| Article Access Statistics|
| Viewed||3231 |
| Printed||122 |
| Emailed||0 |
| PDF Downloaded||42 |
| Comments ||[Add] |
Click on image for details.
|Year : 2021 | Volume
| Issue : 8 | Page : 313-319
Management of Posthemorrhagic Hydrocephalus
Naren Nayak, Suresh K Sankhla
Department of Neurosurgery, Global Hospital, Parel, Mumbai, Maharashtra, India
|Date of Submission||17-Jun-2021|
|Date of Decision||15-Oct-2021|
|Date of Acceptance||18-Oct-2021|
|Date of Web Publication||11-Dec-2021|
Dr. Suresh K Sankhla
Room No. 112, 1st Floor OPD, Global Hospital, 35, Dr. E. Borges Road, Parel, Mumbai – 400 012, Maharashtra
Source of Support: None, Conflict of Interest: None
Background: Although there are several successful treatment options available today, the optimal management of posthemorrhagic hydrocephalus (PHH) still remains undetermined.
Objective: To evaluate the efficacy and outcomes of contemporary treatment methods and to define current evidence-based management for PHH in premature infants.
Material and Methods: Literature was reviewed to identify and analyze merits and demerits of the currently available temporizing measures and definitive treatment for premature low-birth weight babies with PHH.
Results and Conclusions: Advances in treatment and increased experience have led to redefinition of treatment goals to optimize cognitive neurodevelopment, and quality of life in these premature infants with PHH. Current literature favors early diagnosis and intervention using temporizing measures, and prevention of future complications of PHH with a permanent CSF diversion method such as ventricular shunting or endoscopic third ventriculostomy.
Keywords: Germinal matrix hemorrhage, intraventricular hemorrhage, posthemorrhagic ventricular dilatation, premature, temporizing measures
Key Message: Based on recent literature, the management of PHH is focused mainly on early surgical intervention with the aim to clear intraventricular blood and its breakdown products to reduce cognitive disability, the incidence of multiloculated hydrocephalus, and the need for permanent shunt placement.
|How to cite this article:|
Nayak N, Sankhla SK. Management of Posthemorrhagic Hydrocephalus. Neurol India 2021;69, Suppl S2:313-9
Germinal matrix hemorrhage, intraventricular hemorrhage (IVH), and posthemorrhagic ventricular dilation (PHVD) are complications of prematurity that may result in cognitive delay, behavioral abnormalities, epilepsy, visual impairment, cerebral palsy, and symptomatic hydrocephalus.,, Approximately 25%–30% of premature or low birth weight (LBW) infants suffer from IVH and a higher incidence is associated with lower gestational ages and birth weights. Infants weighing less than 1500 g at birth are at a higher risk of developing IVH, and >40% of infants with birth weight 500–750 g are likely to suffer IVH., It has been estimated that approximately 25%–50% of neonates with IVH continue to develop PHVD, and nearly 40% of them require some form of treatment for hydrocephalus.,,,,
The management for IVH and its sequelae in premature infants has evolved over past several decades. Although several treatment paradigms have been proposed, there has been no clear consensus on the optimal treatment for PHH and the guidelines or evidence-based recommendations are lacking till date.,, Presently available therapeutic measures include diuretics, serial lumbar punctures, ventricular access devices (VAD), external ventricular drainage (EVD), and ventriculosubgaleal shunts (VSGS), as well as the permanent cerebrospinal fluid (CSF) diversion methods such as ventriculoperitoneal (VP) shunts and endoscopic third ventriculostomy (ETV). In this report, we review the literature to evaluate the efficacy and outcomes of various treatment modalities available today and make an attempt to outline the current evidence-based management of prematurity-related PHVD/PHH.
| » Diagnosis|| |
Most cases of IVH in premature infants are diagnosed on cranial ultrasound (USG) which is performed soon after the birth, either as a routine procedure or following clinical/systemic instability. There are established criteria to estimate severity and protocols for serial USG in preterm LBW babies with IVH/PHVD, [Table 1]. The highest risk for bleeding is within the first 48 h after birth and most IVH is diagnosed by day 7., Therefore, a close surveillance in the first week after birth with cranial USG of infants with lower gestational age and LBW is extremely crucial for early diagnosis and successful treatment.
