The implication of liquid hemostatic matrices to prevent hemorrhages during stereotactic biopsy of brain tumors

Eduard E. Rostorguev; Natalia S. Kuznetsova; Sergey E. Kavitskiy; Boris V. Matevosyan; Gennadiy A. Reznik; Vladislav E. Khatyushin; Oleg I. Kit

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South Russian

Journal of Cancer..

Vol. 5

No. 3, 2024

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South Russian

Journal of Cancer..

Vol. 5

No. 3, 2024

South Russian Journal of Cancer. 2024. Vol. 5, No. 3. P. 8-15

https://doi.org/10.37748/2686-9039-2024-5-3-1

https://elibrary.ru/cztobq

ORIGINAL ARTICLE

The implication of liquid hemostatic matrices to prevent hemorrhages

during stereotactic biopsy of brain tumors

E. E. Rostorguev , N. S. Kuznetsova, S. E. Kavitskiy, B. V. Matevosyan, G. A. Reznik,

V. E. Khatyushin, O. I. Kit

National Medical Research Centre for Oncology, Rostov-on-Don, Russian Federation

ed.rost@mail.ru

ABSTRACT

Purpose of the study. Development of a method for

preventing hemorrhages during stereotactic

biopsy of a brain tumor using

liquid hemostatic matrices on the example of the drug "Floseal�".

Patients and methods. The target of the biopsy is the most representative area of tumor tissue according to the data of various

modalities of MRI neuroimaging, including contrast-enhanced ones. Out of 133 patients, 60 patients with signs of intraoperative

bleeding along the biopsy needle cannula were included in the study group. Further, patients with signs of intraoperative bleeding

along the cannula of the biopsy needle were divided into 2 subgroups by independent sequential randomization. Control

subgroup (n = 45): cases with signs of intraoperative bleeding of varying severity were operated on, according to the standard

technique, without the use of the liquid hemostatic drug Floseal�. The main subgroup (n =

15): in

case

of intraoperative

signs

of bleeding, the hemostatic fluid drug Floseal� was injected into the area of tumor material removal.

Results. In 6.7 % of patients of the control subgroup, the formation of massive intracerebral hemorrhages was noted in the

postoperative period. In 53.3 % of the observations of the control subgroup according to X-ray computer examinations of the

brain, there were signs of minor hemorrhages at the point of tumor material collection, which did not require repeated surgical

interventions. Postoperative hemorrhages after injection of the Floseal� liquid hemostatic matrix into the biopsy needle in the

study subgroup were not detected according to neuroimaging X-ray CT.

Conclusion. A method of hemostasis has been developed to prevent hemorrhages using liquid hemostatic

matrices. If signs

of bleeding from the biopsy needle appeare, the introduction of a hemostatic matrix in the volume of 2 ml helps to manage

bleeding intraoperatively, as well as to prevent the occurrence of hemorrhage in the early postoperative period.

Keywords: brain tumor, stereotactic biopsy, bleeding prevention, hemorrhagic complications of brain biopsy, hemorrhage,

hemostasis

For citation: Rostorguev E. E., Kuznetsova N. S., Kavitskiy S. E., Matevosyan B. V., Reznik G. A., Khatyushin V. E., Kit O. I. The implication of liquid hemostatic

matrices to prevent hemorrhages during stereotactic biopsy of brain tumors. South Russian Journal of Cancer. 2024; 5(3): 8-15.

https://doi.org/10.37748/2686-9039-2024-5-3-1, https://elibrary.ru/cztobq

For correspondence: Eduard E. Rostorguev � Dr. Sci. (Med.), MD, head of the Department of Neurological Oncology, National Medical Research Centre for

Oncology, Rostov-on-Don, Russian Federation

Address: 63 14 line str., Rostov-on-Don 344037, Russian Federation

E-mail: ed.rost@mail.ru

ORCID: https://orcid.org/0000-0003-2937-0470

SPIN: 8487-9157, AuthorID: 794808

Scopus Author ID: 57196005138

Compliance with ethical standards: this study adhered to the ethical principles outlined in the World Medical Association Declaration of Helsinki, 1964, ed.

