Microsurgical resection of a ruptured intraventricular arteriovenous malformation in a neonate: considerations in management. Illustrative case

Lauren Stone Department of Neurosurgery, Division of Pediatric Neurosurgery, Ann and Robert H Lurie Children’s Hospital of Chicago, Northwestern University Feinberg School of Medicine, Chicago, Illinois
Department of Neurosurgery, University of California, La Jolla, California

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Reid Colliander Department of Neurosurgery, Division of Pediatric Neurosurgery, Ann and Robert H Lurie Children’s Hospital of Chicago, Northwestern University Feinberg School of Medicine, Chicago, Illinois
Chicago Medical School, Rosalind Franklin University of Medicine and Science, North Chicago, Illinois

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Melissa A LoPresti Department of Neurosurgery, Division of Pediatric Neurosurgery, Ann and Robert H Lurie Children’s Hospital of Chicago, Northwestern University Feinberg School of Medicine, Chicago, Illinois

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Ali Shaibani Department of Medical Imaging, Division of Neuroradiology, Ann and Robert H Lurie Children’s Hospital of Chicago, Illinois; and

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Sandi Lam Department of Neurosurgery, Division of Pediatric Neurosurgery, Ann and Robert H Lurie Children’s Hospital of Chicago, Northwestern University Feinberg School of Medicine, Chicago, Illinois

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BACKGROUND

Arteriovenous malformations (AVMs) are the most common cause of intracranial hemorrhage in children, although they are rarer in neonates. Age, location, lesion architecture, and rupture status define treatment options. Sparse literature exists to guide the management of clinically symptomatic intraventricular AVM rupture in neonates. We highlight the case of a neonate with a ruptured intraventricular AVM to showcase considerations in treatment, discuss surgical technique, and help guide management.

OBSERVATIONS

An 18-day-old female presented with lethargy in extremis and was found to have new intraventricular hemorrhage. Angiogram revealed a Spetzler-Martin grade 2 AVM with a right posterior choroidal feeder and deep venous drainage within the ventricle. Her age limited radiosurgical and endovascular interventions. She underwent an interhemispheric, transcollosal, intraventricular approach for complete AVM resection. Perioperative care was managed by a multidisciplinary team, successfully mitigating the patient’s high risk of hemovascular collapse.

LESSONS

Stereotactic radiosurgery, endovascular embolization, and microsurgery are options for AVM obliteration, and multimodal therapy must be tailored to the lesion and patient. Conservative management can also be considered. Each intervention carries risks and varying likelihoods of success. Balancing these outcomes is challenging without definitive, high-quality, evidence-based guidance. The best treatment maximizes the chance of AVM obliteration while minimizing morbidity.

ABBREVIATIONS

AVM = arteriovenous malformation; CT = computed tomography; EVD = external ventricular drain; ICU = intensive care unit; POD = postoperative day; SRS = stereotactic radiosurgery

BACKGROUND

Arteriovenous malformations (AVMs) are the most common cause of intracranial hemorrhage in children, although they are rarer in neonates. Age, location, lesion architecture, and rupture status define treatment options. Sparse literature exists to guide the management of clinically symptomatic intraventricular AVM rupture in neonates. We highlight the case of a neonate with a ruptured intraventricular AVM to showcase considerations in treatment, discuss surgical technique, and help guide management.

OBSERVATIONS

An 18-day-old female presented with lethargy in extremis and was found to have new intraventricular hemorrhage. Angiogram revealed a Spetzler-Martin grade 2 AVM with a right posterior choroidal feeder and deep venous drainage within the ventricle. Her age limited radiosurgical and endovascular interventions. She underwent an interhemispheric, transcollosal, intraventricular approach for complete AVM resection. Perioperative care was managed by a multidisciplinary team, successfully mitigating the patient’s high risk of hemovascular collapse.

LESSONS

Stereotactic radiosurgery, endovascular embolization, and microsurgery are options for AVM obliteration, and multimodal therapy must be tailored to the lesion and patient. Conservative management can also be considered. Each intervention carries risks and varying likelihoods of success. Balancing these outcomes is challenging without definitive, high-quality, evidence-based guidance. The best treatment maximizes the chance of AVM obliteration while minimizing morbidity.

