Management of shunt dysfunction using noninvasive intracranial pressure waveform monitoring: illustrative case

Raphael Bertani Department of Neurosurgery, Cerebral Hydrodynamics Group, University of São Paulo, São Paulo, Brazil;

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Caio Perret Department of Neurosurgery, Hospital Municipal Miguel Couto, Rio de Janeiro, Brazil;

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Stefan Koester School of Medicine, Vanderbilt University, Nashville, Tennessee;

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Paulo Santa Maria Department of Neurosurgery, Hospital Municipal Miguel Couto, Rio de Janeiro, Brazil;

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Savio Batista Medical School, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil;

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Sophia de Andrade Cavicchioli Medical School, Universidade de Araraquara, Araraquara, São Paulo, Brazil;

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Sany Tomomi de Almeida Rocha Arita Medical School, Faculdade Santa Marcelina, São Paulo, Brazil; and

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Ruy Monteiro Department of Neurosurgery, Hospital Municipal Miguel Couto, Rio de Janeiro, Brazil;

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Gianne Lucchesi Department of Neurosurgery, Hospital Municipal Miguel Couto, Rio de Janeiro, Brazil;

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Fernando Augusto Vasconcellos Department of Neurosurgery, Hospital Municipal Miguel Couto, Rio de Janeiro, Brazil;

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Matheus Miranda Department of Neurosurgery, Cerebral Hydrodynamics Group, University of São Paulo, São Paulo, Brazil;

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Wellingson Silva Paiva Department of Neurosurgery, University of São Paulo, São Paulo, Brazil

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Fernando Gomes Pinto Department of Neurosurgery, Cerebral Hydrodynamics Group, University of São Paulo, São Paulo, Brazil;

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BACKGROUND

Normal pressure hydrocephalus (NPH) treatment consists of using valves for drainage, as it is for hydrocephalus in general. Despite this, complications can occur, putting the patient at risk, and neurological monitoring is crucial.

OBSERVATIONS

A 61-year-old male, who had been diagnosed with NPH 3 years prior and was being treated with a ventriculoperitoneal shunt with a programmable valve, presented to the emergency department because of a traumatic brain injury due to a fall from standing height. No previous complications were reported. He had an altered intracranial pressure (ICP) waveform in the emergency room when monitored with the brain4care device, with a P2/P1 ratio of 1.6. Imaging helped to confirm shunt dysfunction. Revision surgery normalized the ratio to 1.0, and the patient was discharged. Upon return after 14 days, an outpatient analysis revealed a ratio of 0.6, indicating improvement.

LESSONS

In selected cases of NPH, noninvasive ICP waveform morphology analysis can be effective as a diagnostic aid, as well as in the pre- and postsurgical follow-up, given the possibility of comparing the values of ICP preoperatively and immediately postoperatively and the outpatient P2/P1 ratio, helping to manage these patients.

ABBREVIATIONS

CSF = cerebrospinal fluid; CT = computed tomography; GCS = Glasgow Coma Scale; ICP = intracranial pressure; NPH = normal pressure hydrocephalus; TBI = traumatic brain injury; VPS = ventriculoperitoneal shunt

BACKGROUND

Normal pressure hydrocephalus (NPH) treatment consists of using valves for drainage, as it is for hydrocephalus in general. Despite this, complications can occur, putting the patient at risk, and neurological monitoring is crucial.

OBSERVATIONS

A 61-year-old male, who had been diagnosed with NPH 3 years prior and was being treated with a ventriculoperitoneal shunt with a programmable valve, presented to the emergency department because of a traumatic brain injury due to a fall from standing height. No previous complications were reported. He had an altered intracranial pressure (ICP) waveform in the emergency room when monitored with the brain4care device, with a P2/P1 ratio of 1.6. Imaging helped to confirm shunt dysfunction. Revision surgery normalized the ratio to 1.0, and the patient was discharged. Upon return after 14 days, an outpatient analysis revealed a ratio of 0.6, indicating improvement.

LESSONS

In selected cases of NPH, noninvasive ICP waveform morphology analysis can be effective as a diagnostic aid, as well as in the pre- and postsurgical follow-up, given the possibility of comparing the values of ICP preoperatively and immediately postoperatively and the outpatient P2/P1 ratio, helping to manage these patients.