2013. The study was approved by the Committee on Biomedical Ethics at the National Medical Research Centre for Oncology (extract from the protocol of the

meeting No. 7 dated 08/08/2022). Informed consents have been obtained from all participants of the study

Funding: this work was not funded

Conflict of interest: Kit O. I. has been the member of the editorial board of the South Russian Journal of Cancer since 2019, however he has no relation to

the decision made upon publishing this article. The article has passed the review procedure accepted in the journal. The authors did not declare any other

conflicts of interest

The article was submitted 01.09.2023; approved after reviewing 20.06.2024; accepted for publication 27.07.2024

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South Russian Journal of Cancer 2024. Vol. 5, No. 3. P. 8-15

Rostorguev E. E. , Kuznetsova N. S., Kavitskiy S. E., Matevosyan B. V., Reznik G. A., Khatyushin V. E., Kit O. I. The implication of liquid hemostatic matrices to prevent

hemorrhages during stereotactic biopsy of brain tumors

INTRODUCTION

Currently, the stereotactic needle biopsy (STB) of

various grades brain tumors is performed in anatomically

inaccessible areas of the brain and when the

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tumor is

localized in

functionally significant

areas

of the brain [1�4].

Given the lack of visual intraoperative control of

the

needle

trajectory, a

serious

complication

after

STB, is hemorrhage in biopsy material withdrawal

as well as along the path of access of the biopsy

needle, despite the intervention being minimally in

vasive [5�9].

The purpose of the study was to

develop a method

for preventing hemorrhages during stereotactic

biopsy of a

brain

tumor using liquid hemostatic matrices

using the example of the drug "Floseal�".

PATIENTS AND METHODS

From 2014 to 2020 133 patients with brain tumors

were operated on using the method of frameless

needle stereotactic biopsy. Informed consent

for surgical intervention was obtained from

all participants of the study. In our observations,

tumor diseases manifested from 5 to 80 years. The

average age of the patients was 56 years. 57 % were

men and 43 % were women. 75.5 % were operated

on with single foci of brain damage, 10.5 % with

two foci. 14

%

of patients had multiple unverified

CNS lesions.

Neoplasms in 28.3 % of cases were localized in

subcortical structures of the brain, in 18.3 % � in

various parts of the corpus callosum with bilateral

distribution, in 53.4 % of cases in periventricular ar

eas under

functionally

significant areas of

the brain.

Neurological symptoms depended on the localization

of the lesion in the brain. Upon admission, the

functional status on the Karnovsky scale of 100�80

points was noted in 71.7 % of patients, 70�50 points

in 21.7 % of patients, and below 40 points was noted

in 6.6

% of cases. All patients underwent a comprehensive

assessment of the hemostasis system in

the preoperative period.

The tissue sampling point was determined by

combining MRT T1 BRAVO with intravenous contrast

enhancement with data from DTI, 2D-TOF, 3D-TOF,

T2, ASL, SWAN modes. If necessary, in the Brainlab

� or Medtronic StealthStation� S7� planning software,

the digital model was combined with DICOM

positron emission tomography (PET CT) data with

11C-methionine. The trajectory of the biopsy needle

insertion was constructed taking into account the

data of tractography, with the localization of the

tumor

in functionally significant areas of the brain

(Fig. 1).

The purpose of the biopsy is the most representative

area of tumor tissue according to various

modalities of MRI neuroimaging, including

contrast enhancement. Surgical intervention was

performed under general anesthesia, according to

the operating regulations of manufacturers of systems

for frameless stereotactic biopsy Brainlab� or

Medtronic StealthStation� S7� using biopsy needles

Biopsy Needle Kit (9733068) or Biopsy Needle Kit

Tip A (41778C).

Control computed tomography was performed

intraoperatively or within 24 hours after surgery.

Fig. 1. Planning the access trajectory

considering functionally significant areas

of the brain

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Out of 133 patients, the study group included 60

patients with signs of intraoperative bleeding through

the cannula of a biopsy needle (45.1

%). Further, by

the method of independent sequential randomization,

patients with signs of intraoperative bleeding

through the cannula of

a biopsy

needle were divided

into 2 subgroups.

Control subgroup (n = 45): cases

with

signs

of

intraoperative bleeding of varying severity were operated

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according to the standard procedure, without

the use of liquid hemostatic matrices.

The main subgroup (n = 15): with intraoperative

signs

of bleeding, the

hemostatic fluid

drug

"Floseal�" was injected into the area of removal of

tumor material.

The subgroups were comparable in terms of sex,

age, localization and histological types of the tumor.

