Rev Drug Discov 2005;4:825-33.
86. McDonough PC, Holler JM, Vorce SP, Bosy TZ, Magluilo J Jr, Past MR. The detection and quantitative analysis of the psychoactive component of Salvia divinorum, salvinorin A, in human biological fluids using liquid chromatography-mass spectrometry. J Anal Toxicol 2008;32:417-21.
87. Doehring A, Freynhagen R, Griessinger N, Zimmermann M, Sittl R, Hentig N, Geisslinger G, Lotsch J. Cross-sectional assessment of the consequences of a GTP cyclohydrolase 1 haplotype for specialized tertiary outpatient pain care. Clin J Pain 2009;25:781-5.
88. Bockaert J, Pin JP. Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 1999;18:1723-9.
89. Klepstad P, Rakvag TT, Kaasa S, Holthe M, Dale O, Borchgrevink PC, Baar C, Vikan T, Krokan HE, Skorpen F. The 118 A > G polymorphism in the human mu-opioid receptor gene may increase morphine requirements in patients with pain caused by malignant disease. Acta Anaesthesiol Scand 2004;48:1232-9.
90. Lotsch J, Skarke C, Grosch S, Darimont J, Schmidt H, Geisslinger G. The polymorphism A118G of the human mu-opioid receptor gene decreases the pupil constrictory effect of morphine-6-glucuronide but not that of morphine. Pharmacogenetics 2002;12:3-9.
91. Skarke C, Darimont J, Schmidt H, Geisslinger G, Lotsch J. Analgesic effects of morphine and morphine-6-glucuronide in a transcutaneous electrical pain model in healthy volunteers. Clin Pharmacol Ther 2003;73:107-21.
92. Pergolizzi JV, Raffa RB. Common opioid-drug interactions: what clinicians need to know. Pract Pain Manag 2012;12:59-73.
93. Rakvag TT, Klepstad P, Baar C, Kvam TM, Dale O, Kaasa S, Krokan HE, Skorpen F. The Val158Met polymorphism of the human catechol-O-methyltransferase (COMT) gene may influence morphine requirements in cancer pain patients. Pain 2005;116:73-8.