ABBREVIATIONS

AVM = arteriovenous malformation; CT = computed tomography; EVD = external ventricular drain; ICU = intensive care unit; POD = postoperative day; SRS = stereotactic radiosurgery

Cerebral arteriovenous malformations (AVMs) are anomalous direct connections between high flow arteries and veins. The resulting tortuous, pressurized blood supply predisposes to rupture, which can lead to lifelong disability or death.1,2 The most common presentation is intracranial hemorrhage, occurring in 52% of all cases and 69% of childhood cases.3,4 Although AVMs are rare in children, they are considered the primary cause of hemorrhagic stroke in the pediatric population and carry a 25% mortality rate.5–7 The annual hemorrhage risk is 3% and the rehemorrhage risk is 4.5% in adults3; however, these rates are significantly higher in the pediatric population, with an annual hemorrhage and rehemorrhage risk of 6.3% and 14.8%, respectively.4 With the increased neuroplasticity and inherently longer life expectancy in children, there may be a stronger indication to intervene in this population even when the AVM is unruptured.8 Interventions for cerebral AVMs include multimodal approaches, including radiosurgery, endovascular embolization, and the traditional gold-standard microsurgical resection.1,9

Choosing an intervention to pursue requires the evaluation of many factors, including AVM location. The role of conservative management should also be considered. Intraventricular lesions are considerably rare, constituting 4% to 19% of cases in the adult population.10–15 Lesions are not infrequently fed by critical choroidal arteries and can be located in difficult to reach areas, such as the atrium. Obtaining the wide view needed for full AVM resection in this area can be challenging, requiring a long corridor, retraction of critical brain parenchyma, and critical access to involved feeding and draining vessels.10,14,16

Herein, we discuss the case of a neonate presenting with a ruptured right intraventricular Spetzler-Martin grade 2 AVM located within the atrium, managed with microsurgical resection. Unique considerations for the evaluation of, approach to, and management of these complex lesions in the youngest of patients are reviewed.

Illustrative Case

An 18-day-old, 4.2-kg female presented to an outside institution with fussiness and lethargy. She was born at 38 weeks 5 days to a 25-year-old woman, gravidity 2, parity 2, via an uncomplicated vaginal delivery and had a normal neonatal course until this point. Computed tomography (CT) and CT angiography revealed a dilated and casted right lateral ventricle adjacent to an irregular tangle of blood vessels in the right atrium, concerning for a ruptured AVM, with compression of the left lateral ventricle, and sulcal and cisternal effacement consistent with elevated intracranial pressure (Fig. 1). The patient was intubated and given 1 g/kg mannitol, and a left frontal external ventricular drain (EVD) was placed prior to transfer to our institution.

FIG. 1
FIG. 1

Initial axial noncontrast CT images (A–C) and axial T2-weighted images (D and E) demonstrating intraventricular hemorrhage with casting of the right lateral ventricle (star) and hydrocephalus. There is an area of parenchymal hemorrhage in the region of the basal ganglia, in the anterior aspect of the right thalamus (arrowhead).

On arrival, her pupils were reactive and the anterior fontanelle was full but soft. Interval imaging demonstrated a persistently dilated and casted right lateral ventricle with trapping of the right temporal horn. Thus, she underwent right-sided parietal EVD placement. After stabilization, diagnostic cerebral angiogram revealed a Spetzler-Martin grade 2 AVM with a right lateral posterior choroidal artery feeder connecting a 5-mm nidus to deep drainage through the right internal cerebral vein (Fig. 2). A three-dimensional reconstruction of the posterior circulation was obtained to further assist with visualization (Fig. 2D).

FIG. 2
FIG. 2

Initial cerebral angiograms, anteroposterior (A), lateral (B), and oblique (C) views, of the posterior circulation, demonstrating an enlarged right posterolateral choroidal artery (arrows) extending to a small nidus (stars), with a single deep draining vein (arrowhead) extending to the right internal cerebral vein. Three-dimensional reconstruction (D) of the same findings. Sagittal (E), coronal (F), and axial (G) reconstructions of the three-dimensional acquisition demonstrating the location of the nidus (stars) along the wall of the right lateral ventricle.

