Pediatric hydrocephalus: systematic literature review and evidence-based guidelines. Part 2: Management of posthemorrhagic hydrocephalus in premature infants

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Object

The objective of this systematic review and analysis was to answer the following question: What are the optimal treatment strategies for posthemorrhagic hydrocephalus (PHH) in premature infants?

Methods

Both the US National Library of Medicine and the Cochrane Database of Systematic Reviews were queried using MeSH headings and key words relevant to PHH. Two hundred thirteen abstracts were reviewed, after which 98 full-text publications that met inclusion criteria that had been determined a priori were selected and reviewed.

Results

Following a review process and an evidentiary analysis, 68 full-text articles were accepted for the evidentiary table and 30 publications were rejected. The evidentiary table was assembled linking recommendations to strength of evidence (Classes I–III).

Conclusions

There are 7 recommendations for the management of PHH in infants. Three recommendations reached Level I strength, which represents the highest degree of clinical certainty. There were two Level II and two Level III recommendations for the management of PHH.

Recommendation Concerning Surgical Temporizing Measures: I. Ventricular access devices (VADs), external ventricular drains (EVDs), ventriculosubgaleal (VSG) shunts, or lumbar punctures (LPs) are treatment options in the management of PHH. Clinical judgment is required. Strength of Recommendation: Level II, moderate degree of clinical certainty.

Recommendation Concerning Surgical Temporizing Measures: II. The evidence demonstrates that VSG shunts reduce the need for daily CSF aspiration compared with VADs. Strength of Recommendation: Level II, moderate degree of clinical certainty.

Recommendation Concerning Routine Use of Serial Lumbar Puncture: The routine use of serial lumbar puncture is not recommended to reduce the need for shunt placement or to avoid the progression of hydrocephalus in premature infants. Strength of Recommendation: Level I, high clinical certainty.

Recommendation Concerning Nonsurgical Temporizing Agents: I. Intraventricular thrombolytic agents including tissue plasminogen activator (tPA), urokinase, or streptokinase are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

Recommendation Concerning Nonsurgical Temporizing Agents. II. Acetazolamide and furosemide are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

Recommendation Concerning Timing of Shunt Placement: There is insufficient evidence to recommend a specific weight or CSF parameter to direct the timing of shunt placement in premature infants with PHH. Clinical judgment is required. Strength of Recommendation: Level III, unclear clinical certainty.

Recommendation Concerning Endoscopic Third Ventriculostomy: There is insufficient evidence to recommend the use of endoscopic third ventriculostomy (ETV) in premature infants with posthemorrhagic hydrocephalus. Strength of Recommendation: Level III, unclear clinical certainty.

Abbreviations used in this paper:AANS = American Association of Neurological Surgeons; CDC = Centers for Disease Control and Prevention; CNS = Congress of Neurological Surgeons; ELBW = extremely low birth weight; ETV = endoscopic third ventriculostomy; EVD = external ventricular drain; HUS = head ultrasound; IVH = intraventricular hemorrhage; LBW = low birth weight; LP = lumbar puncture; OFC = occipitofrontal circumference; PHH = posthemorrhagic hydrocephalus; PHVD = posthemorrhagic ventricular dilation; tPA = tissue plasminogen activator; VAD = ventricular access device; V/BP = ventricular/biparietal; VP = ventriculoperitoneal; VSG = ventriculosubgaleal.

Abstract

Object

The objective of this systematic review and analysis was to answer the following question: What are the optimal treatment strategies for posthemorrhagic hydrocephalus (PHH) in premature infants?

Methods

Both the US National Library of Medicine and the Cochrane Database of Systematic Reviews were queried using MeSH headings and key words relevant to PHH. Two hundred thirteen abstracts were reviewed, after which 98 full-text publications that met inclusion criteria that had been determined a priori were selected and reviewed.

Results

Following a review process and an evidentiary analysis, 68 full-text articles were accepted for the evidentiary table and 30 publications were rejected. The evidentiary table was assembled linking recommendations to strength of evidence (Classes I–III).

Conclusions

There are 7 recommendations for the management of PHH in infants. Three recommendations reached Level I strength, which represents the highest degree of clinical certainty. There were two Level II and two Level III recommendations for the management of PHH.

Recommendation Concerning Surgical Temporizing Measures: I. Ventricular access devices (VADs), external ventricular drains (EVDs), ventriculosubgaleal (VSG) shunts, or lumbar punctures (LPs) are treatment options in the management of PHH. Clinical judgment is required. Strength of Recommendation: Level II, moderate degree of clinical certainty.

Recommendation Concerning Surgical Temporizing Measures: II. The evidence demonstrates that VSG shunts reduce the need for daily CSF aspiration compared with VADs. Strength of Recommendation: Level II, moderate degree of clinical certainty.

Recommendation Concerning Routine Use of Serial Lumbar Puncture: The routine use of serial lumbar puncture is not recommended to reduce the need for shunt placement or to avoid the progression of hydrocephalus in premature infants. Strength of Recommendation: Level I, high clinical certainty.

Recommendation Concerning Nonsurgical Temporizing Agents: I. Intraventricular thrombolytic agents including tissue plasminogen activator (tPA), urokinase, or streptokinase are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

Recommendation Concerning Nonsurgical Temporizing Agents. II. Acetazolamide and furosemide are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

Recommendation Concerning Timing of Shunt Placement: There is insufficient evidence to recommend a specific weight or CSF parameter to direct the timing of shunt placement in premature infants with PHH. Clinical judgment is required. Strength of Recommendation: Level III, unclear clinical certainty.