- Clinically Silent: On most occasions, IVH may be clinically silent and is detected only on ultrasound studies. For this reason, many authors recommend routine head USG in any infant born at less than 34 weeks' gestation or has birth weight <1500 g.
- Catastrophic: A rapid neurological deterioration may occur over a period of minutes to hours mimicking large intracranial hemorrhage. The clinical signs suggestive of IVH may include a sudden alteration in vital signs like bradycardia or apnea, and/or neonatal seizures. A bulging fontanelle, separation of the sutures, or a rapidly increasing head circumference may suggest the development of acute hydrocephalus.
- Saltatory: Symptoms may evolve over a period of hours and days with a fluctuating pattern of decreased alertness, sluggish motor activity, hypotonia, abnormal eye movements, and respiratory difficulties. Clinical evaluation for increasing head circumference, fullness of fontanelle, enlarged scalp veins, and splaying of sutures can be used to assess progressive ventricular dilatation. Other more serious clinical signs of raised Intracranial Pressure (ICP) such as apnea, bradycardia, lethargy, and decreased activity warn urgent neurosurgical intervention.
Management of IVH and PHH
Management of IVH and posthemorrhagic ventriculomegaly in premature infants still remains a challenge to clinicians.,, The approach to treatment is guided by multiple ongoing factors mainly responsible for primary brain injury and subsequent neurodevelopmental outcomes. Brain damage initially caused by the germinal matrix (GM) hemorrhage is compounded by the toxic effects of the blood and its degradation products, especially iron and free radicals. Additional injury is inflicted by an inflammatory response generated secondary to the release of proinflammatory cytokines. The development of hydrocephalus and raised ICP further worsens the insult to the developing neonatal brain., The overall management of IVH/PHH should thus include aggressive removal of intraventricular blood and its breakdown products, and appropriate treatment for raised ICP due to PHVD/PHH [Table 2]. Currently, there is no consistently proven role of medical management in patients with PHH. A large multicenter randomized controlled trial on acetazolamide and furosemide failed to show any significant benefit in survival or reduction in the need for shunt surgery when used for posthemorrhagic ventricular dilatation. It is also clear from the literature that an early definitive treatment like VPS is mostly unsuitable in LBW premature infants with PHVD/PHH due to extreme fragility and immunological immaturity, and is frequently associated with high risks of anesthetic and surgical morbidity and increased rates of shunt failure., Current management paradigm favors the use of temporizing measures initially during the neonatal period to tide over the crisis in the acute phase until placement of a permanent ventricular shunt is considered necessary and safe., This regimen has by far been the most logical therapeutic option in the management of IVH/PHVD and provides an opportunity to enhance the neurodevelopmental outcome in infants by reducing the complications during treatment, to prevent further progression of hydrocephalus, and to reduce the rates of shunt dependency and shunt revisions.
Commonly used temporizing measures for PHVD/PHH include lumbar punctures (LP), transfontanelle ventricular puncture (VP), EVD, VAD, and VSGS [Table 2],[Table 3],[Table 4]. The choice of temporizing method, however, remains a matter of debate. Meta-analysis of trials from 1980s and 1990s has demonstrated that lumbar punctures and ventricular taps do not reduce permanent shunt dependence or neurological disability. Lumbar puncture is often difficult to perform in clinically unstable infants and its effectiveness tends to reduce on repeated attempts. Ventricular tapping is associated with infection, seizures, and parenchymal injury in the form of hemorrhages and porencephalic cyst formation. EVD is generally not considered as the first choice of treatment for PHH because of the associated higher risk of infection, frequent catheter obstruction, CSF over-drainage, subdural hygroma, hyponatremia, and issues related to the integrity of scalp including wound dehiscence, skin erosion, and CSF leakage., Infants with EVD also require management in the intensive care until the drain is removed or converted to a permanent shunt. VAD partly avoids these limitations and is a good alternative to an EVD. However, VADs are associated with higher risk of infection due to repeated percutaneous tappings and cause fluctuations in intraventricular pressure between very high and very low. The VSG shunts are believed to provide an alternative method for continuous drainage of CSF in the treatment of PHH-related raised ICP. VSGSs have very low infection rate (6%–8%) and other complications like CSF leakage, meningitis, electrolyte imbalance, shunt malfunction, migration of the catheter, and intraparenchymal hemorrhage are rare.,,,,, Permanent shunt placement is usually required in 60%–85% of cases. The main advantage of VSGS, however, is the shorter hospital stay and the ease with which the patient can be managed by the nursing and medical staff in the outpatient setting ,,,.