We analyzed the complications that arose in these

subgroups using the method of X-ray computed

tomography performed in the first 24 hours after

surgery. All necessary patient data were recorded

in the Microsoft Excel electronic database, after

�CB D

Fig. 2. Patient T., 67 years old. A, B � MRI neuroimaging data of a tumor lesion, hospitalized on 10/07/2016 with a diagnosis of a tumor of

the temporal, parietal lobe and islet with a spread to the thalamic tubercle. On 10/10/2016, a stereotactic biopsy was performed. Histological

examination: glioblastoma. In

the

immediate

postoperative

period, the

patient

was

conscious. 7

hours

after the

end

of the

surgery, the

patient

had a sudden loss of consciousness to coma I, the appearance of right-sided anisocoria, the rapid development of secondary ischemic stem

damage in the form of inhibition of pupil photoreaction, loss of oculocephalic reflexes. A brain X-ray computed tomography (CT) scan was

performed, extensive hemorrhage (C) in the tumor area with spread to the temporal and parietal lobes of the brain, blood breakthrough into

the ventricular system of the brain, pronounced lateral dislocation syndrome to the left, secondary ischemic brain damage was visualized.

He

was

taken

to the

operating room for vital

signs. D

� postoperative

cerebral

CT

scan: hematoma and tumor removed. Fatal

outcome

dated

by 10/12/2016

�CB D

Fig. 3. A�D. Patient Ch., 58 years old, was hospitalized on 11/08/2016 with suspected lymphoma of the left hemisphere of the cerebellum

with infiltration of the roof of the 4th ventricle. On 11/09/2016, a stereotactic biopsy of the tumor was performed. Histological examination:

non-Hodgkin's lymphoma. Due to the formation of a hematoma in the tumor biopsy area on 11/10/2016, an urgent installation of the Arendt

cerebrospinal fluid drainage system into the anterior horn of the right lateral ventricle was performed, 11/10/2016. � subtotal removal of a

tumor of the left hemisphere of the cerebellum with growth into the cerebellar bridge angle using neurophysiological monitoring, intraoperative

fluorescence microscopy, removal of an intracerebral hematoma in the bed of a removed tumor of the left hemisphere of the cerebellum.

In

the

future, the

postoperative

period proceeded without

complications. Control

X-ray CT

of the

brain

dated 11/11/2016: condition

after

recraniotomy in the suboccipital region. There are areas of reduced density in the surgical area, the postoperative cavity is 3.7 . 3.5 . 3.1 cm.

The median structures are not displaced. The patient was discharged in a satisfactory condition

South Russian Journal of Cancer 2024. Vol. 5, No. 3. P. 8-15

Rostorguev E. E. , Kuznetsova N. S., Kavitskiy S. E., Matevosyan B. V., Reznik G. A., Khatyushin V. E., Kit O. I. The implication of liquid hemostatic matrices to prevent

hemorrhages during stereotactic biopsy of brain tumors

which the data was analyzed in the Statistica 10.0

program. When processing the obtained patient data

in the control and main groups, an assessment was

carried out based on the nonparametric Pearson�s

chi-squared test (.2).

STUDY RESULTS

In a group of 133

observations, neoplasms were

morphologically verified in all cases. In 43.7

%

of

cases, Grade III�IV gliomas of high malignancy

were verified, Grade II

� in 40.5 %, CNS lymphomas

in 11.4 %, metastases of glandular and squamous

cell carcinoma in 4.4 %.

Fig. 4. X-ray CT neuroimaging of postoperative, clinically insignificant

microbleeding in the area of biopsy material withdrawal

�B

Mortality after STB

in a group of 133

patients was

0.75

% (in one patient, in the immediate postoperative

period, the

formation

of a massive

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intracerebral

hematoma was noted, which required urgent surgical

intervention

of a tumor localized in

a functionally

significant area of the brain (Fig. 2)).

We found that in 6.7 % of patients of the control

subgroup, the formation of massive intracerebral

hemorrhages was noted in the postoperative period

(Fig. 3), requiring repeated surgical interventions,

removal of both intracerebral and intracerebral hemorrhages

with forced cytoreduction of the tumor in

a functionally significant area. The mortality rate in

the control subgroup was 2.2 %.

In 53.3 % of the observations in the control subgroup,

according to X-ray computed studies of the

brain

performed

in

the

first

24

hours

after surgery or

intraoperatively, minor hemorrhages were detected

at the point of collection of tumor material, requiring

a delay in the patient's stay in the hospital and

repeated neuroimaging methods (Fig. 4).

The technique of frameless stereotactic needle

biopsy in the main subgroup (n = 15)

was

standard.

If signs of bleeding were noted during the

withdrawal of tumor material

with a biopsy needle,

in the form of the release of blood clots, rare,

frequent drop or jet bleeding, the hemostatic matrix

"Floseal�" was prepared according to the instructions

for use of the drug (Fig. 5). The drug

is approved for use in the territory of the Russian

Federation (RU No. 2019/8305 dated 04/18/2019).

"Floseal�" is widely used in abdominal, vascular, and

neurological

surgical

fields

as

an

applicative

local

hemostatic [10].