Recommendation Concerning Endoscopic Third Ventriculostomy: There is insufficient evidence to recommend the use of endoscopic third ventriculostomy (ETV) in premature infants with posthemorrhagic hydrocephalus. Strength of Recommendation: Level III, unclear clinical certainty.

Although reviews have been recently published, there exists a paucity of guidelines or evidencebased recommendations for the management of posthemorrhagic hydrocephalus (PHH) in infants.62 According to 2007 data provided by the Division of Vital Statistics of the Centers for Disease Control and Prevention (CDC), infants born with very low birth weight and gestational age have a significantly higher risk of mortality.49 In fact, more than 50% of all infant deaths in 2007 occurred in infants born before 32 weeks' gestation.49 In 2008, the reported preterm birth rate declined for the second consecutive year to 12.3%, but this decrease primarily involved those infants born in the later preterm period (34–36 weeks).47 Low birth weight (LBW) also contributes to increased infant mortality, and the CDC has reported that the percentage of LBW infants, or infants born weighing less than 2500 g, increased by 24% between 1984 and 2006.47

A recent study of 15,454 extremely low birth weight (ELBW) infants, each weighing between 401 g and 1000 g, was undertaken to assess neurodevelopmental outcome.1 More than 5000 infants died while in the hospital or before the follow-up visit. Among the 7693 children in whom follow-up studies were available, 2530 (33%) had a history of intraventricular hemorrhage (IVH). The IVH was Grade III or IV for 998 (13%) of the 7693 infants. Remarkably, in only 246 (3%) of the 7693 ELBW infants with follow-up was a shunt placed for PHH.1 There are still many questions about the optimal time to intervene for infants with PHH, and there are many different opinions about the best temporizing mechanism for symptomatic infants too small or unstable for permanent shunt placement.

The objective of this systematic review and analysis was to answer the following question: What are the optimal treatment strategies for posthemorrhagic hydrocephalus (PHH) in premature infants? We evaluated the current literature and constructed evidence-based recommendations supported by the strength of the available data for the management of PHH in premature infants. Specifically, we wanted to investigate relevant evidence for the following:

  • Use of surgical temporizing methods such as ventricular reservoirs, external ventricular drains (EVDs), ventriculosubgaleal (VSG) shunts, and lumbar punctures (LPs).

  • Routine use of serial LPs to reduce the need to shunt or to avoid the progression of hydrocephalus in premature infants.

  • Use of intraventricular thrombolytic agents, including tissue plasminogen activator (tPA), urokinase, and streptokinase, to reduce the need for shunt placement in premature infants with PHH.

  • Use of acetazolamide or furosemide to reduce the need for shunt placement in premature infants with PHH.

  • Efficacy of endoscopic third ventriculosomy (ETV) in this population.

  • Specific CSF parameters to direct the timing of shunt placement in premature infants with PHH.

Methods

Search Criteria

Both the US National Library of Medicine and the Cochrane Database of Systematic Reviews were queried using MeSH headings and key words relevant to PHH.

Key Words. The following key words were used in this study: (((preterm[All Fields] AND Intraventricular[All Fields] AND (“haemorrhage”[All Fields] OR “hemorrhage”[ MeSH Terms] OR “hemorrhage”[All Fields])) OR ((“infant, premature”[MeSH Terms] OR (“infant”[All Fields] AND “premature”[All Fields]) OR “premature infant”[All Fields] OR (“preterm”[All Fields] AND “infant”[All Fields]) OR “preterm infant”[All Fields]) AND (“hydrocephalus”[MeSH Terms] OR “hydrocephalus”[ All Fields]))) OR ((preterm[All Fields] AND (“heart ventricles”[MeSH Terms] OR (“heart”[All Fields] AND “ventricles”[All Fields]) OR “heart ventricles”[All Fields] OR “ventricular”[All Fields]) AND reservoir[All Fields])) AND shunt[All Fields].

Strategy

Two hundred thirteen abstracts were reviewed, after which 98 publications that met the inclusion criteria were selected. In addition to the overall inclusion/exclusion criteria specified in the Methods section of the Guidelines (Part 1), additional inclusion criteria included studies in which infants younger than 12 months with all forms of hydrocephalus—both congenital and acquired—were evaluated to ensure that the maximum number of studies were reviewed. The analysis focused on studies evaluating infants with PHH because of the treatment strategies and challenges unique to this patient population.

As a result of the US National Library of Medicine's search engine functionalities, additional search terms (heart ventricles) not relevant to topics addressed in this chapter were added to the search strategy. Although these search terms remained in the search strategy, we did not recall any references retrieved using them for full-text review. We excluded those references because they were not relevant to the overall scope of this project or the patient population addressed in this chapter and, therefore, did not meet the article inclusion criteria specified in the methodology section of this guideline (Part 1).23

Following an evidentiary analysis and a review of the 98 full-text articles, 68 publications were accepted for inclusion in the evidentiary table and 30 publications were excluded.2,7,12–14,21,22,27,30,33,35,38,48,50–53,55,57,58,62–64,66–68,70,73,75 The evidentiary table was assembled linking recommendations to the strength of the evidence (Levels I–III).