Extensive consideration of treatment options were discussed in our multidisciplinary vascular conference. Consensus opinion was to proceed with resection given the overall lifetime risk of repeat AVM hemorrhage. There is limited knowledge of the application, long-term outcomes, and sequelae of radiosurgery in the literature in a child this young age and with unmyelinated brain. There are technical challenges in endovascular management with an en passage choroidal artery and with weight-based contrast limitations. Extensive discussion was conducted by the treatment team, with family engagement. Surgical intervention was chosen. The timing of surgery after AVM rupture was considered. Ideally, 4 to 6 weeks after AVM rupture allows for the blood clot breakdown to occur at a consistency of soft to liquid components in a hematoma cavity during the resorption process. This process was occurring in the ventricle for this patient, and hydrocephalus was mitigated by external ventricular drainage. For surgical timing in this scenario, we chose to intervene between 4 and 6 weeks after AVM rupture for hematoma resorption to reveal any hidden components of the lesion. The patient underwent an interhemispheric, transcollosal, transventricular craniotomy and approach for AVM excision. Preoperatively, the procedural plan was discussed among anesthesia, neurocritical care, neurointerventional radiology, and neurosurgery, including expected and critical steps of the surgery, an algorithm for managing intraoperative rupture, plan for an immediate postresection diagnostic angiogram to confirm complete AVM resection, and defined postoperative care plan.

A central line and arterial line were placed, and a 10 mg/kg of packed red cells was given at the case outset for a beginning hemoglobin of 8.2 g/dL. Given the patient’s young age and thin skull, her head was immobilized on a horseshoe headholder, and stereotactic navigation was registered via electromagnetic facial registration. A linear incision 1 cm paramedian to the sagittal suture was planned, centered to enter the atrium of the ventricle, using navigation to ensure access to the anterior and posterior aspects of the lesion while minimizing the extent of dissection. The 4-cm craniotomy was performed posterior to the coronal suture, and the dura was opened in a trapdoor fashion, flapped toward the sinus, exposing the interhemispheric fissure with several large cortical veins draining to the superior sagittal sinus, affording several working channels between the draining veins, which were preserved. After an approximately 3-cm callosotomy was made, the body of the right lateral ventricle was entered, and the residual clot evacuated. Intraventricular anatomy including the choroid plexus, thalamostriate vein, and choroidal fissure were identified. A large vessel was noted on the floor of the lateral ventricle that was followed posteriorly to the AVM nidus at the posterior-superior aspect of the thalamus (Fig. 3). The arterial pedicle was identified and cauterized, the nidus was carefully resected, and the draining vein was disconnected. There was no intraoperative rupture. Intraoperative postresection indocyanine green video angiography revealed no anomalous flow.

FIG. 3
FIG. 3

A: View into right lateral ventricle from an interhemispheric exposure. Working channel was selected to avoid a robust superficial cortical vein (octothorpe). Partial corpus callosotomy to expose into right lateral ventricle. Robust intraventricular arterialized early draining vein (asterisk) visualized after removal of intraventricular blood clot (star). Falx cerebri (plus sign). B: Dissection carried forward to expose the anterior nidus and anterior extent of the AVM at the right foramen of Monro (arrowhead). By following this strategy, we ensured exposure of the entire AVM from an interhemispheric approach. Arterialized vein (asterisk), choroid plexus and AVM (double asterisk), and direction to atrium (arrow).

A new EVD was left in the resection cavity and ventricle prior to closure, and the patient was taken to the interventional radiology suite for postoperative cerebral angiography to ensure complete resection. Angiogram revealed complete obliteration of the AVM (Fig. 4). The patient was then extubated and taken to the intensive care unit (ICU) for close hemodynamic monitoring. She began tolerating by mouth intake on postoperative day (POD) 0, and the ventriculostomy was weaned and removed on POD 5. She was discharged home in stable condition on POD 13, neurologically nonfocal.