ABBREVIATIONS

CSF = cerebrospinal fluid; CT = computed tomography; GCS = Glasgow Coma Scale; ICP = intracranial pressure; NPH = normal pressure hydrocephalus; TBI = traumatic brain injury; VPS = ventriculoperitoneal shunt

Hakim-Adams syndrome, also known as “intermittent pressure hydrocephalus” or “normal pressure hydrocephalus” (NPH), is the accumulation of cerebrospinal fluid (CSF) in the ventricles and spaces that contain CSF. This disorder usually affects the elderly and is characterized by the clinical triad of dementia, gait instability (gait apraxia), and urinary incontinence. The estimated annual incidence is 1.8 cases per 100,000 people. However, some studies have shown that the prevalence above 80 years of age can reach 6%, with an increase in this rate observed with age.1 Although the pathophysiology is not fully understood, ventricular enlargement is attributable to an imbalance between CSF production and reabsorption in the systemic circulation. The disorder is referred to as NPH because it is expected that no increase in intracranial pressure (ICP) will be found during diagnosis with lumbar puncture, although we know today that pressure can vary intermittently.2–4

The primary treatment for adult hydrocephalus is the shunting of CSF from the ventricles to the peritoneal cavity, right atrium of the heart, gallbladder, and lungs.3,5–7 Ventriculoperitoneal shunt (VPS) placement is the most common procedure performed. It consists of placing a catheter in the cerebral ventricle connected to a pressure valve implanted under the skin on the scalp, which in turn is connected to another catheter inserted and tunneled through the subcutaneous tissue. This must be large enough to reach the peritoneal cavity, in the region of the abdomen, where excess fluid will be diverted and absorbed.

Conventional valves have previously established pressure values, whereas programmable valves are adjustable. It is possible to increase or decrease the drainage pressure in the office without the need for surgical procedures. The higher the pressure, the lower the drainage.8 The brain4care device is a noninvasive means of monitoring ICP and consists of a strain gauge attached to a mechanical device that touches the scalp’s surface between the lateral frontotemporal region and the sagittal suture.9 In this report, we aim to describe the evolution of a case of NPH decompensation with noninvasive ICP monitoring via the brain4care device.

Illustrative Case

A 61-year-old male diagnosed with NPH had had a VPS implanted 3 years prior without associated comorbidities. For 48 hours, the patient experienced gait alteration, urinary incontinence, and behavior changes, culminating in a traumatic brain injury (TBI) due to a fall from his standing height 1 day prior. He was transferred from another hospital, where cranial tomography was reportedly performed and considered “unremarkable” compared with previous scans.

Immediately, noninvasive analysis with the brain4care device was performed, showing a P2/P1 ratio between 1.35 and 1.65 (Fig. 1A), indicating a possible decline in intracranial compliance. Although he was reported as scoring 14 points on the Glasgow Coma Scale (GCS) during his first admission, he now scored 11 (E2V4M5) points. Given the progressive worsening of symptoms and waveform analysis results, new computed tomography (CT) scans (brain and abdomen) were ordered. Shunt valve pressure adjustment was also performed, from 5 to 2 cm H2O. It had previously been adjusted from 7 to 5 cm H2O.

FIG. 1
FIG. 1

Noninvasive analysis of the ICP waveform showing the waveform, P1/P2 ratio, analyzed heartbeats (pulses) per minute (min.), total heartbeats, and time to peak (TTP), with the latency (or lag) of mechanical propagation of CSF throughout the central nervous system.13 A: Before shunting, with a P2/P1 ratio of 1.35–1.65 and a TTP of 0.25–0.26. B: After shunting, in the same day, with a P2/P1 ratio of 1.11–1.23 and a TTP of 0.27. C: Two weeks after shunting, in the outpatient clinic, the P2/P1 ratio was 0.69–0.81, and TTP was 0.13–0.14.

While scanning was performed, the patient presented with repeated vomiting. Brain CT showed ventriculomegaly and significant transudation with cerebral edema. The finding of abdominal CT was inconclusive. Shunt revision was performed intraoperatively, and a distal catheter obstruction was diagnosed.

At 48 hours postoperatively, the patient was alert and cooperative, had a GCS score of 15, had isochoric and photoreactive pupils, and was mobilizing all four limbs without complaints. Despite complaining of mild diplopia, he showed improvement. Noninvasive ICP monitoring showed a P2/P1 ratio ranging from 1.11 to 1.23 (Fig. 1B), suggesting a more preserved intracranial compliance. The patient was discharged from the hospital and was reassessed 14 days after discharge, remaining asymptomatic, and had an outpatient analysis of ICP pulse morphology showing a P2/P1 ratio ranging from 0.69 to 0.81 (Fig. 1C).

