Cerebral Temperature Dysregulation: MR Thermographic Monitoring in a Nonhuman Primate Study of Acute Ischemic Stroke

S. Dehkharghani; C.C. Fleischer; D. Qiu; M. Yepes; F. Tong

doi:10.3174/ajnr.A5059

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Fig 1.
MR thermographs in subject 3 obtained during t⁻⁷ (A) and t⁰ (B) sessions, overlaid on T1-MPRAGE images. Terminal DWI (C) obtained at the conclusion of the t⁰ session following endovascular stroke induction demonstrates a large MCA territory infarction. Thermographs in A and B are presented in equivalent color scales, depicting voxelwise brain versus systemic temperature gradients. Disturbance to the geographic distribution of brain temperature gradients present during physiologic t⁰ conditions are present, with notable, diffuse cerebral hyperthermia affecting both hemispheres in B. Generalized cerebral heating following infarction corresponds to significant elevation above decoupled systemic temperatures (not shown) as a function of time and infarction volume (see text).
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Fig 2.
Subject-specific absolute temperature versus time for paired prestroke and stroke sessions. For each subject, the vertical columns represent t⁰ above and t⁻⁷ below. The y-axis in t⁰ plots represents MR imaging–derived temperatures for the hemisphere ipsilateral and contralateral to the infarction, as well as systemic temperatures. All plots are presented in the same vertical scale, with errors bars (SD) as indicated. The final time point in all t⁰ plots represents values from the poststroke session. Progressive heating of both cerebral hemispheres is present in all 3 subjects, outpacing the progressive systemic febrile temperatures in stroke aftermath. Brain hyperthermia is noted to resolve in the t¹ session for all subjects. By comparison, all baseline t⁻⁷ scans exhibit closely coupled brain systemic temperatures, despite fluctuations related to early postanesthetic hypothermia during subject preparation.
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Fig 3.
Aggregated fit from individual regressions from each subject, depicted for systemic temperatures, average hemispheric temperature ipsilateral and contralateral to infarction, and those voxels defined within the infarction territory. Individual regressions derived from a linear fixed-effects model demonstrate highly significant associations among all variables relative to time, as well as significant differences between brain temperatures and systemic temperatures following multiple-comparison correction (Table 2).
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Fig 4.
Subject-specific histograms of hemispheric cerebral temperature versus time reflecting divergence of systemic and brain temperatures. The x-axis represents the brain-systemic temperature offset, represented respectively for the initial and final time points, both for ipsilateral and contralateral brain temperatures. The rightward shift of all histograms reflects progressive cerebral hyperthermia decoupled from systemic temperatures present for both hemispheres of all 3 subjects.

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Table 1:

Subject-specific temperature and infarction volumes^{^a}

Parameter	Subject 1	Subject 2	Subject 3
T⁻⁷ scan session
Systemic temperature range	36.3–37.2	36.8–37.9	36.0–38.2
Mean brain temperature range	36.6 ± 1.0–37.1 ± 1.2	36.7 ± 0.6–37.8 ± 1.1	36.3 ± 0.7–38.8 ± 0.7
Temperature difference: brain, systemic^{^b}	−0.1 ± 1.2–0.2 ± 1.0	−0.1 ± 0.6–0.4 ± 1.1	0.3 ± 0.7–1.2 ± 0.7
T⁰ scan session
Infarct volume 1 hr postsurgery (cm³)	0.42	0.28	6.70
Systemic temperature range	36.7–37.6	36.4–38.4	35.7–38.8
Mean ipsilateral brain temperature range	37.4 ± 1.1–40.7 ± 1.4	34.3 ± 1.1–40.3 ± 1.2	35.9 ± 0.6–41.6 ± 2.9
Mean contralateral brain temperature range	37.4 ± 0.8–40.4 ± 0.7	34.1 ± 1.0–40.4 ± 0.7	35.8 ± 0.5–42.2 ± 1.8
Temperature difference: ipsilateral brain, systemic	0.7 ± 1.1–3.2 ± 1.4	−2.1 ± 1.1–2.5 ± 1.3	0.2 ± 0.6–2.8 ± 2.9
Temperature difference: contralateral brain, systemic	0.7 ± 0.8–3.0 ± 0.7	−2.3 ± 1.0–2.3 ± 1.2	0.1 ± 0.5–3.4 ± 1.8
T¹ scan session
Infarct volume 24 hr postsurgery (cm³)	23.82	1.29	25.58
Systemic temperature	35.6	35.1	34.6
Mean brain temperature	37.9 ± 1.0	36.9 ± 1.2	36.3 ± 0.9
Temperature difference: brain, systemic	2.3 ± 1.0	1.7 ± 1.2	1.7 ± 0.9

↵a All temperatures are reported in degrees Celsius. Reported temperature ranges represent the full dynamic range from the indicated imaging session beginning from matched initial systemic and imaging temperature time points.
↵b Indicates a range of systemic-versus-brain temperature offsets.

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Table 2:

Absolute systemic and cerebral temperatures versus time^{^a}

Temperature Parameter	Slope (°C/hr)	Intercept (°C)	F-Stat of Regression (df)	P Value (F-Stat)	Difference in Slope versus Systemic Temperature	P Value of Difference versus Systemic
Systemic	0.352 (0.062)	35.9 (0.3)	32.2 (1,13)	<.0005^{^b}	NA	NA
Ipsilateral brain	0.791 (0.116)	35.8 (0.5)	47.0 (1,13)	<.0005^{^b}	0.439 (0.156)	.007^{^b}
Contralateral brain	0.824 (0.129)	35.8 (0.5)	40.7 (1,13)	<.0005^{^b}	0.471 (0.156)	.004^{^b}
DWI infarct core	0.838 (0.122)	35.9 (0.5)	47.5 (1,13)	<.0005^{^b}	0.486 (0.156)	.003^{^b}

Note:—F-Stat indicates F-statistic; NA, not applicable.
↵a Parameter estimates (standard error when applicable) from a linear fixed-effects model reported relative to normalized time since stroke onset (defined at initiation of scanning 1 hour following stroke induction).
↵b Indicates statistical significance at P < .05, results of 2-tailed t test of F-statistics.