FIG. 4
FIG. 4

Postresection angiograms, anteroposterior (A and B) and lateral (C and D) views, of the posterior circulation in the arterial and early venous phases. There is no evidence of any residual AVM or early draining vein.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

We describe the workflow, perioperative course, and considerations in the management of a ruptured Spetzler-Martin grade 2 intraventricular AVM in a neonate. The value of this discussion begins with the recognition that pediatric AVMs are distinct from their adult counterparts. Architecturally, they are more often deep, diffuse, and prone to arterial aneurysm.17,18 Annual rerupture risk has a more significant cumulative likelihood over a lifetime because of the patient’s young age, thus encouraging early, aggressive care.19 This underscored our desire for definitive treatment after allowing for an adequate period for hematoma resorption to reveal any hidden nidus.20 Furthermore, an intraventricular AVM is itself rare in all age groups.10,11,13,21,22 This unique location provides additional considerations in management, including the impact of ventriculomegaly, dilating the ventricles affording a larger working corridor surgically, and the impact of ventricular casting with blood products in neonates, often managed with lavage to minimize the risk of hydrocephalus and shunting in children.23

These factors 1) informed our decision for when and how to treat and 2) illuminated a gap in the literature where review of these complex pediatric lesions is sparse. Thus, we highlight this case to discuss the deliberations in management selection, our intraoperative considerations, and the importance of multidisciplinary care as the key lessons that achieved a successful outcome for this patient.

Lessons

Considerations in Multimodal Management

Given the patient’s age, cumulative risk of rerupture, and favorable location in a noneloquent and accessible area, the providers and parents agreed to treat rather than observe. The goal was to minimize risk while maximizing outcomes neurologically, functionally, and regarding AVM resection and hydrocephalus development over time. We considered stereotactic radiosurgery (SRS), endovascular therapy, and resection as well as the timing of treatment.

SRS

The time-dependent manner of SRS obliteration is a significant factor to consider for ruptured cases when balancing the risk of rerupture. In the unruptured literature, the University of Pittsburgh reported a 70% obliteration rate at an average 48.9 months for pediatric patients older than 2 years of age.24 This same group reviewed a cohort of pediatric ventricular AVMs, with 64% obtaining full angiographic obliteration at 10 years, although with an annual hemorrhage rate of 3.4% until obliteration.25 Our patient had a ruptured AVM and was significantly younger than is usually considered acceptable for targeted radiation of any kind.26 Therefore, SRS was not considered.

Endovascular Treatment

When and to what degree endovascular therapy is indicated for neonatal AVMs is not well established. For patients younger than 18 years old, deep, high-flow, multipedicled, or large nidus lesions are prime targets for embolization.27 However, neonatal angiography is uniquely limited by contrast maximums (2–8 mL/kg) and ionizing radiation dose, which will reduce the number of runs per angiogram and significantly reduce allowed procedural time, respectively.28,29 These limitations are side-stepped by staged embolizations. Doing so sequentially shuts down arterial pedicles but alters flow dynamics within the remaining vascular channels of the live AVM, resulting in an elevated annual bleed risk between stages.27,30 Full endovascular treatment is nonetheless possible, but large studies have reported obliteration rates around 12% to 21%.1,30–32 However, in cases of en passage vessels, where embolysate reflux would be unacceptable, it becomes technically more challenging to achieve complete obliteration via endovascular treatment alone.

Endovascular intervention as an adjunct to resection is also a viable option, although not without risk. The postprocedural complication rate in pediatric patients is reported to be between 7.3% and 26%. This range is somewhat correlated to age and weight, with the highest risk for those younger than 3 months old and/or weighing <5 kg.18 Prior to these milestones, the patient’s vasculature is less matured (thus more vulnerable to direct vessel injury, i.e., hemorrhage) and more prone to high-flow lesions (thus risking uncontrolled embolysate or coil reflux, i.e, ischemia).18

These factors were taken into consideration for our patient, with additional consideration for the delicate P2 branch feeder. The likelihood of clinically apparent embolysate reflux into other, already dilated choroidal branches was deemed more risky than potentially beneficial. Endovascular involvement in this case was therefore diagnostic, not interventional. Nonetheless, the detailed imaging performed was crucial to understand lesional architecture and confirm resection postoperatively.