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

The initial brain CT (Fig. 2) was deemed unremarkable and was the only examination performed in the first consultation. The patient had progressively worsening neurological symptoms, possibly leading to a fall and TBI. We used the brain4care sensor to monitor the ICP waveform and thus provide an estimate of brain compliance through the altered P2/P1 ratio (P2 > P1), corroborating the suspicion of distal obstruction, which was later confirmed.10,11

FIG. 2
FIG. 2

Brain CT scan showing ventricular dilation (green arrows) as well as CSF transudation (blue arrow) and the proximal catheter placed in the right lateral ventricle (red arrow).

VPS placement is a treatment option for NPH. Isaacs and Hamilton3 showed that, in general, there is significant improvement with such treatment. Still, high failure rates are caused by issues throughout the shunt system and often lead to surgical revision. This situation shows how auxiliary monitoring methods may help to treat this pathology, preferably via noninvasive techniques, avoiding additional risks.12,13

The brain4care device (Figs. 3 and 4) possesses an extensometer sensor that can detect slight changes in cranial dimensions resulting from changes in ICP without requiring invasive procedures. The order of magnitude of the displacements of the skull is nanometric, and the sensor contains electronic tools and software capable of capturing and processing these signals to reveal the ICP waveform morphology. This noninvasive method of monitoring the ICP waveform allows an estimation of brain compliance and visualization of waveform morphology in patients who initially would not have an indication for an invasive ICP catheter but would benefit from such information. Although the method does not provide direct absolute ICP values, a complete ICP waveform with all its characteristic peaks can be obtained while also allowing continuous monitoring.14–19 Clinical trials performed in intensive care units have shown strong agreement between the ICP waveform from invasive ICP catheters and the brain4care device, as well as the device’s ability to detect intracranial hypertension.16,19

FIG. 3
FIG. 3

A: An external battery unit (left) is used to recharge and extend battery life for prolonged use. A sensor unit (right) without the headband attached. B: Outer surface of the external battery unit and sensor, connected. C: Inner soft surface of the sensor that makes contact with the patient’s head. D: Sensor unit with the headband attached.

FIG. 4
FIG. 4

Illustration of the sensor placed on the right frontoparietal area. The headband (red arrows) and the sensor attached to the external battery unit (green arrows) can also be seen. In this illustration, the patient has a right VPS as well.

Lessons

Although treatment for NPH brings significant recovery from disability, complications can expose patients to significant risks, making it essential to prove assertive monitoring early. We believe that in selected cases of NPH, the analysis of ICP pulse morphology can be effective as a diagnostic aid, especially in shunt malfunction cases, as well as in the pre- and postsurgical follow-up, because of the possibility of comparing waveform morphology and associated parameters (P2/P1 ratio and time to peak) in the preoperative, postoperative, and outpatient settings, potentially helping in the follow-up and decision making in an agile and effective way. Greater dissemination of minimally invasive technologies and larger studies such as randomized clinical trials may clarify the applicability of these methods for better management of these patients.

Author Contributions

Conception and design: Bertani, Perret, Cavicchioli, Monteiro, Vasconcellos, Paiva, Pinto. Acquisition of data: Bertani, Santa Maria, Cavicchioli, Arita, Monteiro, Miranda, Paiva. Analysis and interpretation of data: Bertani, Perret, Koester, Cavicchioli, Arita, Miranda, Pinto. Drafting the article: Bertani, Koester, Santa Maria, Batista, Cavicchioli, Arita. Critically revising the article: Bertani, Koester, Santa Maria, Batista, Cavicchioli, Monteiro, Paiva, Pinto. Reviewed submitted version of manuscript: Bertani, Perret, Koester, Batista, Cavicchioli, Monteiro, Vasconcellos. Approved the final version of the manuscript on behalf of all authors: Bertani. Statistical analysis: Batista, Cavicchioli. Administrative/technical/material support: Bertani, Santa Maria, Monteiro, Lucchesi. Study supervision: Bertani, Perret, Monteiro, Paiva, Pinto.

References

  • 1

    Andersson J, Rosell M, Kockum K, Lilja-Lund O, Söderström L, Laurell K Prevalence of idiopathic normal pressure hydrocephalus: A prospective, population-based study. PLoS One. 2019;14(5):e0217705.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Liang K, Chebrolu P Normal-pressure hydrocephalus: a rare cause of reversible dementia. JAAPA. 2022;35(2):3538.

  • 3

    Isaacs AM, Hamilton M Natural history, treatment outcomes and quality of life in idiopathic normal pressure hydrocephalus (iNPH). Neurol India. 2021;69(suppl):S561S568.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Rekate HL A contemporary definition and classification of hydrocephalus. Semin Pediatr Neurol. 2009;16(1):915.