A liquid hemostatic matrix was injected into the

cannula of the inner stylet of the biopsy needle until

Fig. 5. A. Intraoperative signs of

bleeding � the release of blood

clots from a biopsy needle. B. After

preparing the liquid hemostatic matrix

"Floseal�" and filling the inner stylet

of the biopsy needle with it, the liquid

hemostatic matrix is subsequently

injected in a volume of 2 ml

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it was completely filled. After the cannula was inserted

into the biopsy needle, a hemostatic matrix was

additionally injected in a volume of about 2

ml. We

have established a satisfactory possibility of injecting

this drug into the postoperative cavity through the

needle hole for stereotactic biopsy. Next, the biopsy

needle was removed, the milling hole was filled with

bone chips, ensuring hermetically sealed closure of

the bone defect followed by suturing of soft tissues.

Intraoperatively, or within a few hours after waking

up, the patient underwent CT neuroimaging of the

brain to assess postoperative changes and exclude

hemorrhagic complications (Fig. 6).

Hemorrhages and postoperative complications

were not observed in patients of the main subgroup

(n = 15) (.2 = 3.99; p = 0.0458).

In the control subgroup (n

= 45),

the percentage of

clinically significant hemorrhages was 6.7

%, which

required repeated interventions, removal of both

intracerebral and intracerebral hemorrhages. The

percentage of clinically insignificant

hemorrhages

in the control subgroup was 53.3 %. The mortality

rate in the control subgroup was 2.2 %.

DISCUSSION

In

an

international

study by Malone

Hani

et

al. [11]

7514 patients after STBs were analyzed. The most

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common complication of STB was surgically significant

intracerebral bleeding, which was diagnosed in

5.8 % of patients. The risk factors for bleeding in this

study were associated with age above 40 years, hydrocephalus

and cerebral edema. Inpatient mortality

according to the study was 2.8

% [11].

In other publications with different series of patients,

the risk factors for bleeding after STB are not

clearly defined or were

associated by the

authors

with varying degrees

of reliability, i. e. with

the localization

of a pathological focus, e. g. in the brain

stem [8, 9], with

arterial

hypertension, with

impaired

liver function, with the malignant nature of a central

nervous system tumor [12, 13].

According to K. K. Kukanov and co-authors, after

performing the control CT neuroimaging, the presence

of hemorrhages was noted in 40 % of the observations

[14]. Of these, clinically insignificant ones

were noted in 25 %, large diffuse hemorrhages with

a clinical

picture in 5

%, intraventricular hemorrhages

with a pronounced clinical picture in 10

% of cases.

Researchers

see

a

reduction

in

the

risk

of intracranial

hemorrhages after the tumor tissue STB procedure

in careful preoperative planning of the biopsy trajectory,

the use of modern stereotactic devices and

biopsy cannulas, as well as the use of preoperative

hemostatic therapy in patients with suspected high

degree of tumor anaplasia [14].

In the article De Quintana-Schmidt C. with

co-authors

(2019) [15] published the results

of

a

thrombin-gelatin

matrix

inmlication

in

three

cases

of intense bleeding during the STB procedure.

Preliminary results of the work have shown that

injection of a thrombin-gelatin matrix is a safe and

effective procedure for the treatment of persistent

surgical bleeding that cannot be performed by

traditional hemostatic methods used in neuro

surgery [12].

The presented studies do not provide a clear idea

of how to improve the safety of performing stereo

tactic

biopsy. The neurosurgeon faces urgent issues:

what

to choose

as

a reliable hemostatic agent, which

method of administration to use, how to calculate

the administered dose of the drug?

Based on the data of our study conducted from

2014

to 2020, a reliable method of hemostasis was

Fig. 6. Example of brain neuroimaging X-ray CT data 40 minutes

after surgery in a patient using "Floseal�". A reduced density

corresponding to the biopsy point is visualized in the left temporal

lobe. No hemorrhage was found in the area of tumor tissue removal

South Russian Journal of Cancer 2024. Vol. 5, No. 3. P. 8-15

Rostorguev E. E. , Kuznetsova N. S., Kavitskiy S. E., Matevosyan B. V., Reznik G. A., Khatyushin V. E., Kit O. I. The implication of liquid hemostatic matrices to prevent

hemorrhages during stereotactic biopsy of brain tumors

found in a sufficient sample of patients using stereo-CONCLUSION

tactic techniques for collecting tumor material. We

have

proposed

a

technique

for the

introduction

of

If signs of bleeding from a biopsy needle appear

a liquid hemostatic matrix as a preventive measure

during a stereotactic biopsy of a brain tumor, it is

for intraoperative bleeding during STB. possible to inject

a liquid hemostatic matrix

in a vol-

In the course of our study, it was noted that there ume of 2 ml into the point of removal of tumor tissue.

