A retrospective study was performed on 2,767 patients who underwent intracranial lesion resection in the Department of Neurosurgery, Tangdu Hospital of the Air Force Medical University (Xi'an, China), from January 2011 to December 2021. Venous vessels were definitely injured intraoperatively in 93 patients, and it was assumed that venous-related edema, infarction and hemorrhage occurred postoperatively. We collected patient data from electronic medical records and radiology systems. The criteria for exclusion were as follows: (1) emergency surgery for brain trauma, cerebral hemorrhage and cerebral infarction; (2) surgery related to vascular diseases, such as aneurysm, arteriovenous malformation, etc.; and (3) venous edema, infarction and hemorrhage caused by injury or stenosis of the intracranial venous sinus. All study procedures were approved by the ethics committee of Tangdu and followed the guidelines of the Helsinki Declaration. As per the terms of this ethical approval, the necessity for individual patient consent was waived.

All patient data were collected from our hospital electronic medical records. Follow-up data (at least 3 months) were obtained via telephone interviews. Clinical data, such as age, sex, and postoperative clinical manifestations (no symptoms, headache, focal neurological deficits, seizure and coma), were retrieved. Tumor size was determined based on the maximum axial diameter on gadolinium-enhanced T1-weighted and FLAIR MRI sequences. Pathological grading was based on the 2016 WHO criteria. Surgical approaches included the midline, frontotemporal, subfrontal, subtemporal, suboccipital, transcortical, sigmoid sinus and far lateral approaches, etc. Whether to undergo reoperation for edema, infarction, and bleeding after venous injury should be evaluated by two senior clinicians according to the patient's symptoms and imaging. The methods of craniotomy included hematoma evacuation and/or decompressive craniectomy. Disorder of consciousness was defined as drowsiness, lethargy and coma. The interval was defined as the time when the symptoms related to venous injury appeared postoperatively and was confirmed by head CT examination. We routinely performed cranial MRI and MRV examinations to determine the anatomical position of the veins according to sulcus, gyrus, and lesions preoperatively, and judged the consistency based on the observed veins around the lesion intraoperatively and the veins in preoperative MRV. CVI (postoperative CT) was defined as a new or a larger low-density area around the lesion resection. Hemorrhagic CVI was defined as hemorrhage around the low-density area in the brain parenchyma with a mass effect postoperatively. A new or a larger low-density area was located in the scope of the injured venous drainage. No density change in the area of injured venous drainage was considered asymptomatic CVI. Based on the severity of symptoms after venous injury, imaging findings were divided into four stages referring to the previous stages of venous sinus occlusion (10) (I: no change, II: mild edema III: severe edema/infarction, with/without hemorrhage, IV: massive edema/infarction and hemorrhage; Figure 1). We regarded a GOS score of 4–5 as a good prognosis and a GOS score of 1–3 as a poor prognosis.

The results are presented as counts (percentage). Pearson's chi-square test or Fisher's exact was used to compare differences between the distribution of involved venous vessels in the hemorrhagic and non-hemorrhagic groups. The variables that were associated with hemorrhagic CVI were identified in univariate analysis (p < 0.10) and then entered into multivariate logistic regression. All statistical analyses were performed using SPSS software (version 24, IBM Corp.), and p < 0.05 was considered statistically significant.

The GOS score was closely related to the injured vein (Figure 3; Supplementary Table). Patients after CVI were discharged following conservative or surgical treatment. The patients had been followed up for more than 3 months.

The prognosis was good in 78 cases (84%, 78/93). The responsible vessel included cortical pial system (six cases), collateral vein (five cases), superior petrosal vein (eight cases), cerebellar cortical bridging vein (eight cases), anterior frontal vein (seven cases), postcentral vein (five case), superficial middle cerebral vein (15 cases), middle frontal vein (12 cases) and posterior frontal vein (13 cases). The prognosis was poor in 15 cases (16%, 15/93). The responsible vessel included middle frontal vein (two cases), posterior frontal vein (three cases), Labbé (three cases), central vein (four cases) and internal/great cerebral vein (three cases). The clinical outcome was death (two cases, coma-associated pneumonia), vegetative survival (four cases) and severe disability (nine cases).

