7-Tesla magnetic resonance imaging for monitoring microstructural changes in the lenticulostriate artery-neural complex in patients with hypertension

Introduction

Hypertension is one of the most significant risk factors for stroke (1-4). Although hemorrhagic stroke accounts for only 6.5% to 19.6% of global stroke cases, it is associated with high in-hospital and long-term mortality rates (5-7). Hemorrhagic stroke is commonly divided into deep and lobar types. The most common site for deep hemorrhagic strokes is the basal ganglia (BG), which receives blood primarily from the lenticulostriate arteries (LSAs) (8-10). The LSA originates from the anterior cerebral artery and the middle cerebral artery (MCA), including the medial and lateral branches, which supply blood to the internal capsule and the thalamus (11-13). Instability or injury of the LSA can result in symptoms, including a notable reduction in motor control on the contralateral side (14). Thus, imaging of the LSA in vivo provides important insight into the mechanisms of microvascular diseases associated with hypertension.

In recent years, research into the LSA and hemorrhagic stroke has broadened its scope to include a more comprehensive analysis of its surrounding structure. According to theory, the blood-brain barrier in the BG region is formed by LSA capillaries and surrounding neural tissues (15). Therefore, the concept of the LSA-neural complex (LNC) has emerged, which encompasses the structural and functional network formed by the vascular network (i.e., LSA), the neural network (i.e., the BG and thalamus), and the nerve tract/fasciculus network (i.e., the internal capsule) (16). This complex network encompasses the LSA and LSA-supplied neural regions and serves as a critical entity for studying hypertension-induced BG injury.

Evaluation of LNC microstructure changes in vivo via conventional low-field magnetic resonance imaging (MRI), such as 1.5-Tesla (T) and 3-T MRI, is limited. A major restriction is that LSAs comprise a set of microvessels that can range from 2 to 12 in number (with an average of 6–8) and from 80 to 1,400 µm in diameter (with an average of 469 µm) based on dissection (16). The use of 7-T MRI has emerged as a promising approach for microstructure imaging due to its ultrahigh spatial resolution (17-19). With the United States Food and Drug Administration (FDA) approval of new 7-T platforms in 2020, many structural and functional studies have used 7-T for visualizing details in the white matter; cortical and hippocampal subfields; subregions of the thalamus, caudate nucleus, pallidum, putamen, thalamus, and substantia nigra; and small structures such as the subthalamic nucleus, perforating arteries, and the perivascular space (20,21).

Given the above, we hypothesized that the microstructures of LNC in patients with prestroke hypertension are changed and can only be detected using 7-T MRI and not conventional low-magnitude MRI. Our study focused on confirming this hypothesis and identifying early MRI markers for hypertension management and prevention of adverse events. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-869/rc).

Methods

Study design

This prospective, cross-sectional study was conducted in Chongqing, China, from February 2023 to January 2024. Its protocol complied with the Declaration of Helsinki (revised in 2013) and was approved by and registered with the Medical Science Research Ethics Committee of Southwest Hospital, Third Military Medical University [Army Medical University, No. (A) KY2023071]. All participants provided written informed consent. A total of 45 patients that were newly diagnosed with hypertension within the 4 weeks prior to the recruitment were included, and 48 healthy sex- and age-matched volunteers served as controls in the study. As outlined in the 2018 European Society of Cardiology (ESC)/European Society of Hypertension (ESH) Guidelines for the Management of Hypertension, hypertension is characterized by a systolic/diastolic blood pressure equal to or exceeding 140/90 mmHg (22).

The inclusion criteria were as follows: (I) a diagnosis of prestroke hypertension, with no evidence of no brain lesions, including subcortical leukoencephalopathy beyond Fazekas stage I, on MRI anatomical images (23); (II) no other underlying diseases that could easily cause secondary bleeding or stroke (hematological diseases, cerebral infarction, vasculitis, moyamoya disease etc.); (III) no history of intracranial artery occlusion; (IV) no autoimmune diseases or amyloidosis; and (V) no contraindications to MRI, such as severe claustrophobia, pacemakers, or metallic implants. Meanwhile, the exclusion criteria included (I) discontinuation of the MRI procedure, (II) poor image quality, (III) intracranial vascular malformations (arteriovenous malformations and aneurysms), and (IV) diagnosis of diabetes. The flowchart of participant inclusion is shown in Figure 1.

Figure 1 Flowchart of participant inclusion in the study. MRI, magnetic resonance imaging.