Operative Considerations

Given the aforementioned considerations, consensus opinion was to proceed with microsurgical resection, the timing of which was considered first. We elected for interval treatment within 4 to 6 weeks of rupture to allow for ample hematoma resorption, revealing any areas of hidden nidus, while using the dilated ventricles and hematoma cavity to assist in planes of dissection surgically. Additionally, we submit that in this neonate with casted ventricles, we considered an added benefit of intraventricular surgery to be the opportunity to complete ventricular lavage and hematoma evacuation, hopefully mitigating the risk of hydrocephalus requiring shunting.

There were several key surgical considerations to weigh. Cranial fixation in this age population is challenging because of a paper-thin calvaria, although it is important for neuronavigation registration and accuracy and stability in the surgery itself.33–35 We circumvented this concern by using a horseshoe headholder, avoiding pinning in this age group, while stabilizing the head and allowing for electromagnetic stereotaxy registration. We also weighed surgical approaches, electing an interhemispheric approach allowing us to “walk up” to the AVM by following the draining vein through a safe transventricular corridor, albeit risking contact with large, immature sinus draining veins and falcine vascularity.36 Neither of these interfered with our approach but were necessary to anticipate prior to incision. Posterior parietal, transcortical approaches were considered, although these would require significant transgression through the neonatal brain close to eloquent, developing white matter tracts.37 Furthermore, anecdotally, the infant brain is softer and more difficult to dynamically retract for the necessary long corridor.38 Our goal was to minimize parenchymal manipulation without compromising direct access to irregular vasculature, thus maximizing control in case of rupture.

Multidisciplinary Coordination

The ultimate success of this case is also a testament to united multidisciplinary care, particularly with neonatology, anesthesiology, interventional radiology, and critical care. To optimize this neonate for successful surgery, all parties were instrumental in collaborating on care. Preoperatively, the child was immediately resuscitated in the neonatal ICU on admission. She remained under their care for several weeks, undergoing endovascular drainage, close hemodynamic monitoring, and optimization medically. Furthermore, in institutions in which hybrid operating rooms are unavailable, close coordination with interventional radiology allows for safe and coordinated transfer for preoperative and postoperative angiography in conjunction with surgery, minimizing anesthesia events, and in consideration of multimodal treatments in AVM management. Additionally, postoperative care in the ICU ensures close hemodynamic monitoring in an environment equipped for augmentation and resuscitation, should it be needed, and close neurological monitoring and ventriculostomy management. Penultimately, the complexity of surgery in a neonate raises many considerations; thus, close coordination and communication with anesthesiology preoperatively and intraoperatively are instrumental for success and safety.

Unique anesthetic considerations exist for both pediatric and adult AVM interventions.39,40 An intraoperative AVM rupture is challenging in the best of circumstances but is significantly more complicated in the neonatal population. Namely, blood loss is poorly tolerated.41,42 This is inherently due to low blood volumes, decreased clotting abilities, and immaturity of the cardiovascular system.43–45 For example, our patient had estimated circulating blood volume of 350 mL with viable but small-caliber vascular access. Early bidirectional communication with our anesthesia team was therefore necessary to prepare for untoward hemovascular collapse. Preoperative planning clarified the concerns of each team prior to the procedure, unifying the operative protocol prior to a possible critical moment, with an emphasis on adequate lines including vascular access for medication administration and arterial lines for monitoring, availability of blood products, and blood pressure goals. In our case, we transfused 1 unit of packed red blood cells prior to incision to supplement the patient’s hemoglobin to be at the upper edge of normal throughout the case to provide a buffer for high blood loss. We also ensured that operative video displays were in line with the anesthesiologist’s line of sight and that patient vital sign displays were in line with the surgeon’s line of sight. This provided visual context in addition to verbal communication between teams as stages of the case elapsed. We also took care intraoperatively to minimize blood loss with the approach and dissection, electing an approach that would minimize brain transgression and allow for circumferential dissection of the nidus, minimizing the risk of blood loss and brain tissue disruption. Although some of these points are not unique to AVM procedures, the aggregated product allowed intraoperative care of the patient to run smoothly.

In summary, ruptured intraventricular AVMs in the pediatric population are rare; thus, the available literature to guide management is also rare. SRS and endovascular embolization can be effective for treating some AVMs but with limited value for neonates. We highlight the case of a neonate with an intraventricular, ruptured AVM treated with an interhemispheric, transcollosal transventricular approach for resection to underscore considerations in the management of this unique lesion in this vulnerable population, weighing risks, benefits, and multidisciplinary care to optimize safety and outcomes.