  • 5

    Isaacs AM, Krahn D, Walker AM, Hurdle H, Hamilton MG Transesophageal echocardiography-guided ventriculoatrial shunt insertion. Oper Neurosurg (Hagerstown). 2020;19(1):2531.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Isaacs AM, Williams MA, Hamilton MG Hydrocephalus in the elderly: surgical management of idiopathic normal pressure hydrocephalus. In Berhouma M, Krolak-Salmon P, eds. Brain and Spine Surgery in the Elderly. Springer International Publishing; 2017:469500.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Keough MB, Isaacs AM, Urbaneja G, Dronyk J, Lapointe AP, Hamilton MG Acute low-pressure hydrocephalus: a case series and systematic review of 195 patients. J Neurosurg. 2020;135(1):300308.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Rojas SSO, Ordinola AAM, Veiga VC, Souza JM The use of a noninvasive intracranial pressure monitoring method in the intensive care unit to improve neuroprotection in postoperative cardiac surgery patients after extracorporeal circulation. Rev Bras Ter Intensiva. 2021;33(3):469476.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Gomes I, Shibaki J, Padua B, et al. Comparison of waveforms between noninvasive and invasive monitoring of intracranial pressure. Acta Neurochir Suppl (Wien). 2021;131:135140.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Bollela VR, Frigieri G, Vilar FC, et al. Noninvasive intracranial pressure monitoring for HIV-associated cryptococcal meningitis. Braz J Med Biol Res. 2017;50(9):e6392.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Enrione MA Current concepts in the acute management of severe pediatric head trauma. Clin Pediatr Emerg Med. 2001;2(1):2840.

  • 12

    Mascarenhas S, Vilela GHF, Carlotti C, et al. The new ICP minimally invasive method shows that the Monro-Kellie doctrine is not valid. Acta Neurochir Suppl (Wien). 2012;114:117120.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Nakajima M, Yamada S, Miyajima M, et al. Guidelines for Management of Idiopathic Normal Pressure Hydrocephalus (Third Edition): endorsed by the Japanese Society of Normal Pressure Hydrocephalus. Neurol Med Chir (Tokyo). 2021;61(2):6397.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Andrade R de AP, Oshiro HE, Miyazaki CK, et al. A nanometer resolution wearable wireless medical device for non invasive intracranial pressure monitoring. IEEE Sens J. 2021;21(20):2227022284.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Rubiano AM, Figaji A, Hawryluk GW Intracranial pressure management: moving beyond guidelines. Curr Opin Crit Care. 2022;28(2):101110.

  • 16

    de Moraes FM, Rocha E, Barros FCD, et al. Waveform morphology as a surrogate for ICP monitoring: a comparison between an invasive and a noninvasive method. Neurocrit Care. 2022;37(1):219227.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Brasil S, Solla DJF, Nogueira RC, Teixeira MJ, Malbouisson LMS, Paiva WDS A novel noninvasive technique for intracranial pressure waveform monitoring in critical care. J Pers Med. 2021;11(12):1302.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Hassett CE, Uysal SP, Butler R, Moore NZ, Cardim D, Gomes JA Assessment of cerebral autoregulation using invasive and noninvasive methods of intracranial pressure monitoring. Neurocrit Care. 2023;38(3):591599.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Brasil S, Frigieri G, Taccone FS, et al. Noninvasive intracranial pressure waveforms for estimation of intracranial hypertension and outcome prediction in acute brain-injured patients. J Clin Monit Comput. 2023;37(3):753760.

    • PubMed
    • Search Google Scholar
    • Export Citation
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  • Expand
  • FIG. 1

    Noninvasive analysis of the ICP waveform showing the waveform, P1/P2 ratio, analyzed heartbeats (pulses) per minute (min.), total heartbeats, and time to peak (TTP), with the latency (or lag) of mechanical propagation of CSF throughout the central nervous system.13 A: Before shunting, with a P2/P1 ratio of 1.35–1.65 and a TTP of 0.25–0.26. B: After shunting, in the same day, with a P2/P1 ratio of 1.11–1.23 and a TTP of 0.27. C: Two weeks after shunting, in the outpatient clinic, the P2/P1 ratio was 0.69–0.81, and TTP was 0.13–0.14.

  • FIG. 2

    Brain CT scan showing ventricular dilation (green arrows) as well as CSF transudation (blue arrow) and the proximal catheter placed in the right lateral ventricle (red arrow).

  • FIG. 3

    A: An external battery unit (left) is used to recharge and extend battery life for prolonged use. A sensor unit (right) without the headband attached. B: Outer surface of the external battery unit and sensor, connected. C: Inner soft surface of the sensor that makes contact with the patient’s head. D: Sensor unit with the headband attached.