Search Results

Of the 98 full-text articles selected for review, 30 full-text publications were rejected based on the criteria listed above and only 68 articles were used to construct the evidentiary table (Fig. 1). The criteria for the decision to treat were quite variable among different institutions and different study groups. For example, we evaluated 1 Class II study in which hydrocephalus was defined as the atrium of the lateral ventricle measuring > 10 mm on the horizontal plane of a head ultrasound (HUS) study or the body of the lateral ventricle at the level of the midthalamus measuring > 10 mm on a sagittal ultrasound image.10 We reviewed another Class III study in which hydrocephalus was defined as anterior cortical mantle thickness < 20 mm at an average postnatal age of 21 days along with increasing occipitofrontal circumference (OFC) as an indicator of hydrocephalus that should be treated.5 Bada et al.5 reported that of 10 infants requiring shunts, 5 (50%) experienced normal development, which was defined by physical and neurological assessment and evaluation using the Denver developmental screening tool. Evan's ratio, which is described as the lateral measurement of the ventricle across the frontal horns divided by the lateral measurement across the brain (biparietal diameter; also known as the ventricular/biparietal [V/BP] ratio) can also be used to describe the severity of PHH.16 The majority of studies that were evaluated based on an initial diagnosis of PHH on HUS, CT, and MRI studies were also used. Choudhury described mild hydrocephalus as a V/ BP ratio of 0.26–0.40, moderate hydrocephalus as a V/ BP ratio of 0.40–0.60, severe hydrocephalus as a V/BP ratio of 0.60–0.90, and extreme hydrocephalus as a V/ BP ratio of 0.91–1.0.16 These authors also reported that the thickness of the cortical mantle was not a statistically significant indicator of outcome because several infants with extreme hydrocephalus displayed normal motor development.16 One Class II and 1 Class III study indicated that when ventriculoperitoneal (VP) shunts were placed, even in cases of severe or extreme hydrocephalus, there were some infants with normal development and motor outcome (50 of 82 patients in the Choudhury study).5,16 Numerous studies have reported that good neurodevelopmental outcomes may be seen if and when infants with hydrocephalus are aggressively treated and cortical mantle thickness is restored.

Fig. 1.
Fig. 1.

Flowchart showing the process involved in identifying relevant literature. The criteria for “records excluded” and “fulltext articles excluded with reasons” are detailed in Part 1 of the Guidelines.

Results

Surgical Temporizing Measures

Recommendation: Ventricular access devices (VADs), external ventricular drains (EVDs), ventriculosubgaleal (VSG) shunts, or lumbar punctures (LPs) are treatment options in the management of PHH. Clinical judgment is required. Strength of Recommendation: Level II, moderate degree of clinical certainty.

Recommendation: The evidence demonstrates that VSG shunts reduce the need for daily CSF aspiration compared with VADs. Strength of Recommendation: Level II, moderate degree of clinical certainty.

The evidence demonstrates that VADs reduce morbidity and mortality compared with EVDs. Three Class II and 7 Class III studies were included as evidence to support the first recommendation, and these lower-quality studies documented the safety and efficacy of VADs, or Ommaya reservoirs, for the aspiration of CSF, ventricular decompression, and lowering of intracranial pressure.3,8,11,25,26,29,31,39,78,80 The authors of 2 Class II studies reported that ventricular reservoirs may reduce the incidence of shunt infection as well as noninfectious shunt complications.8,26 In one Class II study and one class III study, repeated aspiration of CSF from a VAD did not significantly increase the risk of infection.26,39 Three Class III studies reported that ventricular reservoirs did not significantly reduce the need for permanent shunt placement.29,31,78 One Class III study reported that the use of VADs, compared with the use of continuous ventricular drainage, significantly reduced morbidity and mortality rates that were associated with the surgical treatment of PHH in LBW infants with reservoirs, instead of EVDs (Table 1).26

TABLE 1:

Surgical temporizing measures: summary of evidence*

Authors & YearStudy DescriptionData Class, Quality, & ReasonsResults & Conclusions
Cornips et al., 1997Retrospective review of 14 pts w/ Grade III or Grade IV IVH diagnosed on HUS study & treated w/ EVD.Class IIVentricular drainage is a safe option for infants w/ PHH.
Retrospective review of 2 cohorts: premature infants treated w/ EVD vs those treated medically.
14 pts were compared w/ a historical cohort of 15 infants w/ similar Grade III/IV IVH.
Gurtner et al., 1992Retrospective consecutively enrolled study of 736 LBW infants (< 1500 g).Class IIFrequency & mortality of Grades III & IV hemorrhage in infants weighing btwn 500 & 700 g remained relatively constant over the 3-yr period.
Consecutive, but not a randomized controlled study.
After exclusion of some infants for various reasons, 547 infants were included in the retrospective consecutive review.A nonrandomized historical cohort, compared by yr of treatment & treatment type. 1st yr: EVD.
Authors concluded that there was a significant reduction in morbidity & mortality associated w/ LBW infants when they began using reservoirs instead of EVDs.
Shunts were placed for progressive hydrocephalus & OFC > 95 percentile.2nd & 3rd yr: subcutaneous reservoir was used.
Outcomes evaluated: morbidity, mortality, & need for shunt revision.
3 yrs of data examined by yr, by analyses of variance, & Duncan's mean comparison tests.
Chi-square analyses on discrete variables such as rates of complication & mortality. Student t-test w/ Bonferroni corrections. Spearman correlation coefficients were computed when appropriate. Quantitative data are presented.
Hudgins et al., 1997Use of urokinase via reservoir to treat PHH in 18 pts. 4 different doses of urokinase; ultimately grouped into “high” (n = 9) & “low” dose (everyone else, n = 9).Class II“Low dose” urokinase reduced shunt rate (71% vs 92%) compared to historical controls. Fewer shunt revisions in both groups compared to control group.
Prospective, nonrandomized, case-control series.
Division of 9 pts into “low” dose group would appear to dilute statistical power despite statistical significance obtained.
Both groups compared to historical control group w/ respect to outcome & need for shunt. Prospective, case control.
Lam & Heilman, 2009Single-institution, retrospective historical cohort study of 32 preterm infants w/ PHH. This study compared 2 cohorts of infants: those treated w/ VAD/Ommaya placement vs those treated w/ VSG shunts.Class IIThere was a trend toward VP shunt independence in the VSG shunt group, as compared to the VAD group, but it did not reach significance.
A chi-square test was performed (χ2 = 19.2, df = 1, p = 0.000016, p < 0.05), which showed that VSG shunts significantly reduced the need for daily CSF aspiration compared to VADs.
VSG shunts decreased the need for daily taps. There was a slightly higher rate of complications in the VSG shunt group, but it was not significant.
There were no statistical differences in age or birth weight of the infants in the 2 groups. The groups were studied for IVH grade, need for daily CSF withdrawal, CSF leak from the scalp, CSF infection, & need for a VP shunt.
The higher rate of complications of VSG shunts was not statistically significant compared w/ the VAD group (p = 0.17).
93.75% (15 of 16 pts) in the VAD group required VP shunts while 71.42% (10 of 14 pts) in the VSG shunt group needed VP shunts.
Anwar et al., 1986Consecutive, nonrandomized study of 19 preterm infants w/ PHH who underwent placement of reservoirs for symptomatic hydrocephalus.Class IIIThe authors concluded that reservoirs provide safe & effective treatment for infants w/ PHH & symptomatic hydrocephalus.
Study was a case series of infants weighing <2000 g, w/ clear CSF & treated w/ reservoirs.
Symptomatic hydrocephalus was defined as infants w/ rapidly increasing OFC, ventriculomegaly, & signs of increased ICP present, such as tense fontanelle, splayed sutures, apnea, bradycardia, seizure, feeding difficulties, or lethargy.There was only limited presentation of qualitative & quantitative data. Data included: morbidity, mortality, & need for shunt placement in these infants.
There was no comparison w/ a cohort of nontreated infants or infants treated w/ ventricular drains.
Benzel et al., 199341 pts requiring ventricular drainage for hydrocephalus/PHH were evaluated retrospectively.Class IIIAuthors state, “The placement of ventricular reservoirs is acceptable as an alternative to early placement of ventriculo-peritoneal shunts. This approach may reduce the incidence of shunt infection as well as noninfectious shunt complications.”
Retrospective case series of 41 consecutive premature infants.
All drainage procedures were performed on pts w/ IVH & hydrocephalus (Grade III [25 pts]) & pts w/ IVH & IPH (Grade IV [16 pts]) in whom medical management had failed.
26 ventricular reservoirs (Rickham or McComb reservoirs) were placed in neonates weighing <1500 g, allowing for safe but intermittent ventricular access.18 of these reservoirs were subsequently converted to VP shunts. 32% of pts developed a VP shunt &/or reservoir infection & 59% required a shunt revision during the 1st yr of life.
No Grade IV pts achieved normal functional level, while 10 Grade III pts did. The incidence of severe developmental delay (44% vs 28%) & death (38% vs 12%) was greater in Grade IV than in Grade III pts.
Berger et al., 2000Retrospective review of outcomes after placement of EVDs in 37 premature infants (51 drains). PHH diagnosed by ultrasound.Class IIINeurodevelopmental outcome dependent on extent of parenchymal injury.
Single-institution retrospective review.
Infection rates: 5.4% pts, 3.9% drain. 11 of 37 pts did not require shunt placement.
Brouwer et al., 2007Single-center retrospective review of 76 preterm infants treated for PHVD w/ ventricular reservoirs.Class IIIWhile the no. of reservoir punctures did not change, the infection rate was lower in the 2nd, more recent interval (2 of 50 pts [4%] vs 5 of 26 pts [19.2%]).
Single-center retrospective review.
Infection rates were measured in 2 successive 6-yr intervals. No. of reservoir punctures also examined.
Conclusion: Risks associated w/ ventricular reservoirs are w/in acceptable limits.
de Vries et al., 2002Retrospective review of consecutive preterm infants (EGA ≤34 wks) w/ Grade III IVH treated for posthemorrhagic ventricular dilatation in 5 collaborating NICUs (n = 95). Pts were subdivided into early intervention or late intervention groups, depending on their ventricular index at the time of initial treatment.Class IIIEarly treatment was associated w/ a reduced requirement for VP shunt (OR = 0.22) & reduced risk of moderate-to-severe disability.
Multicenter study, retrospective case series.
Treatments were not standardized treatments.
LPs, reservoir, & shunt.