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were no complications, clinically significant hemor-The proposed method of preventing hemorrhages

rhages or microbleeds in the subgroup of patients demonstrates the potential solution to the only seriwith

biopsy needle bleeding after the introduction ous type of complications in this minimally invasive

of a

liquid

hemostatic matrix. On

the

contrary, in

the

diagnostic intervention. A liquid hemostatic matrix

subgroup of patients with the standard stereotactic as intraoperative hemostasis method at the point

biopsy procedure, in cases of intraoperative bleeding of biopsy sampling following the stereotactic interon

a biopsy needle, macro and micro hemorrhages

vention helps to prevent the development or even

were observed in 60 % of patients, repeated surgical stop bleeding intraoperatively, it also prevents the

interventions were performed in 6.7 % of cases, and occurrence of hemorrhages and complications in

the mortality rate was 2.2 %. the early postoperative period.

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Information about authors:

Eduard E. Rostorguev

� Dr. Sci. (Med.), MD, head of the Department of Neurological Oncology, National Medical Research Centre for Oncology,

Rostov-on-Don, Russian Federation

ORCID: https://orcid.org/0000-0003-2937-0470, SPIN: 8487-9157, AuthorID: 794808, Scopus Author ID: 57196005138

Natalia S. Kuznetsova � MD, oncologist, Department of Neurooncology, National Medical Research Centre for Oncology, Rostov-on-Don,

Russian Federation

ORCID: https://orcid.org/0000-0002-2337-326X, SPIN: 8553-3081, AuthorID: 920734

Sergey

E. Kavitskiy

� Cand. Sci. (Med.), MD, neurosurgeon, Consultative and Diagnostic Department, National Medical Research Centre for Oncology,

Rostov-on-Don, Russian Federation

ORCID: https://orcid.org/0000-0002-6924-8974, SPIN: 6437-0420, AuthorID: 734582

Boris V. Matevosyan � MD, neurosurgeon, Department of Neurooncology, National Medical Research Centre for Oncology, Rostov-on-Don,

Russian Federation

ORCID: https://orcid.org/0000-0001-7612-8754

Gennadiy A. Reznik � MD, neurosurgeon, Department of Neurooncology, National Medical Research Centre for Oncology, Rostov-on-Don,

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Russian Federation

ORCID: https://orcid.org/0000-0001-8914-3996

Vladislav E. Khatyushin � MD, neurosurgeon, Department of Neurooncology, National Medical Research Centre for Oncology, Rostov-on-Don,

Russian Federation

ORCID: https://orcid.org/0000-0002-1526-5197, SPIN: 5719-9345, AuthorID: 1129641

Oleg I. Kit � Academician at the Russian Academy

of Sciences, Dr. Sci. (Med.), MD, professor, general director, National Medical Research Centre

for Oncology, Rostov-on-Don, Russian Federation

ORCID: https://orcid.org/0000-0003-3061-6108, SPIN: 1728-0329, AuthorID: 343182, ResearcherID: U-2241-2017, Scopus Author ID: 55994103100

Contribution of the authors:

Rostorguev E. E. � idea and research design development, analysis of the obtained data, writing the text of the manuscript;

Kuznetsova N. S. � collecting the clinical materials;

Kavitskiy S. E. � review of publications on the topic of the article;

Matevosyan B. V. � collecting the clinical materials;

Reznik G. A. � collecting the clinical materials;

Khatyushin V. E. � collecting the clinical materials, review of publications on the topic of the article;

Kit O. I. � development of the research design, critical revision with the introduction of valuable intellectual content, final approval of the published

version of the manuscript.

The implication of liquid hemostatic matrices to prevent hemorrhages during stereotactic biopsy of brain tumors Текст научной статьи по специальности «Клиническая медицина»

Аннотация научной статьи по клинической медицине, автор научной работы — Eduard E. Rostorguev, Natalia S. Kuznetsova, Sergey E. Kavitskiy, Boris V. Matevosyan, Gennadiy A. Reznik

Похожие темы научных работ по клинической медицине , автор научной работы — Eduard E. Rostorguev, Natalia S. Kuznetsova, Sergey E. Kavitskiy, Boris V. Matevosyan, Gennadiy A. Reznik

Использование жидких гемостатических матриц для предупреждения кров оизлияний при выполнении стереотаксической биопсии опухолей головного мозга

Текст научной работы на тему «The implication of liquid hemostatic matrices to prevent hemorrhages during stereotactic biopsy of brain tumors»