The role of sleep quality on white matter integrity and concussion symptom severity in adolescents.

The role of sleep quality on white matter integrity and concussion symptom severity in adolescents.
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DOI:
10.1016/j.nicl.2022.103130
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发表时间:
2022
影响因子:
4.2
通讯作者:
Versace, Amelia
Versace, Amelia
中科院分区:
医学2区
文献类型:
--
作者:
Santos, Joao Paulo Lima;Kontos, Anthony P.;Holland, Cynthia L.;Stiffler, Richelle S.;Bitzer, Hannah B.;Caviston, Kaitlin;Shaffer, Madelyn;Suss, Stephen J., Jr.;Martinez, Laramie;Manelis, Anna;Iyengar, Satish;Brent, David;Ladouceur, Cecile D.;Collins, Michael W.;Phillips, Mary L.;Versace, Amelia

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睡眠不好的人在几个方面的NDI比睡眠好的人低。在受伤和扫描之间的七天后,睡眠质量的影响是显着的。睡眠良好的人与未脑震荡的对照组相比没有表现出任何差异。低NDI、睡眠不佳与较高的症状严重程度之间存在显着关系。女性和低NDI与症状的严重程度显著相关。脑震荡后的睡眠问题很常见;然而,到目前为止,还没有研究评估青少年睡眠、白色物质完整性和脑震荡后症状之间的关系。在受伤后的前10天内使用自我报告的睡眠质量测量,我们的目的是确定睡眠质量是否对主要神经束的白色物质完整性产生主要影响,通过弥散磁共振成像(dMRI)测量,并进一步检查这种影响是否有助于解释12至17.9岁青少年脑震荡后症状严重程度的差异。收集了57例脑震荡青少年(平均年龄[SD] = 15.4[1.5]岁; 41.2%为女性)的dMRI数据,这些青少年没有重大精神病诊断史。在研究入组时评估脑震荡后症状的严重程度(平均天数[SD] =受伤后3.7[2.5]天)。使用匹兹堡睡眠质量指数(PSQI),脑震荡青少年根据他们在受伤和扫描之间的睡眠质量分为两组:睡眠良好者(PSQI总分≤ 5; N = 33)和睡眠不良者(PSQI总分> 5; N = 24)。神经突方向分散和分散指数(NODDI),特别是神经突密度指数(NDI),被用来量化主要的管道,包括18个双边和一个纵裂道的微观结构特性,并确定是否存在dMRI差异,良好与穷人的睡眠。由于脑震荡和神经影像学采集之间的时间间隔在脑震荡青少年中各不相同,因此该时间间隔与睡眠组的相互作用项一起沿着纳入分析。正则化回归用于确定睡眠质量相关的dMRI测量是否与脑震荡后症状严重程度相关。由于女性中报告的脑震荡症状严重程度较高,因此将dMRI和性别之间的相互作用项纳入正则化回归模型中。在33名性别和年龄匹配的非脑震荡对照(平均年龄[SD] = 15.2[1.5]; 45.5%为女性)中收集的数据用作健康参考,性别和年龄是所有分析的协变量。相对于睡眠好的人,睡眠差的人表现出广泛的NDI较低(19条中的18条; FDR校正P < 0.048)。只有在脑震荡和神经成像采集之间至少有七天的时间,这种组效应才有意义。脑震荡后症状的严重程度与以下四条神经束的NDI呈负相关:扣带束、视辐射、纹状体-额眶束和上级纵束I。结合性别和NDI的多元线性回归模型能够解释33.2%的症状严重程度变异(F[7,49] = 4.9,P < 0.001,校正R2 = 0.332)。相对于无脑震荡的对照组,睡眠不佳者在扣带回束、视辐射和上级纵束I中表现出较低的NDI(FDR校正P < 0.040)。脑震荡后睡眠质量差与主要白色物质束的普遍较低完整性相关,这反过来有助于解释12-17.9岁青少年脑震荡后症状的严重程度。睡眠对脑震荡后白色物质完整性的影响在一周后是显著的,这表明急性睡眠干预可能需要这段时间才能开始生效。我们的研究结果可能表明脑震荡后几天的良好睡眠质量与主要白色物质束的完整性之间存在重要关系。展望未来,研究人员应该评估睡眠干预对脑震荡后白色物质完整性和临床结果的有效性。
Poor sleepers showed lower NDI in several tracts relative to good sleepers. The effect of sleep quality was significant after seven days between injury and scan. Good sleepers showed no differences relative to non-concussed controls. Significant relationship between low NDI, poor sleep, and higher symptom severity. Being female and low NDI significantly correlate with higher severity of symptoms. Sleep problems are common after concussion; yet, to date, no study has evaluated the relationship between sleep, white matter integrity, and post-concussion symptoms in adolescents. Using self-reported quality of sleep measures within the first 10 days of injury, we aimed to determine if quality of sleep exerts a main effect on white matter integrity in major tracts, as measured by diffusion Magnetic Resonance Imaging (dMRI), and further examine whether this effect can help explain the variance in post-concussion symptom severity in 12- to 17.9-year-old adolescents. dMRI data were collected in 57 concussed adolescents (mean age[SD] = 15.4[1.5] years; 41.2 % female) with no history of major psychiatric diagnoses. Severity of post-concussion symptoms was assessed at study entry (mean days[SD] = 3.7[2.5] days since injury). Using the Pittsburgh Sleep Quality Index (PSQI), concussed adolescents were divided into two groups based on their quality of sleep in the days between injury and scan: good sleepers (PSQI global score ≤ 5; N = 33) and poor sleepers (PSQI global score > 5; N = 24). Neurite Orientation Dispersion and Dispersion Index (NODDI), specifically the Neurite Density Index (NDI), was used to quantify microstructural properties in major tracts, including 18 bilateral and one interhemispheric tract, and identify whether dMRI differences existed in good vs poor sleepers. Since the interval between concussion and neuroimaging acquisition varied among concussed adolescents, this interval was included in the analysis along with an interaction term with sleep groups. Regularized regression was used to identify if quality of sleep-related dMRI measures correlated with post-concussion symptom severity. Due to higher reported concussion symptom severity in females, interaction terms between dMRI and sex were included in the regularized regression model. Data collected in 33 sex- and age-matched non-concussed controls (mean age[SD] = 15.2[1.5]; 45.5 % female) served as healthy reference and sex and age were covariates in all analyses. Relative to good sleepers, poor sleepers demonstrated widespread lower NDI (18 of the 19 tracts; FDR corrected P < 0.048). This group effect was only significant with at least seven days between concussion and neuroimaging acquisition. Post-concussion symptoms severity was negatively correlated with NDI in four of these tracts: cingulum bundle, optic radiation, striato-fronto-orbital tract, and superior longitudinal fasciculus I. The multiple linear regression model combining sex and NDI of these four tracts was able to explain 33.2 % of the variability in symptom severity (F[7,49] = 4.9, P < 0.001, Adjusted R2 = 0.332). Relative to non-concussed controls, poor sleepers demonstrated lower NDI in the cingulum bundle, optic radiation, and superior longitudinal fasciculus I (FDR corrected P < 0.040). Poor quality of sleep following concussion is associated with widespread lower integrity of major white matter tracts, that in turn helped to explain post-concussion symptom severity in 12–17.9-year-old adolescents. The effect of sleep on white matter integrity following concussion was significant after one week, suggesting that acute sleep interventions may need this time to begin to take effect. Our findings may suggest an important relationship between good quality of sleep in the days following concussion and integrity of major white matter tracts. Moving forward, researchers should evaluate the effectiveness of sleep interventions on white matter integrity and clinical outcomes following concussion.
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期刊: RADIOLOGY
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