Abstract

BACKGROUND: We characterized, in patients with severe acute traumatic spinal cord injuries, the relationships between intraoperative spinal cord blood flow (SCBF) and postoperative injury-site metabolism and physiology, preoperative magnetic resonance imaging (MRI) features, and neurological outcome. METHODS: Twenty-six adults with severe, acute traumatic spinal cord injuries (American Spinal Injury Association Impairment Scale, grades A-C) had surgery within 72 h of injury. All had preoperative spine MRI and intraoperative laser speckle contrast imaging of SCBF. For four days after operation, we monitored from the injury site, intraspinal pressure (ISP), and spinal cord perfusion pressure (SCPP) as well as tissue metabolism with surface microdialysis. RESULTS: We observed three intraoperative SCBF patterns: necrosis-penumbra SCBF (SCBF-necr) in 34.6% of patients, patchy-perfusion SCBF (SCBF-patchy) in 38.5% of patients, and hyperperfusion SCBF (SCBF-hyper) in 26.9% of patients. On preoperative MRI, SCBF-necr was associated with higher Brain and Spinal Injury Center MRI score versus SCBF-patchy or SCBF-hyper (median 4 vs. 2 or 2.5). SCBF-necr was associated with higher postoperative ISP, lower postoperative SCPP, and more deranged postoperative injury-site metabolism (lower glucose; higher lactate, glutamate, and glycerol) than SCBF-patchy or SCBF-hyper, with little difference between SCBF-patchy and SCBF-hyper. Machine learning analysis of physiological-metabolic data considered as seven-dimensional vectors (ISP, SCPP, glucose, pyruvate, lactate, glutamate, and glycerol) accurately distinguished between the three SCBF patterns with an area under the curve of 0.85-0.95. The seven-dimensional physiological-metabolic vectors were segregated as SCBF-necr, SCBF-patchy, and SCBF-hyper in Kohonen self-organizing maps. SCBF-patchy was associated with greater improvement in motor score than SCBF-necr or SCBF-hyper (35.3 vs. 5.2 or 2.2), independent of admission American Spinal Injury Association Impairment Scale grade. CONCLUSIONS: Our findings challenge the prevailing concept in the field, derived from animal experiments, that spinal cord injury causes necrosis at the injury site with surrounding penumbra. In humans, spinal cord injury causes three abnormal SCBF patterns detected intraoperatively, with distinct postoperative physiological-metabolic signatures, preoperative MRI characteristics, and neurological outcomes.