|Table 3: Studies showing results in patients with PHH treated by VSGS and NEL|
Click here to view
|Table 4: Comparative results of temporizing measures used in premature infants with IVH/PHH|
Click here to view
[Table 2],[Table 3],[Table 4] summarize comparative results of temporizing measures in IVH/PHVD. In a systematic review and meta-analysis of outcome and complications, Badhiwala and colleagues, demonstrated no significant difference in outcome among VAD, EVD, and VSGS. When factors like risks of infection, rates of permanent VPS placement, and subsequent shunt revisions are compared, both VADs and VSGSs are found to be almost equal in effectiveness., Frassanito et al. in a recent publication described a treatment algorithm of combined neuroendoscopic ventricular lavage (NEL) and VSGS in 63 infants with PHH and suggested that the combination is effective and the complication risks including infection and multiloculated hydrocephalus can be reduced significantly.
Timing of intervention is very crucial and several landmark studies in recent years have highlighted the importance of early surgical treatment in premature infants with PHVD.,,, A retrospective comparative study between Dutch and Canadian cohorts found lower rates of cognitive (P = 0.002) and motor (P = 0.03) disability in a cohort whose treatment was initiated when the VI exceeded the 97th centile compared to a cohort whose treatment was initiated in the presence of clinical signs of raised ICP. The early versus late ventricular intervention study (ELVIS) has demonstrated that early intervention (VI exceeding 97th centile or Anterior Horn Width (AHW) >6 mm) is associated with lesser disability than late intervention (VI exceeding 97th centile + 4 mm or AHW 10 mm), and the composite rate of death or disability at 24 months' corrected age was 51% in the late intervention group and 35% in the early intervention group., Regardless of the type of temporizing method used, a close monitoring with regular head circumference measurement, clinical evaluation, and USG assessment is extremely essential to ensure ventricular dilatation is under control.
Intraventricular blood and breakdown products
The toxic effects of blood and its degradation products on the developing brain are well documented.,, It is therefore not uncommon to see infants whose PHVD has been treated adequately with an appropriate intervention are still suffering from serious neurological disability and even infants with less severe IVH (grades I and II) tend to develop severe neurological deficits, disproportionate to their initial hemorrhage.,,,, Thus, there appears a role of early removal of the intraventricular blood and its breakdown products in the management of IVH/PHVD of prematurity. Use of intraventricular fibrinolytic agents has been proposed in the past for the treatment of PHH., However, most of the studies using various intraventricular agents, including recombinant tissue plasminogen activator (rtPA), streptokinase, and urokinase have failed to prove effectiveness in the treatment of IVH.
| » DRIFT Trial|| |
The drainage, irrigation, and fibrinolytic therapy (DRIFT) is so far the best study to provide direct evidence in favor of removal of blood from the ventricles to improve outcome. The aim of the trial was to decrease mortality and cognitive, motor, and sensory disabilities. The procedure involves continuous ventricular irrigation for 72 h to allow clearance of blood and its products from the CSF. The trial was suspended prematurely because of suspected treatment futility and increased risk of secondary bleeding. The short-term outcomes from this randomized controlled trial showed no reduction in shunt surgery or death in the DRIFT intervention arm. In the long-term follow-up, however, the study demonstrated a significant reduction in the proportion of children with severe cognitive disability or death at 2 years in the DRIFT arm, from 71% to 54%, and the mean cognitive quotient score was 69.3 in the DRIFT group and 53.7 in the standard treatment group. This benefit was maintained at 10-year follow-up. The DRIFT is not recommended for the treatment of PHH because of its resource-intensive nature and the risk of secondary hemorrhage, but it sparked a number of research efforts and opportunities to investigate optimal treatment approaches for PHH.
| » Neuroendoscopic Ventricular Lavage|| |
The hypothesis of NEL was based on the 2-year outcome results of DRIFT trial which showed a lower morbidity and reduced cognitive disability in survivors. The technique involves the use of a neuroendoscope to gently irrigate the ventricular cavity, remove the blood clots from both lateral ventricles through a septostomy, ensure patency of the foramina of Monro, and control bleeding sites under direct visualization [Figure 1]. Unlike the technique used in DRIFT, NEL allows for a complete control of inflow, outflow, and intracranial volume balance in a sterile operative setting. Infusion of thrombolytic or other agents which may increase risk of complications is avoided. The procedure is short and associated with reduced risks of infection and fluctuations in CSF pressure.