  • FIG. 4

    Illustration of the sensor placed on the right frontoparietal area. The headband (red arrows) and the sensor attached to the external battery unit (green arrows) can also be seen. In this illustration, the patient has a right VPS as well.

  • 1

    Andersson J, Rosell M, Kockum K, Lilja-Lund O, Söderström L, Laurell K Prevalence of idiopathic normal pressure hydrocephalus: A prospective, population-based study. PLoS One. 2019;14(5):e0217705.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Liang K, Chebrolu P Normal-pressure hydrocephalus: a rare cause of reversible dementia. JAAPA. 2022;35(2):3538.

  • 3

    Isaacs AM, Hamilton M Natural history, treatment outcomes and quality of life in idiopathic normal pressure hydrocephalus (iNPH). Neurol India. 2021;69(suppl):S561S568.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Rekate HL A contemporary definition and classification of hydrocephalus. Semin Pediatr Neurol. 2009;16(1):915.

  • 5

    Isaacs AM, Krahn D, Walker AM, Hurdle H, Hamilton MG Transesophageal echocardiography-guided ventriculoatrial shunt insertion. Oper Neurosurg (Hagerstown). 2020;19(1):2531.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Isaacs AM, Williams MA, Hamilton MG Hydrocephalus in the elderly: surgical management of idiopathic normal pressure hydrocephalus. In Berhouma M, Krolak-Salmon P, eds. Brain and Spine Surgery in the Elderly. Springer International Publishing; 2017:469500.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Keough MB, Isaacs AM, Urbaneja G, Dronyk J, Lapointe AP, Hamilton MG Acute low-pressure hydrocephalus: a case series and systematic review of 195 patients. J Neurosurg. 2020;135(1):300308.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Rojas SSO, Ordinola AAM, Veiga VC, Souza JM The use of a noninvasive intracranial pressure monitoring method in the intensive care unit to improve neuroprotection in postoperative cardiac surgery patients after extracorporeal circulation. Rev Bras Ter Intensiva. 2021;33(3):469476.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Gomes I, Shibaki J, Padua B, et al. Comparison of waveforms between noninvasive and invasive monitoring of intracranial pressure. Acta Neurochir Suppl (Wien). 2021;131:135140.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Bollela VR, Frigieri G, Vilar FC, et al. Noninvasive intracranial pressure monitoring for HIV-associated cryptococcal meningitis. Braz J Med Biol Res. 2017;50(9):e6392.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Enrione MA Current concepts in the acute management of severe pediatric head trauma. Clin Pediatr Emerg Med. 2001;2(1):2840.

  • 12

    Mascarenhas S, Vilela GHF, Carlotti C, et al. The new ICP minimally invasive method shows that the Monro-Kellie doctrine is not valid. Acta Neurochir Suppl (Wien). 2012;114:117120.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Nakajima M, Yamada S, Miyajima M, et al. Guidelines for Management of Idiopathic Normal Pressure Hydrocephalus (Third Edition): endorsed by the Japanese Society of Normal Pressure Hydrocephalus. Neurol Med Chir (Tokyo). 2021;61(2):6397.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Andrade R de AP, Oshiro HE, Miyazaki CK, et al. A nanometer resolution wearable wireless medical device for non invasive intracranial pressure monitoring. IEEE Sens J. 2021;21(20):2227022284.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Rubiano AM, Figaji A, Hawryluk GW Intracranial pressure management: moving beyond guidelines. Curr Opin Crit Care. 2022;28(2):101110.

  • 16

    de Moraes FM, Rocha E, Barros FCD, et al. Waveform morphology as a surrogate for ICP monitoring: a comparison between an invasive and a noninvasive method. Neurocrit Care. 2022;37(1):219227.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Brasil S, Solla DJF, Nogueira RC, Teixeira MJ, Malbouisson LMS, Paiva WDS A novel noninvasive technique for intracranial pressure waveform monitoring in critical care. J Pers Med. 2021;11(12):1302.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Hassett CE, Uysal SP, Butler R, Moore NZ, Cardim D, Gomes JA Assessment of cerebral autoregulation using invasive and noninvasive methods of intracranial pressure monitoring. Neurocrit Care. 2023;38(3):591599.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Brasil S, Frigieri G, Taccone FS, et al. Noninvasive intracranial pressure waveforms for estimation of intracranial hypertension and outcome prediction in acute brain-injured patients. J Clin Monit Comput. 2023;37(3):753760.

    • PubMed
    • Search Google Scholar
    • Export Citation

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