MRI

All participants underwent a 7-T MRI with a MAGNETOM Terra scanner (Siemens Healthineers, Erlangen, Germany). The scan was performed with a 32-channel head coil (Nova Medical, Wilmington MA, USA), along with a head gradient insert coil (80 mT/m and 200 T/m/s). For each participant, we acquired T1-weighted Magnetization-Prepared 2 Rapid Gradient Echo (T1w-MP2RAGE) sequences and time-of-flight magnetic resonance angiography (TOF-MRA). The T1w-MP2RAGE was acquired to produce structural images and was conducted under the following parameters: voxel-size =0.70×0.70×0.70 mm³, repetition time (TR) =3,000 ms, field of view (FOV) =224×224×179 mm, flip angle (FA) =8°, echo time (TE) =3.23 ms, bandwidth (BW) =320 Hz/Px, inversion time =1,050 ms, generalized auto-calibrating partial parallel acquisition (GRAPPA) acceleration factor =3, and acquisition time (TA) =5 minutes and 54 seconds. The parameters of TOF-MRA were as follows: voxel-size =0.36×0.23×0.23mm³, FOV =180×135×52 mm, FA =20°, BW =151 Hz/Px, TR =15 ms, GRAPPA factor =2, TE =3.57 ms, and TA =8 minutes 20 seconds. The imaging plate was tilted to be located in the axial plane, covering the lower border of the MCA and the upper border of the BG. TOF-MRA images were converted into maximum intensity projection (MIP) format, with a projection thickness of 25 mm.

Image analysis

These images were analyzed using the ITK-SNAP image-processing software (Penn Image Computing and Science Laboratory). To achieve optimal visualization of LSA, we used a coronal MIP with a slab thickness of 25 mm for image reconstruction. The analysis includes the number of branches of the LSA trunk, the total length from the starting point to the end, and the local length of the skeletonized vascular tree (5–15 mm from the MCAs) (24). The stem was defined as an LSA originating directly from the first segment of the anterior cerebral artery (A1) or MCA (M1). We defined branches as vessels arising from the parent LSA stems without any single vessel. The maximum length was measured on the most prominent LSA in the coronal MIP. The tortuosity of LSA was defined as the ratio of its curved distance to its linear distance, with a smaller tortuosity indicating a larger equivalent stress on the distal vessel, thereby increasing the risk of LSA rupture (18). All data on the morphology of LSA were recorded for all individuals. Additionally, the volumes of neural structures, including the caudate, putamen, internal capsule, globus pallidum, and thalamus were quantified using ITK-SNAP on T1-weighted MPRAGE images. The process for quantifying the volumes of LSA and BG is illustrated in Figure 2.

Figure 2 Methodology for measuring the length and tortuosity of the LSA and the quantification workflow for measuring the neural regions. (A) A schematic illustration of the measurement of LSA parameters is presented, along with representative images of the LSA and its tracings with measured values. (B) The workflow for quantification began with the manual segmentation of the original image using ITK-SNAP, which was followed by mesh-surface reconstruction. The reconstructed surface was subsequently used for quantitative measurements. LSA, lenticulostriate artery.

Tracking work was manually performed by two radiologists with 5–7 years of experience. To ensure the accuracy, another senior radiologist with 10 to 15 years of experience in MRI interpretation examined the results in a randomly selected group of 40 participants, and interclass correlation coefficients (ICCs) were used to evaluate the reproducibility. An ICC greater than 0.75 indicated good agreement of the data (25,26).

Statistical analysis

Continuous variables were reported as means with standard deviations (SDs), while categorical variables were expressed as total numbers with percentages. We compared the morphological characteristics of LSA in each hemisphere and the volume of the BG in two groups using a two-tailed independent samples t-test. The same test was also conducted to compare variables within age-matched subgroups. Histograms were used to visualized the comparison of LSA characteristics between younger and older participants in each group. The criterion for statistical significance was set at a P value of less than 0.05. A partial correlation analysis was conducted to investigate the association between LSA morphometry and BG volumetric measurements. All statistical analyses were performed using SPSS 26 (IBM Corp., Armonk, NY, USA).

Results

Participant characteristics

Out of the 93 recruited participants, 7 were excluded due to poor image quality and/or incomplete acquisition. The demographic data of 6 participants were missing, and 18 participants with the presence of lesions or subcortical leukoencephalopathy exceeding Fazekas stage I in the MRI scan were excluded, leaving a total of 62 participants. Participants’ age ranged from 37 to 59 years. The distribution of the sexes was similar between the two groups. Significant differences in blood pressure and heart rate were observed between the two groups. A detailed overview of the participants’ demographics is presented in Table 1.