|Figure 1: Endoscopic view of the right lateral ventricle during neuroendoscopic lavage in a patient who had developed intraventricular hemorrhage and posthemorrhagic hydrocephalus. (a) Heavily blood-stained CSF and unclear view of the intraventricular structures in the beginning of the procedure; (b) Clearer vision and a better view of the ventricular anatomy after continuous fluid irrigation and aspiration of the blood clots; (c) More clear view of the ventricle and the site of a septostomy. Abbreviations: CP - choroid plexus, F - fornix, FM - foramen Monro, S - septostomy, SP - septum pellucidum|
Click here to view
There is no class I evidence of its efficacy but retrospective evaluations have shown encouraging results regarding the procedure safety, reductions in VentriculoPeritoneal Shunt (VPS) insertion and revision rates, and favorable neurodevelopment outcome.,,,, Schulz et al. reported a significant reduction in the rates of shunt placement (from 100% to 58%), infection, shunt occlusion, and multiloculated hydrocephalus in the NEL group. There also appears a trend in their series toward a longer period of shunt-free interval in the NEL group compared with the conventional treatment group. This is important because by the time the shunt insertion is required, the CSF characteristics and the patient's age, weight, and general condition improve in favor of a safe shunt surgery. However, the majority of these studies have potential limitations, including the design of the studies, small patient sample, and no systematic assessment of the neurodevelopmental outcomes, and hence warrant validation in an appropriately structured prospective randomized trial.
Permanent CSF diversion
Once temporizing measure is used, a close monitoring with regular head circumference measurement as well as periodic clinical and USG assessments is followed to ensure control of PHVD. A careful evaluation at or around term-equivalent age or when the bodyweight is 1.8–2.0 kg is essential to determine the ongoing need for the temporizing measures and/or to consider permanent CSF diversion in the form of a VPS/ETV. Additional data can be obtained from CSF sampling (protein levels <1.5 g/L, normal cytology, and negative cultures) and brain imaging with MRI. In recent large series of PHH in premature infants, the VPS placement rates have been reported to vary from 58%–100%.,,,,,
One of many challenges with permanent shunt insertion in premature infants with PHH is infection, which occurs in 13.8% of cases., The high rate of infection in this population is mainly due to an immature immune system and/or an inherent impaired inflammatory response. Also, the thin and fragile skin of LBW infants is vulnerable to frequent wound breaks and ulcerations over the shunt valve and tubing. Thus, delaying the procedure until the infant is grown older is likely to reduce the risk of shunt infection and other complications significantly. Most authors agree that the following must be present for a VP shunt to function in a premature infant with PHH: a mature immune system, an adequate capacity of the peritoneal cavity, the effective elimination of blood products from the CSF, and sufficient thickness of subcutaneous tissue.
Recent literature suggests that shunt failure can occur in up to 12.6% of cases within the first 3 months of VP shunt placement and about 45% of shunts in preterm PHH require shunt revision within 9 months., With regards to shunt infection, results with the currently available silver or antibiotic impregnated catheters are promising and the recent British Antibiotic and Silver Impregnated Catheters for ventriculoperitoneal (Shunts) BASIC study has demonstrated a 3-fold reduction in shunt infection using antibiotic impregnated catheters compared to standard or silver impregnated catheters. There is no clear consensus on the optimal valve type to use in these premature infants. Many authors advocate the use of programmable valves to avoid potential over drainage and complications like subdural hygroma or slit-ventricular syndrome. Peritoneal complications of VP shunts like bowel perforation, necrotizing enterocolitis, pseudocyst formation, and malabsorption of CSF are also common in this population and a ventriculo-atrial shunt can be offered as an alternative, if the diameter of the jugular vein is adequate.