Gaskill et al., 1988The use of a subcutaneous reservoir was studied in a consecutive, nonrandomized series of 38 infants w/ preterm IVH & PHH. In all infants LP & medical treatment had failed.Class IIIThe authors concluded that early reservoir placement is a feasible, safe, & effective treatment for PHH associated w/ preterm IVH.
Retrospective study of a series of premature infants who required temporizing measures (reservoir placement) after medical treatment/LP for PHH had failed.
There were 28 survivors overall (8 died before a shunt could be placed, 2 died after shunt placement). 4 survivors (15%) did not require a shunt.
Harbaugh et al., 1981Retrospective review of 11 premature infants w/ IVH & PHH who were treated w/ tunneled EVD. The mean duration of drainage for this group was 20.7 days.Class IIIEVD via a subcutaneously tunneled catheter was found to be a safe & reliable initial method of treating PHH in premature infants.
Small retrospective case review.
No morbidity or mortality occurred as a result. 7 of 11 pts required a shunt. 2 of 11 did not require a VP shunt.
Heep et al., 2001Safety/efficacy of Rickham reservoir placement for pts w/ PHH.Class IIIOmmaya/Rickham reservoir is a safe, effective option for managing PHH until pt is ready for a shunt. 5% infection rate, 85% of pts needed a shunt.
Retrospective review. Broad inclusion criteria for reservoir placement.
No comparison w/ pts managed w/ other methods.
Hudgins et al., 1998Use of VAD in 149 pts w/ PHH. Daily taps for 1st “several” days (10–15 cm3/kg).Class III8% infection & 20% revision rates. 88% shunt implantation rate.
Single-institution retrospective case series.
Shunts placed at 2 kg if pt was still symptomatic, but criteria not otherwise clear on when to stop VAD aspirations.
Kazan et al., 2005Retrospective review of preterm & LBW infants diagnosed w/ IVH by ultrasound (n = 42).Class IIIRisk factors for VP shunt included IVH grade, later EGA at birth, & age (days) at time of IVH, but not treatment for IVH/PHH (acetazolamide, furosemide, LP, & external ventricular drainage).
11 infants who required VP shunts were compared w/ 31 who did not. All pts received acetazolamide & furosemide as an initial medical treatment.Small, single-center retrospective case series w/ grouping of pts despite variable treatments.
Kormanik et al., 2010Retrospective review of the outcome of infants receiving a ventricular reservoir for PHH.Class III35 ventricular reservoirs were placed. 6 pts (17%) were excluded. 29 pts had a total of 681 taps. There was no increased risk of infection from repeated or daily aspiration.
Retrospective observational study: a review of medical records of all infants who received a ventricular reservoir in 1 center between 2000 & 2007.
Only 1 CSF culture-proven reservoir infection: Candida albicans.
Kreusser et al., 1984Study of 19 consecutive infants w/ PHH documented by CT or cranial ultrasound, & ICP measurement by an indwelling ICP monitor.Class IIIExternal ventricular drainage decreased ventricular size.
Case series of a group of 19 consecutive infants treated w/ external ventricular drainage. There was no randomization to treat or not treat, & no randomization of type of treatment. There was no case-controlled comparative cohort or group.
3 infants did not develop recurrent hydrocephalus & did not require a shunt. 16 infants suffered recurrent hydrocephalus, w/in 1 wk after drain removal. Another EVD was placed in 10 pts.
5 of 19 pts were initially treated w/ LP, 30–40 ml CSF drained daily for 5–7 days.
Surviving pts were evaluated w/ the Bayley Scale of Infant Development, the Cartell Infant Intelligence Scale, or the Stanford-Binet Intelligence Test, based on the child's age at evaluation. Developmental quotient (DQ) was determined using the Denver Developmental Screening Test.
Following repeated EVDs, 9 of the 10 infants were stable enough for a shunt. The authors conclude that EVD is a safe & effective treatment for PHH.
Limbrick et al., 2010Large single-center retrospective review of 325 preterm infants w/ Grade III or IV IVH. The development of PHH & the need for a temporizing device (VAD or VSG shunt) were studied. Infections, complications, & need for VP shunt were analyzed, as was the mortality rate.Class IIIThere was no significant difference in outcome between infants treated w/ VAD or VSG shunts.
Retrospective analysis showed 75.4% of the 65 infants treated w/ VAD needed a shunt; 66.7% of the 30 treated w/ VSG shunts required a shunt.
There was no significant difference in the infection rate between VAD & VSG shunts, revision rate, or VP shunt infection afterwards.
Rahman et al., 1993Single-institution, small retrospective review of 37 pts w/ PHH, 31 of whom required VP shunt.Class IIISuggested LP, VSG, Ommaya reservoir, & VP shunts are safe & effective. Of 26 infants w/ PHH treated w/ EVD, 20 did require shunts. 6 did not require further treatment.
Observational study of outcomes. LP, EVD, VSG shunts, & Ommaya reservoirs were used.
No statistical data available.
Rhodes et al., 198737 premature infants w/ PHH were treated w/ an EVD. Complications, including morbidity, are presented.Class IIILevel III
Retrospective, consecutive case series.Ventricular drainage is a safe & effective mechanism for treating infants w/ PHH & may obviate the need for a shunt.
32 pts did not require a permanent shunt. Neurodevelopmental & neuromuscular outcomes are presented.
Weninger et al., 1992Study of 27 consecutive infants w/ an average gestational age of 31 wks, who had PHH & increased ICP & were treated w/ a tunneled EVD.Class IIIPHH was successfully treated in all pts; the EVD was left in situ for an average of 23 ± 9 days. 4 pts died of unrelated causes, & 23 pts survived. 16 required shunts.
The study is a case series report.
PHH was defined as ventricular dilation, progressively increasing OFC, bulging fontanelle, widening of the sutures, apnea, or bradycardia.
Neurological outcome correlated w/ severity of the Grade of IVH. Grade IV IVH infants had the worst neurological outcomes, despite treatment.
The authors conclude that EVD is a safe & effective treatment for PHH in premature infants.
Willis et al., 200932 premature infants w/ PHH were treated w/ shunts or reservoirs.Class IIIInitially reservoirs were placed in 46.8% of pts & shunts in 53% of pts. The groups were not comparable.
Retrospective, consecutive case series of 32 infants who needed treatment for PHH. Multivariate analysis & time series were used to identify factors that influence the outcome in terms of shunt revisions.
Permanent shunts were needed in 90.6% of cases.
Infants who were treated w/ a shunt initially had more revisions. p = 0.0027.
CSF reservoirs are a safe & effective method of treatment in infants considered too small for VP shunt placement, but this does not obviate the need for a shunt.
Yu et al., 2009The authors performed a retrospective case study of 11 pre-mature infants w/ PHH who were all treated w/ a subcutaneous reservoir for CSF aspiration.Class IIIThe authors concluded that CSF reservoir treatment is safe & effective for infants w/ PHH.
Retrospective case series.

