Sensory neurons of the human brachial plexus: A quantitative study employing optical fractionation and in vivo volumetric magnetic resonance imaging

Neurosurgery

Volumn 70, Issue 5, 2012, Pages 1183-1194

  West, Christian Alexander ^a,b,c   McKay Hart, Andrew ^a,d,e   Terenghi, Giorgio ^c   Wiberg, Mikael ^a,b  

^a UMEÅ UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e CANNIESBURN PLASTIC SURGERY UNIT   (United Kingdom)

Author keywords

Dorsal root ganglia; Human; Magnetic resonance imaging; Nerve trauma; Neuroprotection; Sensory neuron death

Indexed keywords

ADULT; ARTICLE; BRACHIAL PLEXUS; CADAVER; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; DORSAL ROOT; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INNERVATION; INTERMETHOD COMPARISON; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTICAL FRACTIONATION; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; QUANTITATIVE STUDY; SENSORY NERVE CELL; SEX DIFFERENCE; VERTEBRAL ARTERY; VOLUMETRY;

ADULT; BRACHIAL PLEXUS; CADAVER; CELL COUNT; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; SENSORY RECEPTOR CELLS;

EID: 84860307748     PISSN: 0148396X     EISSN: None     Source Type: Journal    
DOI: 10.1227/NEU.0b013e318241ace1     Document Type: Article

References (56)