ETV with or without choroid plexus coagulation offers an alternative to a shunt in the treatment of PHH, as it provides an opportunity to avoid shunt dependency.,, However, with a success rate of 37%–40% and limited data available on its efficacy in PHH, ETV can only be advocated in selected patients in whom imaging shows favorable findings like aqueductal stenosis and triventricular hydrocephalus or a patent, nonscarred prepontine cistern.
| » Conclusions|| |
The management of prematurity-related IVH/PHVD and PHH is still evolving and the treatment paradigms are constantly changing from time to time since past few decades. Treatment goals have now shifted from saving life to optimizing cognitive function, neurodevelopment, and quality of life in premature infants. The importance of early intervention with clearing the blood and its breakdown products from the ventricles has been realized by all and the newer techniques have been devised or modified for a safe and effective treatment and improved long-term outcome. In this respect, the preliminary results of newer techniques like VSGSs and NEL are promising. Based on the recent literature, the contemporary management of IVH/PHH recommends early diagnosis and intervention using temporizing measure (VSGS, or NEL) and prevention of future complications of PHH with a permanent CSF diversion method such as ventricular shunting or ETV. Since the cognitive outcomes are now considered more relevant, the future work should be directed toward identifying earlier biomarkers of cognitive neurodevelopmental outcome in order to define safe and more effective treatment protocols.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| » References|| |
Adams-Chapman I, Hansen NI, Stoll BJ, Higgins R. Neurodevelopmental outcome of extremely low birth weight infants with posthemorrhagic hydrocephalus requiring shunt insertion. Pediatrics 2008;121:e1167–77.
Klebermass-Schrehof K, Czaba C, Olischar M, Fuiko R, Waldhoer T, Rona Z, et al
. Impact of low-grade intraventricular hemorrhage on long-term neurodevelopmental outcome in preterm infants. Childs Nerv Syst 2012;28:2085-92.
Roze E, Van Braeckel KN, van der Veere CN, Maathuis CG, Martijn A, Bos AF. Functional outcome at school age of preterm infants with periventricular hemorrhagic infarction. Pediatrics 2009;123:1493–500.
Lemons JA, Bauer CR, Oh W, Korones SB, Papile LA, Stoll BJ, et al
. Very low birth weight outcomes of the National Institute of Child health and human development neonatal research network, January 1995 through December 1996. NICHD Neonatal Research Network. Pediatrics 2001;107:E1. doi: 10.1542/peds. 107.1.e1.
Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, et al
. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: A systematic analysis and implications. Lancet 2012;379:2162–72.
Gale C, Statnikov Y, Jawad S, Uthaya SN, Modi N. Brain Injuries expert working group (2018) Neonatal brain injuries in England: Population-based incidence derived from routinely recorded clinical data held in the National Neonatal Research Database. Arch Dis Child Fetal Neonatal Ed 2018;103:F301–6.
Limbrick DD Jr, Mathur A, Johnston JM, Munro R, Sagar J, Inder T, et al
. Neurosurgical treatment of progressive posthemorrhagic ventricular dilation in preterm infants: A 10-year single-institution study. Clinical article. J Neurosurg Pediatr 2010;6:224–30.
Brouwer AJ, Brouwer MJ, Groenendaal F, Benders MJ, Whitelaw A, de Vries LS. European perspective on the diagnosis and treatment of posthaemorrhagic ventricular dilatation. Arch Dis Child Fetal Neonatal Ed 2012;97:F50–5.
de Vries LS, Liem KD, van Dijk K, Smit BJ, Sie L, Rademaker KJ, et al
. Early versus late treatment of posthaemorrhagic ventricular dilatation: Results of a retrospective study from five neonatal intensive care units in The Netherlands. Acta Paediatr 2002;91:212–7.
Murphy BP, Inder TE, Rooks V, Taylor GA, Anderson NJ, Mogridge N, et al
. Posthaemorrhagic ventricular dilatation in the premature infant: Natural history and predictors of outcome. Arch Dis Child Fetal Neonatal Ed 2002;87:F37–41.
Wellons JC, Shannon CN, Kulkarni AV, Simon TD, Riva-Cambrin J, Whitehead WE, et al
. A multicenter retrospective comparison of conversion from temporary to permanent cere- brospinal fluid diversion in very low birth weight infants with posthemorrhagic hydrocephalus. Clinical article. J Neurosurg Pediatr 2009;4:50–5.
Robinson S. Neonatal posthemorrhagic hydrocephalus from prematurity: Pathophysiology and current treatment concepts. J Neurosurg Pediatr 2012;9:1–23.