The differences in the LSA and the volumes of surrounding nerve structures between two groups

The characteristics of the LSA, the volumes of surrounding nerve structures (i.e., putamen, caudate nucleus, globus pallidus), the internal capsules, and thalamus in both hemispheres were analyzed between the two groups, and typical cases are shown in Figure 3. There were significant statistical differences in the length and tortuosity of LSA between the two groups (P<0.05). In the right hemisphere, the number of LSA stems was higher in the healthy group (2.3±0.9 vs. 2.9±1.2; P<0.05). Other features, such as the branch number, the distance between the largest branch and the MCA, and the numbers of branches, showed no significant difference between the two groups (P>0.05). Furthermore, the volumes of the globus pallidus, putamen, thalamus, caudate nucleus, and internal capsule were found to be significantly larger in healthy participants than in patients with hypertension (P<0.05) (Table 2).

Figure 3 Representative cases for both the hypertension and control groups. LSA morphological and perivascular nerve tissue volumetric parameter measurements of the bilateral cerebral hemisphere in (A,C) a healthy individual and (B,D) a patient with hypertension. The red arrows indicate the maximum diameter of the LSA. L, left hemisphere; R, right hemisphere; LSA, lenticulostriate artery.

The correlations between the LSA and surrounding nerve structures in LNC

The correlations between the LSA’ features and the volumes of these neural nuclei were then investigated in the overall sample (n=62) (Table 3). The correlation analysis indicated that in the left hemisphere, the tortuosity of the LSA was positively correlated with the volume of globus pallidus (r=0.460; P<0.001) and internal capsule (r=0.517; P<0.001). In the right hemisphere, the number of LSA stems was positively correlated with the volume of the internal capsule (r=0.340; P=0.007) and globus pallidus (r=0.299; P=0.018), while the tortuosity of the LSA was positively correlated with the volume of the globus pallidus (r=0.431; P<0.001) and internal capsule (r=0.504; P<0.001) (Figure 4). We further conducted a quantitative analysis of the number of LSA branches entering the perivascular nerve tissue in the two groups and found no LSA branches entering the thalamus. The number of LSA branches entering the putamen was higher in healthy individuals than in patients with hypertension (P<0.01), but there was no significant difference in the number of LSA branches entering other nuclei between healthy individuals and patients with hypertension.

Figure 4 The correlations between LSA features and the volumes of the neural regions in the LNC. (A,B) Correlation between the tortuosity of the LSA and volume of the internal capsule and globus pallidus in the left hemisphere. (C,D) Correlation between the stem number of LSA and the volume of the internal capsule and globus pallidus in the right hemisphere. (E,F) Correlation between the tortuosity of LSA and the volume of the internal capsule and globus pallidus in the right hemisphere. L, left hemisphere; R, right hemisphere; LSA, lenticulostriate artery; LNC, lenticulostriate-artery neural complex.

Age-related morphological changes of the LSA and surrounding nerve structures in the LNC of the hypertension and healthy groups

We analyzed middle-aged and older individuals to better characterize the early-warning signals of morphological and ultrastructural changes caused by hypertension. According to the definition of the World Health Organization (WHO), individuals aged ≥45 years are considered middle-aged or older adult (27-29). All participants (older ≥45 years) in both the hypertension (n=27) and healthy groups (n=28) were included. The results revealed that among individuals aged over 45 years, the hypertension group exhibited a decrease in the number of LSA stems for the right hemisphere and a decreased in the volume of the globus pallidus and internal capsule in both hemispheres (Figure 5).

Figure 5 Comparison of the LSA characteristics and neural regions in the LNC between the hypertension and healthy groups in patients aged over 45 years. (A,B) Average number of stems, LSA branches, and total LSA length. (C,D) The average volume of the neural regions in the left and right hemispheres in participants older than 45 years old. **, P value <0.01; ***, P value <0.001. L, left hemisphere; R, right hemisphere; LSA, lenticulostriate artery; LNC, lenticulostriate-artery neural complex.