The hemorrhagic cases with more injured veins and obvious symptoms were middle frontal vein (14 cases) and posterior frontal vein (15 cases). These were poor prognosis rates of 14% (2/14) and 20% (3/15), respectively. Once Labbé, central vein and internal/great cerebral vein were injured, it would inevitably cause CVI or hemorrhagic CVI, leading to irreversible severe neurological dysfunction and even death.

The article clarified the incidence of hemorrhagic cerebral venous infarction (CVI) after venous injury postoperatively during surgery, and confirmed risk factors for hemorrhagic venous cerebral infarction. The incidence of hemorrhagic CVI was 38% (35/93), with poor outcomes in ~16% (15/93) of cases, similar to that with venous thrombosis hemorrhage (6–8, 23). Our research group reviewed the cases of meningioma resection in our hospital, combined them with the relevant literature to identify the risk factors for CVI (21), and further analyzed the risk factors for a large sample of patients with hemorrhagic CVI after intracranial lesion resection. There was a significant difference between hemorrhagic CVI and non-hemorrhagic CVI, and the difference was in the clinical symptoms and prognosis after surgery. The results showed that hemorrhagic CVI was mostly seen in meningiomas, especially superficial meningiomas, in which the postoperative CVI rate was as high as 5.5% (24). Similarly, to increase the surgical field of vision, lesion resection through the midline approach often sacrifices the bridging vein, increasing the probability of hemorrhage. Hemorrhagic symptoms occurred earlier than simple edema/infarction. The interval postoperatively was within 72 h, and the clinical manifestation was sudden seizure and coma, indicating brain function decompensation after acute hemorrhage.

The prognosis of CVI patients was closely related to the responsible veins for injury. We analyzed the prognosis of CVI patients with natural venous injuries during intraoperative lesion resection. The imaging staging after venous injury reflected the severity of the patient's condition to a certain extent. The higher the grading, the more severe the condition, and the higher the proportion of poor prognosis. The results indicated that the injured central vein, vein of Labbé, middle frontal vein and posterior frontal vein were more likely to bleed. Most patients needed emergency craniotomy to remove the hematoma after bleeding, and the bone flap was removed for decompression if necessary (25). Timely intervention has a good prognosis, but injuries to the central vein and vein of Labbé result in irreversible neurological dysfunctions and even death (26). Internal/great cerebral vein injury is mainly caused by infarction, with minor hemorrhages but poor prognosis. The preservation of the SPV vein is a neurosurgical dilemma (16, 27). A literature review and experiences from large series have shown that obliterating the vein of SPV could be associated with negligible complications. However, the opposite view cannot be ignored in light of some series showing a complications rate of up to 30% (28–30). The cortical pial system is usually located among the arachnoid membrane, pia mater and cortex (31). It is inevitable to injure the venous system when removing lesion. Minor venous injury will not cause symptoms, and excessive venous system injury can lead to mild edema, infarction and minor bleeding without causing serious complications. The anterior frontal vein and posterior central veins dominate a small area of drainage, have no important functional areas, and generally do not show clinical symptoms after injury. Because of the rich collateral circulation of the superficial middle cerebral vein, some injuries will not cause obvious symptoms (32). Cerebellar cortical bridging veins are mostly seen in the retrosigmoid and supracerebellar infratentorial approach, but the risk of CVI is an unpredictable (33). When the cerebellum is pulled during the operation, the bridging veins that enter the transverse sinus/sigmoid sinus will be injured. Cerebellar edema is often seen, and cerebellar parenchyma hemorrhage is occasionally seen. The prognosis is good through conservative treatment or removal of the hematoma.