Reekes Tyler H, Upadhya Vinith R, Merenstein Jenna L, Cooter-Wright Mary, Madden David J, Reese Melody A, Boykin Piper C, Timko Noah J, Moul Judd W, Garrigues Grant E, Martucci Katherine T, Cohen Harvey Jay, Whitson Heather E, Mathew Joseph P, Devinney Michael J, Zetterberg Henrik, Blennow Kaj, Shaw Leslie M, Waligorska Teresa, Browndyke Jeffrey N, Berger Miles
Department of Anesthesiology, Duke University Medical Center, Durham, NC.
Trinity College of Arts and Sciences, Duke University, Durham, NC.
medRxiv. 2025 Jan 9:2025.01.08.24319243. doi: 10.1101/2025.01.08.24319243.
Postoperative delirium is the most common postsurgical complication in older adults and is associated with an increased risk of long-term cognitive decline and Alzheimer's disease (AD) and related dementias (ADRD). However, the neurological basis of this increased risk-whether postoperative delirium unmasks latent preoperative pathology or leads to AD-relevant pathology after perioperative brain injury-remains unclear. Recent advancements in neuroimaging techniques now enable the detection of subtle brain features or damage that may underlie clinical symptoms. Among these, Neurite Orientation Dispersion and Density Imaging (NODDI) can help identify microstructural brain damage, even in the absence of visible macro-anatomical abnormalities. To investigate potential brain microstructural abnormalities associated with postoperative delirium and cognitive function, we analyzed pre- and post-operative diffusion MRI data from 111 patients aged ≥60 years who underwent non-cardiac/non-intracranial surgery. Specifically, we investigated preoperative variation in diffusion metrics within the posterior cingulate cortex (PCC), a region in which prior work has identified glucose metabolism alterations in the delirious brain, and a key region in the early accumulation of amyloid beta (Aβ) in preclinical AD. We also examined the relationship of preoperative PCC NODDI abnormalities with preoperative cognitive function. Compared to patients who did not develop postoperative delirium (n=99), we found increased free water (FISO) and neurite density index (NDI) and decreased orientation dispersion index (ODI) in the dorsal PCC before surgery among those who later developed postoperative delirium (n=12). These FISO differences before surgery remained present at six weeks postoperatively, while these NDI and ODI differences did not. Preoperative dorsal PCC NDI and ODI values were also positively associated with preoperative attention/concentration performance, independent of age, education level, and global brain atrophy. Yet, these diffusion metrics were not correlated with cerebrospinal fluid Aβ positivity or levels. These results suggest that preoperative latent brain abnormalities within the dorsal PCC may underlie susceptibility to postoperative delirium, independent of AD-related (i.e., Aβ) neuropathology. Furthermore, these preoperative microstructural differences in the dorsal PCC were linked to preoperative deficits in attention/concentration, a core feature of postoperative delirium. Our findings highlight microstructural vulnerability within the PCC, a key region of the default mode network, as a neuroanatomic locus that can help explain the link between preoperative attention/concentration deficits and increased postoperative delirium risk among vulnerable older surgical patients.
术后谵妄是老年人最常见的术后并发症,与长期认知功能下降、阿尔茨海默病(AD)及相关痴呆症(ADRD)风险增加有关。然而,这种风险增加的神经学基础——术后谵妄是揭示潜在的术前病理状态,还是导致围手术期脑损伤后出现与AD相关的病理改变——仍不清楚。神经成像技术的最新进展现在能够检测出可能是临床症状基础的细微脑特征或损伤。其中,神经突方向离散度和密度成像(NODDI)即使在没有明显宏观解剖异常的情况下,也有助于识别脑微结构损伤。为了研究与术后谵妄和认知功能相关的潜在脑微结构异常,我们分析了111例年龄≥60岁接受非心脏/非颅内手术患者的术前和术后扩散加权磁共振成像(MRI)数据。具体而言,我们研究了后扣带回皮质(PCC)内扩散指标的术前差异,先前的研究已在该区域发现谵妄脑内葡萄糖代谢改变,且该区域是临床前期AD中淀粉样β蛋白(Aβ)早期积聚的关键区域。我们还研究了术前PCC的NODDI异常与术前认知功能的关系。与未发生术后谵妄的患者(n = 99)相比,我们发现后来发生术后谵妄的患者(n = 12)术前背侧PCC的自由水(FISO)和神经突密度指数(NDI)增加,方向离散度指数(ODI)降低。术前这些FISO差异在术后六周仍存在,而NDI和ODI差异则不存在。术前背侧PCC的NDI和ODI值也与术前注意力/集中力表现呈正相关,不受年龄、教育水平和全脑萎缩的影响。然而,这些扩散指标与脑脊液Aβ阳性或水平无关。这些结果表明,背侧PCC内术前潜在的脑异常可能是术后谵妄易感性的基础,与AD相关(即Aβ)神经病理学无关。此外,背侧PCC术前这些微结构差异与术前注意力/集中力缺陷有关,这是术后谵妄的一个核心特征。我们的研究结果突出了默认模式网络关键区域PCC内的微结构易损性,作为一个神经解剖学部位,有助于解释术前注意力/集中力缺陷与脆弱老年手术患者术后谵妄风险增加之间的联系。