Badhiwala JH, Hong CJ, Nassiri F, Hong BY, Riva-Cambrin J, Kulkarni AV. Treatment of posthemorrhagic ventricular dilation in preterm infants: A systematic review and meta-analysis of outcomes and complications. J Neurosurg Pediatr 2015;16:545–55.
Zaben M, Finnigan A, Bhatti MI, Leach P. The initial neuro- surgical interventions for the treatment of posthaemorrhagic hydrocephalus in preterm infants: A focused review. Br J Neurosurg 2016;30:7-10.
Levene MI. Measurement of the growth of the lateral ventricles in preterm infants with real-time ultrasound. Arch Dis Child 1981;56:900–4.
Jary S, Kmita G, Wroblewska J, Whitelaw A. Quantitative cranial ultrasound prediction of severity of disability in premature infants with post-haemorrhagic ventricular dilatation. Arch Dis Child 2012;97:955–9.
Ballabh P, de Vries LS. White matter injury in infants with intraventricular haemorrhage: Mechanisms and therapies. Nat Rev Neurol 2021;17:199–214.
Volpe JJ. Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009;8:110–24.
International randomised controlled trial of acetazolamide and furosemide in posthaemorrhagic ventricular dilatation in infancy. Lancet 1998;352:433-40.
Bock HC, Feldmann J, Ludwig HC. Early surgical management and long-term surgical outcome for intraventricular hemorrhage-related posthemorrhagic hydrocephalus in shunt treated premature infants. J Neurosurg Pediatr 2018;22:61–7.
Mazzola CA, Choudhri AF, Auguste KI, Limbrick DD, Rogido M, Mitchell L, et al
. Pediatric hydrocephalus: Systematic literature review and evidence-based guidelines. Part 2: Management of posthemorrhagic hydrocephalus in premature infants. J Neurosurg Pediatrics (Suppl) 2014;14:8–23.
Riva-Cambrin J, Shannon CN, Holubkov R, Whitehead WE, Kulkarni AV, Drake J, et al
. Center effect and other factors influencing temporization and shunting of cerebrospinal fluid in preterm infants with intraventricular hemorrhage. J Neurosurg Pediatr 2012;9:473–81.
Whitelaw A, Lee-Kelland R. Repeated lumbar or ventricular punctures in newborns with intraventricular haemorrhage. Cochrane Database Syst Rev 2017;4:CD000216.
Shooman D, Portess H, Sparrow O. A review of the current treatment methods for posthaemorrhagic hydrocephalus of infants. Cerebrospinal Fluid Res 2009;6:1–15.
Köksal V, Öktem S. Ventriculosubgaleal shunt procedure and its long-term outcomes in premature infants with posthemorrhagic hydrocephalus. Childs Nerv Syst 2010;26:1505–15.
Li D, Romanski K, Kilgallon M, Speck S, Bowman R, DiPatri A, et al
. Safety of ventricular reservoir sampling in pediatric posthemorrhagic hydrocephalus patients: Institutional experience and review of the literature. J Neurosci Nurs 2021;53:11–7.
Rahman S, Teo C, Morris W, Lao D, Boop FA. Ventriculosubgaleal shunt: A treatment option for progressive posthemorrhagic hydrocephalus. Childs Nerv Syst 1995;11:650–4.
Lam HP, Heilman CB. Ventricular access device versus ventriculosubgaleal shunt in post hemorrhagic hydrocephalus associated with prematurity. J Matern Neonatal Med 2009;22:1097–101.
Tubbs RS, Banks JT, Soleau S, Smyth MD, Wellons JC 3rd
, Blount JP, et al
. Complications of ventriculosubgaleal shunts in infants and children. Childs Nerv Syst 2005;21:48–51.
Frassanito P, Serrao F, Gallini F, Bianchi F, Massimi L, Vento G, et al
. Ventriculosubgaleal shunt and neuroendoscopic lavage: Refining the treatment algorithm of neonatal post hemorrhagic hydrocephalus. Child's Nervous System 2021;37:3531-40.
Fountain DM, Chari A, Allen D, James G. Comparison of the use of ventricular access devices and ventriculosubgaleal shunts in posthaemorrhagic hydrocephalus: Systematic review and metaanalysis. Childs Nerv Syst 2016;32:259–67.