1. Hart AM, Terenghi G, Wiberg M. Neuronal death after peripheral nerve injury and experimental strategies for neuroprotection. Neurol Res. 2008;30(10): 999-1011.
2. McKay HA, Brannstrom T, Wiberg M, Terenghi G. Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat: time course of cell death and elimination. Exp Brain Res. 2002;142(3):308-318. (Pubitemid 34117811)
3. Suzuki H, Oyanagi K, Takahashi H, Kono M, Yokoyama M, Ikuta F. A quantitative pathological investigation of the cervical cord, roots and ganglia after long-term amputation of the unilateral upper arm. Acta Neuropathol. 1993;85(6): 666-673. (Pubitemid 23212036)
4. Hart AM, Terenghi G, Kellerth JO, Wiberg M. Sensory neuroprotection, mitochondrial preservation, and therapeutic potential of N-acetyl-cysteine after nerve injury. Neuroscience. 2004;125(1):91-101. (Pubitemid 38402162)
5. Wilson AD, Hart A, Brannstrom T, Wiberg M, Terenghi G. Primary sensory neuronal rescue with systemic acetyl-L-carnitine following peripheral axotomy. A dose-response analysis. Br J Plast Surg. 2003;56(8):732-739. (Pubitemid 37461623)
6. Aberg M, Ljungberg C, Edin E, et al. Considerations in evaluating new treatment alternatives following peripheral nerve injuries: a prospective clinical study of methods used to investigate sensory, motor and functional recovery. J Plast Reconstr Aesthet Surg. 2007;60(2):103-113. (Pubitemid 46076041)
7. Schenker M, Riederer BM, Kuntzer T, Barakat-Walter I. Thyroid hormones stimulate expression and modification of cytoskeletal protein during rat sciatic nerve regeneration. Brain Res. 2002;957(2):259-270. (Pubitemid 35356521)
8. West CA, Davies KA, Hart AM, Wiberg M, Williams SR, Terenghi G. Volumetric magnetic resonance imaging of dorsal root ganglia for the objective quantitative assessment of neuron death after peripheral nerve injury. Exp Neurol. 2006;203(1): 22-33. (Pubitemid 44821160)
9. Hart AM, Terenghi G. Frozen-section fluorescence microscopy and stereology in the quantification of neuronal death within dorsal root ganglia. J Mol Histol. 2004; 35(6):565-580. (Pubitemid 41404642)
10. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec. 1991;231(4):482-497.
11. Dorph-Petersen KA, Nyengaard JR, Gundersen HJ. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc. 2001; 204(pt 3):232-246. (Pubitemid 34075121)
12. Gundersen HJ, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987;147(pt 3):229-263.
13. Sterio DC. The unbiased estimation of number and sizes of arbitrary particles using the dissector. J Microsc. 1984;134(pt 2):127-136. (Pubitemid 14121386)
14. Reyes O, Sosa I, Kuffler DP. Neuroprotection of adult human neurons against ischemia by hypothermia and alkalinization. P R Health Sci J. 2006;25(1):43-50.
15. Wessels WJ, Marani E. A rostrocaudal somatotopic organization in the brachial dorsal root ganglia of neonatal rats. Clin Neurol Neurosurg. 1993;95(suppl):S3-S11. (Pubitemid 23091664)
16. Wessels WJ, Feirabend HK, Marani E. The rostrocaudal organization in the dorsal root ganglia of the rat: a consequence of plexus formation? Anat Embryol (Berl). 1994;190(1):1-11. (Pubitemid 24246308)
17. Ma J, Novikov LN, Kellerth JO, Wiberg M. Early nerve repair after injury to the postganglionic plexus: an experimental study of sensory and motor neuronal survival in adult rats. Scand J Plast Reconstr Surg Hand Surg. 2003;37(1):1-9. (Pubitemid 36207762)
18. Mille-Hamard L, Bauchet L, Baillet-Derbin C, Horvat JC. Estimation of the number and size of female adult rat C4, C5 and C6 dorsal root ganglia (DRG) neurons. Somatosens Mot Res. 1999;16(3):223-228. (Pubitemid 29454460)
19. Goldstein RS. Axial level-dependent differences in size of avian dorsal root ganglia are present from gangliogenesis. J Neurobiol. 1993;24(8):1121-1129. (Pubitemid 23213690)
20. Goldstein RS, Avivi C, Geffen R. Initial axial level-dependent differences in size of avian dorsal root ganglia are imposed by the sclerotome. Dev Biol. 1995;168(1): 214-222.
21. Lee MW, McPhee RW, Stringer MD. An evidence-based approach to human dermatomes. Clin Anat. 2008;21(5):363-373. (Pubitemid 351976904)
22. Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J Neurosci. 1995;15(5 pt 2):3886-3895.
23. Natt O, Watanabe T, Boretius S, Radulovic J, Frahm J, Michaelis T. High-resolution 3D MRI of mouse brain reveals small cerebral structures in vivo. J Neurosci Methods. 2002;120(2):203-209. (Pubitemid 35248169)
24. Gadeberg P, Gundersen HJ, Tagehoj F. How accurate are measurements on MRI? A study on multiple sclerosis using reliable 3D stereological methods. J Magn Reson Imaging. 1999;10(1):72-79. (Pubitemid 29336641)
25. Marziali S, Gaudiello F, Bozzao A, et al. Evaluation of anterior pituitary gland volume in childhood using three-dimensional MRI. Pediatr Radiol. 2004;34(7): 547-551. (Pubitemid 38967793)
26. McDaniel B, Sheng H, Warner DS, Hedlund LW, Benveniste H. Tracking brain volume changes in C57BL/6J and ApoE-deficient mice in a model of neuro-degeneration: a 5-week longitudinal micro-MRI study. Neuroimage. 2001;14(6): 1244-1255. (Pubitemid 33124173)
27. Moats RA, Velan-Mullan S, Jacobs R, et al. Micro-MRI at 11.7 T of a murine brain tumor model using delayed contrast enhancement. Mol Imaging. 2003;2(3): 150-158.
28. Nagel S, Wagner S, Koziol J, Kluge B, Heiland S. Volumetric evaluation of the ischemic lesion size with serial MRI in a transient MCAO model of the rat: comparison of DWI and T1WI. Brain Res Brain Res Protoc. 2004;12(3):172-179. (Pubitemid 38316797)