Discussion

LNC is a key entity in the study of hypertension-induced BG damage. To our knowledge, this is the first study to examine the ultrahigh-resolution microstructure of the LNC in prestroke hypertension by using 7-T MRI. Although it is possible to use 3-T MRI or high-resolution ultrasound to evaluate the morphological features of LSA (30,31), due to the limitations of anatomical structure and the insufficient resolution of conventional equipment, visualizing the coupling between the LSA and the surrounding nerve tissue is challenging (24,32-34). The advent of 7-T MRI has provided a promising avenue for observing not only vessel microstructures but also cranial nerve nuclei (15,33,35). Our research findings indicate that the microstructure of LNC in patients with prestroke hypertension appears changed on 7-T MRI. The MRI monitoring of LNC including the stem number of LSA and the volumes of the peripheral nerve tissue can serve as predictive biomarkers for intracranial changes and potential complications in hypertension as age increases.

One of the primary findings in our study is the presence of ultrahigh resolution microstructure changes of LNC, including morphological changes of the bilateral LSA and the reduction in surrounding nerve tissue. First, we observed that the length and tortuosity of LSA in patients with hypertension were significantly reduced as compared to those of healthy individuals obtained from 7-T TOF-MRA. In our patient group, we also found a significant decrease in the stem number of the right hemisphere. This could be because prolonged exposure to high blood pressure can accelerate arteriosclerosis, leading to reduced vessel elasticity and luminal narrowing. Additionally, increased peripheral vascular resistance caused by hypertension can decrease microvascular blood flow and signal strength (36,37). These pathological alterations may hinder the visualization of microvessels in vascular angiography (38,39).

Additionally, we observed a significant decrease in nuclear volume in the BG and thalamus in patients with hypertension. Previous studies have also documented the occurrence of BG and other subcortical nuclei atrophy in a variety of neurodegenerative diseases (40,41). This might be due to insufficiency in blood supply, oxidative stress, and hypertension-induced inflammatory damage or death of the neuronal cells within the BG (39). Meanwhile, we also found a correlation between LSA and the surrounding neural tissues in both hemispheres. Except for the thalamus, where no obvious LSA branches were observed, the neural tissues all exhibited varying degrees of being penetrated by branches of the LSA. Among them, the putamen showed a significant decrease in LSA branch penetration in patients with hypertension. The results of our study indicate that hypertension has a clear damaging effect on the LNC.

The microstructure changes of LNC in the prestroke state of patients with hypertension differ between the left and right hemispheres, and these differences may be markers for future MRI monitoring. In our study, we found that among individuals with hypertension aged over 45 years, the right hemisphere exhibited a decline in LSA number and a reduction in the volume of the internal capsule and globus pallidus in both hemispheres. It is possible that as age increases and blood pressure increases, hypoxia and abnormal neurotransmission lead to significant nerve nucleus atrophy of the BG region (42). These changes may suggest both the cause and location of future adverse events and thus warrant further attention.

There are several significant limitations that need to be taken into account in the interpretation of our findings. First, the relatively small sample size might have led to an underestimation of actual microstructure damage affecting the LNC. As we did not analyze classification and course of hypertension, it is possible that some of the more important predictive values and thresholds were missed. Second, we did not employ advanced automatic segmentation and reconstruction techniques. Finally, there were statistically significant differences in heart rate between the two groups, with the hypertension group having a higher heart rate than the control group. However, the heart rate levels in the hypertension group were still within normal range and did not reach the pathological state. There is no literature reporting on effects of heart rate on blood vessels and nerve nuclei in nonpathological states, but we cannot completely rule out the influence of the factor on the study. For these reasons, further studies should be conducted to confirm our findings through an enlargement of the sample size and more refined hypertension grouping.

Conclusions

Our study provides the first evidence supporting the presence of ultrahigh resolution microstructure changes of the LNC in patients with hypertension as detected by 7-T MRI. In patients with hypertension, advanced age, along with a decreased number of LSA stems and reduced volumes of internal capsule and globus pallidus, may serve as MRI markers for monitoring the prestroke state in future. This new insight certainly warrants further investigations and extension to the construction of LNC, more specifically, the development of a neurovascular three-dimensional coupling model, in order to facilitate the clinical assessment and prediction of different stages of disease.

Acknowledgments

The authors would like to thank the volunteers who participated in the study.

Funding: This work was supported by Chongqing Science, Technology, and Health Joint Project (No. 2021msxm341) and Chongqing Science and Health Joint Medical Research Project of China (No. 2023MSXM063).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-869/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-869/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by and registered with Southwest Hospital, Third Military Medical University Medical Science Research Ethics Committee [Army Medical University, No. (A) KY2023071]. Informed consent was obtained from all participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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