Lai GY, Chu-Kwan W, Westcott AB, Kulkarni AV, Drake JM, Lam SK. Timing of temporizing neurosurgical treatment in relation to shunting and neurodevelopmental outcomes in posthemorrhagic ventricular dilatation of prematurity: A meta-analysis. J Pediatr 2021;234:54-64.e20. doi: 10.1016/j.jpeds. 2021.01.030
Brouwer A, Groenendaal F, van Haastert IL, Rademaker K, Hanlo P, de Vries L. Neurodevelopmental outcome of preterm infants with severe intraventricular hemorrhage and therapy for posthemorrhagic ventricular dilatation. J Pediatr 2008;152:648–54.
Leijser LM, Miller SP, vanWezel-Meijler G, Brouwer AJ, Traubici J, van Haastert IC, et al
. Posthemorrhagic ventricular dilatation in preterm infants: When best to intervene? Neurology 2018;90:e698-706.
de Vries LS, Groenendaal F, Liem KD, Heep A, Brouwer AJ, van't Verlaat E, et al
. Treatment thresholds for intervention in posthaemorrhagic ventricular dilation: A randomised controlled trial. Arch Dis Child Fetal Neonatal Ed 2019;104:F70–5.
Cizmeci MN, Groenendaal F, Liem KD, van Haastert IC, Benavente-Fernández I, van Straaten HL, et al
. Randomized controlled early versus late ventricular intervention study in posthemorrhagic ventricular dilatation: Outcome at 2 years. J Pediatr 2020;226:28–35.e3
Savman K, Blennow M, Hagberg H, Tarkowski E, Thoresen M, Whitelaw A. Cytokine response in cerebrospinal fluid from preterm infants with posthaemorrhagic ventricular dilatation. Acta Paediatr 2002;91:1357–63.
Savman K, Nilsson UA, Blennow M, Kjellmer I, Whitelaw A. Non-protein bound iron is elevated in cerebrospinal fluid from preterm infants with posthemorrhagic ventricular dilatation. Pediatr Res 2001;49:208–12.
Guo J, Chen Q, Tang J, Zhang J, Tao Y, Li L, et al
. Minocycline-induced attenuation of iron overload and brain injury after experimental germinal matrix hemorrhage. Brain Res 2015;1594:115–24.
Patra K, Wilson-Costello D, Taylor HG, Mercuri-Minich N, Hack M. Grades I-II intraventricular hemorrhage in extremely low birth weight infants: Effects on neurodevelopment. J Pediatr 2006;149:169–73.
Whitelay A, Odd D, Brion LP, Kennedy CR. Intraventricular streptokinas after intraventricular hemorrhage in newborn infants. Cochrane Database Syst Rev 2007;4:CD000498. doi: 10.1002/14651858.CD000498.pub2.
Hudgins R, Boydston W, Hudgins PA, Morris R, Adler SM, Gilreath CL. Intrathecal urokinase as a treatment for intraventricular hemorrhage in the preterm infant. Pediatr Neurosurg 1997;26:281-7.
Whitelaw A, Pople I, Cherian S, Evans D. Phase 1 trial of prevention of hydrocephalus after intraventricular hemorrhage in newborn infants by drainage, irrigation, and fibrinolytic therapy. Pediatrics 2003;111:759–66.
Whitelaw A, Jary S, Kmita G, Wroblewska J, Musialik-Swietlinska E, Mandera M, et al
. Randomized trial of drainage, irrigation and fibrinolytic therapy for premature infants with posthemorrhagic ventricular dilatation: developmental outcome at 2 years. Pediatrics 2010;125:e852–8.
Luyt K, Jary S, Lea C, Young GJ, Odd D, Miller H, et al
. Ten-year follow-up of a randomised trial of drainage, irrigation and fibrinolytic therapy (DRIFT) in infants with post-haemorrhagic ventricular dilatation. Health Technol Assess 2019;23:1–116.
Behrens P, Tietze A, Walch E, Bittigau P, Bührer C, Schulz M, et al
. Neurodevelopmental outcome at 2 years after neuroendoscopic lavage in neonates with posthemorrhagic hydrocephalus. J Neurosurg Pediatr 2020;26:1–9.
d'Arcangues C, Schulz M, Bührer C, Thome U, Krause M, Thomale UW. Extended experience with neuroendoscopic lavage for posthemorrhagic hydrocephalus in neonates. World Neurosurg 2018;116:e217-24.
