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The Drainage Dysfunction of Meningeal Lymphatic Vessels Is Correlated with the Recurrence of Chronic Subdural Hematoma: a Prospective Study

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Abstract

Meningeal lymphatic vessels (mLVs) were recently discovered to be involved in the waste drainage process in the brain, which has also been associated with a variety of neurological diseases. This research paper hypothesizes that the drainage function of mLVs may be affected after chronic subdural hematoma (CSDH) and the alterations of mLVs’ drainage may predict CSDH recurrence. In this prospective observational study, unenhanced 3D T2-fluid-attenuated inversion recovery (3D T2-FLAIR) MRI data were collected from CSDH patients and healthy participants for analysis. Patients with CSDH who underwent surgery received MRI scans before and after surgery, whereas healthy controls and patients with CSDH who received pharmaceutical treatment received only one MRI scan at enrollment. The signal unit ratio (SUR) of mLVs were then measured according to the MRI data and calculated to define mLVs’ drainage function. Finally, the relationship between mLVs’ drainage function and CSDH recurrence was analyzed accordingly. Thirty-four participants were enrolled in this study, including 27 CSDH patients and 7 controls. The SUR of mLVs in all CSDH patients changed significantly before and after surgery. Moreover, the drainage function of the mLVs ipsilateral to hematoma (mLVs-IH) in CSDH patients was significantly lower than that in the controls (p < 0.05). Last, a higher improvement rate of the drainage function of the mLVs-IH is correlated to a lower risk of recurrence (p < 0.05). This study revealed the mLVs’ drainage dysfunction after CSDH through non-invasive MRI. Furthermore, the drainage function of mLVs is an independent predictive factor of CSDH recurrence.

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Abbreviations

AUC:

Area under the curve

CFS:

Clinical frailty score

CSDH:

Chronic subdural hematoma

dCLV:

Deep cervical lymph vessel

GCS:

Glasgow Coma Scale

ICC:

Interclass correlation coefficient

Lo-mLVs:

Lower mLVs

mLVs:

Meningeal lymphatic vessels

mLVs-CH:

mLVs contralateral to hematoma

mLVs-IH:

mLVs ipsilateral to hematoma

MRI:

Magnetic resonance imaging

MRS:

Modified Rankin scale

ROC:

Receiver operating characteristic

SSS:

Superior sagittal sinus

SUR:

Signal unit ratio

dCLNs:

Deep cervical lymphatic nodes

T2-FLAIR:

T2-fluid-attenuated inversion recovery

TBI:

Traumatic brain injury

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Acknowledgements

We are grateful for the data support from the Second Affiliated Hospital, School of Medicine, Zhejiang University.

Funding

This study was supported by the National Natural Science Foundation of China (82371300, to SC), the National Natural Science Foundation of China (82201430, to YJF), the National Natural Science Foundation of China (82270823, to QW), the Zhejiang Provincial Natural Science Foundation of China (LY23H090014, to SC), and the Medical Health Science and Technology Project of Zhejiang Provincial Health Commission (WKJ-ZJ-2427, to SC).

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Author notes

  1. Jiahao Zhang, Lei Yu, and Xiaoyu Wang contributed equally.

Authors and Affiliations

  1. Department of Neurosurgery, The Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang Province, China

    Jiahao Zhang, Xiaoyu Wang, Qian Yu, Bingrui Zhu, Haocheng Zhang, Yibo Liu, Huaming Li, Anke Zhang, Kaikai Wang, Yezhao He, Qun Wu, Yuanjian Fang & Sheng Chen

  2. Clinical Research Center for Neurological Diseases of Zhejiang Province, Hangzhou, China

    Jiahao Zhang, Xiaoyu Wang, Qian Yu, Bingrui Zhu, Haocheng Zhang, Yibo Liu, Huaming Li, Anke Zhang, Kaikai Wang, Yezhao He, Qun Wu, Yuanjian Fang & Sheng Chen

  3. Department of Radiology, The Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, China

    Lei Yu & Jianzhong Sun

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Contributions

JHZ wrote the manuscript; SC, JZS, and WQ designed the manuscript; JHZ, LY, ZYZ, and XYW collected the study data; YJF, QY, HML, BRZ, and AKZ revised the manuscript; YBL, HCZ, KKW, and YZH participated in the design and coordination of the study. All authors read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Yuanjian Fang, Jianzhong Sun or Sheng Chen.

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Ethical Approval and Consent to Participate

Our study complies with the Declaration of Helsinki that the local ethics committee has approved the research protocol. All patients or their legally authorized representative signed a written informed consent.

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The authors declare no competing interests.

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Supplementary Information

ESM 1

Supplemental Fig. 1 MRI image of patient NO.27 (A1, A2) are the two adjacent MRI images of patient NO.27 before treatment; (A3, A4) are the two adjacent MRI images of patient NO.27 after treatment. Supplemental Fig. 2 Relationship between outcome and suspicious factors. (a-d) Relationship between recurrence and suspicious (n=22); (e-f) Relationship between percentage change of SUR and prognostic scores (n=22). SUR: signal unit ratio. (DOCX 643 kb)

ESM 2

(DOCX 15 kb)

ESM 3

Supplemental Table 1 Basic clinical data of all subjects. (DOCX 25 kb)

ESM 4

Supplemental Table 2 The SUR of all patients. (DOCX 17 kb)

ESM 5

Supplemental Table 3 The SUR of all controls. (DOCX 15 kb)

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Zhang, J., Yu, L., Wang, X. et al. The Drainage Dysfunction of Meningeal Lymphatic Vessels Is Correlated with the Recurrence of Chronic Subdural Hematoma: a Prospective Study. Transl. Stroke Res. 16, 438–447 (2025). https://doi.org/10.1007/s12975-023-01227-4

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