29. Wolf OT, Dyakin V, Vadasz C, de Leon MJ, McEwen BS, Bulloch K. Volumetric measurement of the hippocampus, the anterior cingulate cortex, and the retrosplenial granular cortex of the rat using structural MRI. Brain Res Brain Res Protoc. 2002;10(1):41-46.
30. Eriksson SH, Free SL, Thom M, et al. Correlation of quantitative MRI and neuropathology in epilepsy surgical resection specimens-T2 correlates with neuronal tissue in gray matter. Neuroimage. 2007;37(1):48-55. (Pubitemid 47068980)
31. Saitoh O, Courchesne E, Egaas B, Lincoln AJ, Schreibman L. Cross-sectional area of the posterior hippocampus in autistic patients with cerebellar and corpus callosum abnormalities. Neurology. 1995;45(2):317-324.
32. Nemanic S, Alvarado MC, Price RE, Jackson EF, Bachevalier J. Assessment of locus and extent of neurotoxic lesions in monkeys using neuroimaging techniques: a replication. J Neurosci Methods. 2002;121(2):199-209. (Pubitemid 35418245)
33. Bobinski M, de Leon MJ, Wegiel J, et al. The histological validation of post mortem magnetic resonance imaging-determined hippocampal volume in Alzheimer's disease. Neuroscience. 2000;95(3):721-725.
34. Zarow C, Vinters HV, Ellis WG, et al. Correlates of hippocampal neuron number in Alzheimer's disease and ischemic vascular dementia. Ann Neurol. 2005;57(6): 896-903. (Pubitemid 40798628)
35. Csernansky JG, Hamstra J, Wang L, et al. Correlations between antemortem hippocampal volume and postmortem neuropathology in AD subjects. Alzheimer Dis Assoc Disord. 2004;18(4):190-195. (Pubitemid 40076147)
36. Aota Y, Onari K, An HS, Yoshikawa K. Dorsal root ganglia morphologic features in patients with herniation of the nucleus pulposus: assessment using magnetic resonance myelography and clinical correlation. Spine (Phila Pa 1976). 2001; 26 (19) 2125-2132. (Pubitemid 32936626)
37. Castillo M, Mukherji SK. MRI of enlarged dorsal ganglia, lumbar nerve roots, and cranial nerves in polyradiculoneuropathies. Neuroradiology. 1996;38(6):516-520. (Pubitemid 26288235)
38. Hamanishi C, Tanaka S. Dorsal root ganglia in the lumbosacral region observed from the axial views of MRI. Spine (Phila Pa 1976). 1993;18(13):1753-1756. (Pubitemid 23312827)
39. Hasegawa T, Mikawa Y, Watanabe R, An HS. Morphometric analysis of the lumbosacral nerve roots and dorsal root ganglia by magnetic resonance imaging. Spine (Phila Pa 1976). 1996;21(9):1005-1009. (Pubitemid 26148154)
40. Blumenthal DT, Salzman KL, Baringer JR, Forghani B, Gilden DH. MRI abnormalities in chronic active varicella zoster infection. Neurology. 2004;63(8): 1538-1539. (Pubitemid 39426306)
41. Karger CP, Hoss A, Bendl R, Canda V, Schad L. Accuracy of device-specific 2D and 3D image distortion correction algorithms for magnetic resonance imaging of the head provided by a manufacturer. Phys Med Biol. 2006;51(12):N253-N261. (Pubitemid 43885454)
42. Sumanaweera T, Glover G, Song S, Adler J, Napel S. Quantifying MRI geometric distortion in tissue. Magn Reson Med. 1994;31(1):40-47. (Pubitemid 24016939)
43. Wang D, Doddrell DM, Cowin G. A novel phantom and method for comprehensive 3-dimensional measurement and correction of geometric distortion in magnetic resonance imaging. Magn Reson Imaging. 2004;22(4):529-542. (Pubitemid 38534669)
44. Caramanos Z, Fonov VS, Francis SJ, et al. Gradient distortions in MRI: characterizing and correcting for their effects on SIENA-generated measures of brain volume change. Neuroimage. 2010;49(2):1601-1611.
45. Jovicich J, Czanner S, Greve D, et al. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage. 2006;30(2):436-443.
46. Fransson A, Andreo P, Potter R. Aspects of MR image distortions in radiotherapy treatment planning. Strahlenther Onkol. 2001;177(2):59-73. (Pubitemid 32162659)
47. Flannigan BD, Lufkin RB, McGlade C, et al. MR imaging of the cervical spine: neurovascular anatomy. AJR Am J Roentgenol. 1987;148(4):785-790. (Pubitemid 17047774)
48. Yenerich DO, Haughton VM. Oblique plane MR imaging of the cervical spine. J Comput Assist Tomogr. 1986;10(5):823-826. (Pubitemid 16020615)
49. Ygge J, Aldskogius H, Grant G. Asymmetries and symmetries in the number of thoracic dorsal root ganglion cells. J Comp Neurol. 1981;202(3):365-372. (Pubitemid 11030511)
50. Arvidsson J, Ygge J, Grant G. Cell loss in lumbar dorsal root ganglia and transganglionic degeneration after sciatic nerve resection in the rat. Brain Res. 1986;373(1-2):15-21. (Pubitemid 16039872)
51. Groves MJ, Schanzer A, Simpson AJ, An SF, Kuo LT, Scaravilli F. Profile of adult rat sensory neuron loss, apoptosis and replacement after sciatic nerve crush. J Neurocytol. 2003;32(2):113-122. (Pubitemid 38019303)
52. Gundersen HJ, Bagger P, Bendtsen TF, et al. The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS. 1988;96(10):857-881
53. Firbank MJ, Coulthard A, Harrison RM, Williams ED. Partial volume effects in MRI studies of multiple sclerosis. Magn Reson Imaging. 1999;17(4):593-601.
54. Bergman E, Ulfhake B. Loss of primary sensory neurons in the very old rat: neuron number estimates using the disector method and confocal optical sectioning. J Comp Neurol. 1998;396(2):211-222. (Pubitemid 28249172)
55. McAllister RM, Gilbert SE, Calder JS, Smith PJ. The epidemiology and management of upper limb peripheral nerve injuries in modern practice. J Hand Surg Br. 1996;21(1):4-13. (Pubitemid 26067979)
56. Rosberg HE, Carlsson KS, Hojgard S, Lindgren B, Lundborg G, Dahlin LB. Injury to the human median and ulnar nerves in the forearm-analysis of costs for treatment and rehabilitation of 69 patients in southern Sweden. J Hand Surg Br. 2005;30(1):35-39. (Pubitemid 40058052)