Tirado-Caballero J, Rivero-Garvia M, Arteaga-Romero F, Herreria-Franco J, Lozano-Gonzalez Á, Marquez-Rivas J. Neuroendoscopic lavage for the management of posthemorrhagic hydrocephalus in preterm infants: Safety, effectivity, and lessons learned. J Neurosurg Pediatr 2020;26:1–10.
Etus V, Kahilogullari G, Karabagli H, Unlu A. Early endoscopic ventricular irrigation for the treatment of neonatal posthemorrhagic hydrocephalus: A feasible treatment option or not? A multicenter study. Turk Neurosurg 2018;28:137–41.
Cavalheiro SD, Dastoli PA, Suriano IC, Sparapani F, Mello FB. Brain wash in premature neonate with intraventricular hemorrhage. Childs Nerv Syst 2007;23:1051.
Schulz M, Bührer C, Pohl-Schickinger A, Habert H, Thomale UW. Neuroendoscopic lavage for the treatment of intraventricular hemorrhage and hydrocephalus in neonates. J Neurosurg Pediatr 2014;13:626-35.
Wellons JC, Shannon CN, Holubkov R, Riva-Cambrin J, Kulkarni AV, Limbrick DD, et al
. Shunting outcomes in posthemorrhagic hydrocephalus: Results of a Hydrocephalus Clinical Research Network prospective cohort study. J Neurosurg Pediatr 2017;20:19–29.
Christian EA, Melamed EF, Peck E, Krieger MD, McComb JG. Surgical management of hydrocephalus secondary to intraventricular hemorrhage in the preterm infant. J Neurosurg Pediatr 2016;17:278-84.
Fulkerson DH, Vachhrajani S, Bohnstedt BN, Patel NB, Patel AJ, Fox BD, et al
. Analysis of the risk of shunt failure or infection related to cerebrospinal fluid cell count, protein level, and glucose levels in low-birth-weight premature infants with posthemorrhagic hydrocephalus Clinical article. J Neurosurg Pediatr 2011;7:147–51.
Lin CY, Chang YC, Wang ST, Lee TY, Lin CF, Huang CC. Altered infammatory responses in preterm children with cerebral palsy. Ann Neurol 2010;68:204–12.
Mallucci CL, Jenkinson MD, Conroy EJ, Hartley JC, Brown M, Dalton J, et al
. Antibiotic or silver versus standard ventriculoperitoneal shunts (BASICS): A multicentre, singleblinded, randomised trial and economic evaluation. Lancet 2019;394:1530–9.
Gebert A-F, Schulz M, Schwarz K, Thomale U-W. Longterm survival rates of gravity-assisted, adjustable differential pressure valves in infants with hydrocephalus. J Neurosurg Pediatr 2016;17:544–51.
Warf BC, Campbell JW, Riddle E. Initial experience with combined endoscopic third ventriculostomy and choroid plexus cauterization for post-hemorrhagic hydrocephalus of prematurity: The importance of prepontine cistern status and the predictive value of FIESTAMRI imaging. Childs Nerv Syst 2011;27:1063–71.
Chamiraju P, Bhatia S, Sandberg DI, Ragheb J. Endoscopic third ventriculostomy and choroid plexus cauterization in posthemorrhagic hydrocephalus of prematurity. J Neurosurg Pediatr 2014;13:433–9.
Etus V, Ceylan S. Success of endoscopic third ventriculostomy in children less than 2 years of age. Neurosurg Rev 2005;28:284–8.
Sklar F, Adegbite A, Shapiro K, Miller K. Ventriculosubgaleal shunts: management of posthemorrhagic hydrocephalus in premature infants. Pediatr Neurosurg 1992;18:263-5.
Karas CS, Baig MN, Elton SW. Ventriculosubgaleal shunts at Colombus Children's Hospital: neurosurgical implant placement in the neonatal intensive care unit. J Neurosurg 2007;107:220-3.
Nagy A, Bognar, Pataki I, Barta Z, Novak L. Ventriculosubgaleal shunt in the treatment of posthemorrhagic and postinfectious hydrocephalus of premature infants. Childs Nerv Syst 2013; 29:413-8.
Ellenbogen JR,Waqar M, Pettorini B. Management of posthaemorrhagic hydrocephalus in premature infants. J Clin Neurosci 2016;31:30-34.
[Table 1], [Table 2], [Table 3], [Table 4]