Author Contributions

Conception and design: Lam, Stone. Acquisition of data: Stone, Shaibani. Analysis and interpretation of data: Lam, Stone. Drafting the article: Stone, Colliander, LoPresti. Critically revising the article: Lam, Stone, Colliander, LoPresti. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Lam. Administrative/technical/material support: Lam. Study supervision: Lam.

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    Ogilvy CS, Stieg PE, Awad I, et al. Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Circulation. 2001;103(21):26442657.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Newfield P, Hamid RK. Pediatric neuroanesthesia. Arteriovenous malformations. Anesthesiol Clin North America. 2001;19(2):229235.

  • 41

    Kim DH. Transfusion practice in neonates. Korean J Pediatr. 2018;61(9):265270.

  • 42

    Bharadwaj A, Khandelwal M, Bhargava SK. Perioperative neonatal and paediatric blood transfusion. Indian J Anaesth. 2014;58(5):652657.

  • 43

    Piastra M, Di Rocco C, Caresta E, et al. Blood loss and short-term outcome of infants undergoing brain tumour removal. J Neurooncol. 2008;90(2):191200.

  • 44

    Palmieri TL. Children are not little adults: blood transfusion in children with burn injury. Burns Trauma. 2017;5:24.

  • 45

    Fikac L. Neonatal blood loss risks. Crit Care Nurs Q. 2019;42(2):202204.

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  • FIG. 1

    Initial axial noncontrast CT images (A–C) and axial T2-weighted images (D and E) demonstrating intraventricular hemorrhage with casting of the right lateral ventricle (star) and hydrocephalus. There is an area of parenchymal hemorrhage in the region of the basal ganglia, in the anterior aspect of the right thalamus (arrowhead).

  • FIG. 2

    Initial cerebral angiograms, anteroposterior (A), lateral (B), and oblique (C) views, of the posterior circulation, demonstrating an enlarged right posterolateral choroidal artery (arrows) extending to a small nidus (stars), with a single deep draining vein (arrowhead) extending to the right internal cerebral vein. Three-dimensional reconstruction (D) of the same findings. Sagittal (E), coronal (F), and axial (G) reconstructions of the three-dimensional acquisition demonstrating the location of the nidus (stars) along the wall of the right lateral ventricle.

  • FIG. 3

    A: View into right lateral ventricle from an interhemispheric exposure. Working channel was selected to avoid a robust superficial cortical vein (octothorpe). Partial corpus callosotomy to expose into right lateral ventricle. Robust intraventricular arterialized early draining vein (asterisk) visualized after removal of intraventricular blood clot (star). Falx cerebri (plus sign). B: Dissection carried forward to expose the anterior nidus and anterior extent of the AVM at the right foramen of Monro (arrowhead). By following this strategy, we ensured exposure of the entire AVM from an interhemispheric approach. Arterialized vein (asterisk), choroid plexus and AVM (double asterisk), and direction to atrium (arrow).

  • FIG. 4

    Postresection angiograms, anteroposterior (A and B) and lateral (C and D) views, of the posterior circulation in the arterial and early venous phases. There is no evidence of any residual AVM or early draining vein.

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    • PubMed
    • Search Google Scholar
    • Export Citation
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    Newfield P, Hamid RK. Pediatric neuroanesthesia. Arteriovenous malformations. Anesthesiol Clin North America. 2001;19(2):229235.

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    Kim DH. Transfusion practice in neonates. Korean J Pediatr. 2018;61(9):265270.

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    Bharadwaj A, Khandelwal M, Bhargava SK. Perioperative neonatal and paediatric blood transfusion. Indian J Anaesth. 2014;58(5):652657.

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    Piastra M, Di Rocco C, Caresta E, et al. Blood loss and short-term outcome of infants undergoing brain tumour removal. J Neurooncol. 2008;90(2):191200.

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    Palmieri TL. Children are not little adults: blood transfusion in children with burn injury. Burns Trauma. 2017;5:24.

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    Fikac L. Neonatal blood loss risks. Crit Care Nurs Q. 2019;42(2):202204.

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