EGA = estimated gestational age; ICP = intracranial pressure; IPH = intraparenchymal hemorrhage; NICU = neonatal intensive care unit; pts = patients.

The placement of an EVD has also been used to treat hydrocephalus in preterm infants with PHH and is an option for these children, as shown in 1 Class II and 7 Class III studies.9,17,28,36,40,59,60,69 Three Class III studies reported that an EVD obviated the need for VP shunt placement in fewer than one-third of infants treated.9,40,60 More than 50% of preterm infants with PHH did require permanent VP shunt placement following removal of an EVD (95 out of 132 survivors required a shunt).9,40,59,60,69

It has been reported that placement of a VSG shunt may reduce the need for permanent shunt placement. The authors of Class II and Class III studies reported trends toward shunt independence, but the studies only enrolled 32 and 95 patients, respectively, and the results were not statistically significant.41,43 In their report of a Class II, retrospective historical cohort study, Lam and Heilman demonstrated that VSG shunting significantly reduced the need for daily CSF aspiration, which may decrease the risk of introducing a de novo CSF infection.41 A chisquare test performed on their data indicated that a VSG shunt did significantly reduce the need for daily CSF aspiration when compared with a VAD (χ2 = 19.2, df = 1, p = 0.000016, p < 0.05).41 This may reduce the risk of infection or other complications. A larger, prospective study reported a statistically significant decreased need for permanent CSF diversion in infants treated with VSG shunts.43 This study reported that 66% of infants (20 of 30) treated with VSG shunts required VP shunts and 33% (10 of 30) remained shunt free; this was compared with a group of infants treated with VADs in which 75% (49 of 65) required VP shunts and only 25% of infants (16 of 65) remained shunt free.43

In 2 studies, 1 intervention was compared to another with specific recommendations about the timing of the intervention for temporizing measures for the treatment of PHH in very LBW infants. In 1 Class III study, the authors compared early versus late intervention, as assessed by ventricular dilation in 5 collaborating neonatal centers.18 Ninety-five patients were subdivided into early intervention or late intervention groups, depending on their ventricular index at the time of initial treatment. Early treatment was safe and effective regardless of whether LP and/or reservoir placement was used. Early intervention was associated with a reduced requirement for a VP shunt (OR = 0.22) and reduced risk of moderate-to-severe disability.18 Additionally, there was a single Class III observational study of outcomes in which LPs, EVD, VSG shunts, and reservoirs were used.57 All interventional studies were found to be safe and effective.57

Routine Use of Serial Lumbar Puncture

Recommendation: The routine use of serial lumbar puncture (LP) is not recommended to reduce the need for shunt placement or to avoid the progression of hydrocephalus in premature infants. Strength of Recommendation: Level I, high degree of clinical certainty.

One Class I study was included, and it reported no statistical differences in outcomes of preterm infants with PHH treated with observation alone or infants treated with daily LP (Table 2).4 Lumbar puncture is often used early in the treatment of PHH, despite the fact that there is no statistically significant reduction in the need for a shunt or progression of PHH.4,54 In fact, LP neither predicts nor prevents the need for a permanent VP shunt.36 A second study, a Class III study, also reported no difference in adverse outcome regardless of whether infants were untreated or treated with serial LP.15 Without aggressive treatment of hydrocephalus and with persistent ventricular dilation, outcome was poor.15 Additionally, there was a single Class III study that concluded that repeated LPs may cause or contribute to subsequent shunt infection.6 Although LP may be useful for drawing off CSF as an immediate treatment for elevated intracranial pressure in infants with PHH, or for sampling CSF, we do not recommend the routine use of LP to eliminate the need for a VP shunt.15

TABLE 2:

Serial lumbar punctures: summary of evidence

Authors & YearStudy DescriptionData Class, Quality, & ReasonsResults & Conclusions
Anwar et al., 1986Randomized controlled study of 47 consecutive preterm infants w/ PHH & Grade III or Grade IV IVH.Class IThere were no statistical differences in outcomes studied in infants treated w/ observation alone & infants treated w/ daily LP.
Consecutively enrolled infants randomized to treatment (daily LP) (n = 24) or observation only (n = 23).
Infants enrolled in the study were randomized to observation only or daily LP. Cohorts were studied for morbidity, mortality, & need for a shunt.
10 of 24 infants treated w/ LP required shunts & 9 of 23 infants in the observation-only group required shunt placement for progressive PHH & hydrocephalus.Although LP was safe, there was no statistically significant reduction in the need for shunt or progression of PHH.
Behjati et al., 2011Case series study that investigated risk factors for VP shunts in infants w/ hydrocephalus following IVH in 97 consecutive preterm infants w/ IVH.Class IIIInfants w/ Grade III or IV IVH are atthe highest risk of PHH & hydrocephalus.
Case series of 97 infants w/ IVH associated w/ prematurity. Risks factors associated w/ need for a shunt were investigated. Infants were followed for 1 yr.
11 of 31 pts who required a shunt developed shunt infection, which was significantly associated w/ repeated LPs.
Morbidities & mortalities were reported in a quantitative fashion. Pts treated medically w/ acetazolamide showed no benefit; however, infants treated w/ repeated CSF drainage through LP did have a higher shunt infection rate once the shunts were placed.
Chaplin et al., 1980Retrospective review of 22 consecutive LBW infants w/ PHH.Class IIIFollow-up when pt was 1–8 yrs of age in 18 infants.
Retrospective review of 22 infants w/ PHH. There were 2 cohorts: 12 pts treated w/ VP shunt, & 10 pts treated w/ LP & diuretics.
All pts developed hydrocephalus after 2 wks of age. The first 12 required VP shunts. In 10 infants born after September 1974, an attempt was first made to control the hydrocephalus w/ repeated LPs & diuretics prior to placing a shunt.2 of 12 pts treated w/ permanent shunts & 3 of 6 pts treated medically had IQ scores ≥85. These results indicate a poor long-term outlook for the LBW infant who develops clinically overt hydrocephalus after intracranial bleeding.
In 7 of 10 pts hydrocephalus was successfully arrested by medical therapy alone.
Kazan et al., 2005Single-center retrospective review of preterm & LBW infants w/ IVH diagnosed by ultrasonography (n = 42).Class IIIRisk factors for VP shunt included IVH grade, later EGA at birth, & age (days) at time of IVH, but not treatment for IVH/PHH (acetazolamide, furosemide, LP, or external ventricular drainage).
Small, retrospective case series w/ grouping of pts despite variable treatments.
11 infants who required VP shunts were compared w/ 31 who did not. All pts received acetazolamide & furosemide as an initial medical treatment.
Müller et al., 1998Effect of aggressive LP schedule on PHH.Class IIISerial LP should be started early for treatment of hydrocephalus.
LPs started at 0–4 days; on average 11 LPs performed per pt, 15 ml/kg or end of CSF flow per LP.Single-institution nonrandomized prospective study.
Used protein, red blood cell count, glucose, & ventricle size to determine end point.16% complete resolution, 65% ventriculomegaly but no shunts, 19% w/ shunts.

Nonsurgical Temporizing Agents

Intraventricular Thrombolytic Agents

Recommendation: Intraventricular thrombolytic agents including tissue plasminogen activator (tPA), urokinase, or streptokinase are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

Based on 1 high-quality Class I study, the DRIFT procedure—DRainage, Irrigation, and Fibrinolytic Therapy (intraventricular tPA)—is not recommended for PHH.71 DRIFT did not significantly reduce shunt surgery or death, but it was associated with an increased rate of secondary IVH (Table 3).71 Forty-four percent (15 of 34) of infants in the DRIFT group died or required a shunt, compared with 50% (19 of 36) of infants who received standard treatment. Thirty-five percent (12 of 34) of preterm infants in the DRIFT study had secondary IVH, compared with 8% (3 of 34) who received standard treatment.71 These results differ from those of earlier Class II and Class III studies in which a decreased rate for the need for permanent shunt placement was reported when low-dose urokinase or fibrinolytic therapy with tPA was used for ventricular irrigation and clot reduction.32,61,75,77

TABLE 3:

Intraventricular thrombolytic agents: summary of evidence

Authors & YearStudy DescriptionData Class, Quality, & ReasonsResults & Conclusions
Whitelaw et al., 2007Randomized multicenter clinical trial comparing standard treatment to DRIFT.Class I15 of 34 pts (44%) in the DRIFT group died or required a shunt, compared w/ 19 of 36 pts (50%) who received standard treatment.
Multicenter randomized controlled trial.
70 infants enrolled (34: DRIFT; 36: standard treatment).
Outcomes: pts at 6 mos of age or at hospital discharge: death or VP shunt surgery, secondary IVH, & infection.12 of 34 pts (35%) in DRIFT group had secondary IVH compared w/ 8% of pts who received standard treatment.
Conclusion: DRIFT did not reduce shunt surgery or death but was associated w/ an increased rate of secondary IVH.
Hudgins et al., 1997Use of urokinase via reservoir to treat PHH in 18 pts. 4 different doses of urokinase; pts ultimately grouped into “high” (n = 9) & “low” dose (everyone else, n = 9).Class II“Low dose” urokinase reduced shunt rate
Prospective nonrandomized case-control series.(71% vs 92%) compared to historical controls.
Division of 9 pts into “low” dose group would appear to dilute statistical power, despite statistical significance obtained.Fewer shunt revisions in both groups compared to control group.
Both groups compared to historical control group w/ respect to outcome & need for shunt. Prospective, case control.
Whitelaw & Odd, 2007Review & meta-analysis of 2 prospective case-control studies (Luciano et al., 1997 & Yapicioğlu et al., 2003).Class IINo difference in mortality or VP shunt rate was observed w/ intraventricular streptokinase.
Both sources' studies were Class II (both were small randomized, prospective case-control studies).
Both source studies included total of 12 pts: 6 cases, 6 controls.Intraventricular fibrinolytic therapy cannot be recommended for infants following IVH.
Meta-analysis.
Yapicioğlu et al., 2003Single-blind prospective study.Class II5 of 6 infants in the streptokinase group & 3 of 6 in the control group required VP shunts.
12 preterm infants who developed PHH were randomly assigned to the control group (no treatment) or to receive intraventricular streptokinase (×3 days). Note: the streptokinase group also had an LP (10–15 ml) prior to treatment & then daily LPs (5–10 ml). They also received intraventricular vancomycin.Small randomized, prospective study
No complications were noted.
Routine use of intraventricular streptokinase in PHH was not recommended.
Primary outcome: VP shunt placement.
Richard et al., 2001Single-institution experience w/ Ommaya reservoir in 64 pts.Class IIIFibrinolytic therapy led to statistically significant lower rate of shunt placement (31% vs 87%).
Retrospective case series.
17 pts received fibrinolytic therapy through Ommaya reservoir.Statistics performed on fibrinolytic therapy subgroup, which consisted of 2 different agents w/ multiple doses. Fibrinolytic subgroup then mixed back into overall outcome analysis.
Whitelaw et al., 2003Prospective Phase I trial of new treatment methodology (DRIFT) for prevention of PHH of prematurity.Class III1 pt died. 17 of 23 (74%) did not require a shunt. 2 pts experienced secondary IVH, & 2 experienced infections. 19 pts >12 mos had neurodevelopmental testing: 8 (42%) were normal; 7 (37%) had a single disability; 4 (21%) had multiple disabilities.
Prospective Phase I trial in 24 pts & compared w/ historical controls.
Data from 24 pts compared w/ historical controls. Outcome measures: death, need for shunt, secondary IVH, infection, & neurodevelopmental outcome.
Conclusion: Compared w/ historical controls, DRIFT reduced the need for shunts & showed a trend toward lower rates of mortality & disability.
Whitelaw et al., 1992Prospective study of 9 preterm infants w/ progressive posthemorrhagic ventricular dilation who underwent a 48- to 72-hr continuous intraventricular infusion of streptokinase.Class IIIAll pts survived; only 1 of 9 required a shunt prior to discharge (later reports indicated that a total of 4 of 9 ultimately required shunts).
Small, prospective, nonrandomized cohort study (Phase I trial).
No infections, 1 repeat hemorrhage.
Outcomes: death, need for shunt, secondary IVH, & infection.
Whitelaw et al., 1996Phase I study to evaluate safety of tPA in 22 preterm infants w/ posthemorrhagic ventricular dilation.Class IIIDose-finding & pharmacokinetic data reported ([tPA], half-life tPA).
Small, prospective, nonrandomized cohort study (Phase I trial).
21 (95%) of 22 pts survived. 9 (43%) of 21 pts required shunts. 1 pt experienced secondary IVH.
Dose-finding data reported.Conclusion: tPA resulted in survival w/o shunt in most pts.
Outcome measures: death & need for shunt prior to discharge & secondary IVH.

Reviews conducted by Whitelaw and Odd74 have also revealed that intraventricular injection of streptokinase has not been shown to be beneficial.74 A single case report of intravenous streptokinase, published in 1998, suggested that there may be some benefit.45 This report was followed by an early Class III study that found benefit in a nonrandomized cohort of preterm infants with PHH who were treated with intravenous low-dose streptokinase.76 However, data from a later Class II study led to the conclusion that routine use of intraventricular streptokinase in PHH was not recommended.79 These studies were included in the 2007 Whitelaw and Odd Cochrane review,74 which argues against intravenous streptokinase for the treatment of PHH in preterm infants (Table 3).

Despite increased short-term morbidity and recurrent IVH, some benefits were noted in the DRIFT survivors.72 In the most recent Whitelaw study,72 the reduction in the primary long-term outcome—death or severe disability—at 2 years in the DRIFT group reached statistical significance when adjusted for sex, birth weight, and grade of IVH. Severe cognitive disability also was reduced, and this improvement in cognitive function was statistically significant. There was also a reduction in severe sensorimotor disability with DRIFT, but this clinical improvement did not reach statistical significance. The authors hypothesized that the greater effect on cognitive rather than sensorimotor function may be attributed to parenchymal infarction in the periventricular white matter, which was seen in about half of the infants enrolled in the trial.72

Acetazolamide and Furosemide

Recommendation: Acetazolamide and furosemide are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

After our review of the literature, we found two Class I studies that reported that preterm infants with a diagnosis of PHH who were treated with acetazolamide and furosemide demonstrated higher risks of neurological complications, morbidity, and mortality (Table 4).34,37 The International Posthemorrhagic Ventricular Dilation (PHVD) Drug Trial Group reported that administration of acetazolamide plus furosemide leads to higher rates of shunt placement (relative risk 1.42) and morbidity (84% vs 60%) compared with standard therapy.34 Kennedy et al.37 reported that treatment of PHVD with acetazolamide and furosemide did not decrease the rate of shunt placement (64% in the acetazolamide/furosemide group vs 52% in the control group, not treated with acetazolamide/ furosemide).37 However, treatment was associated with an increased rate of neurological morbidity (81% vs 66%).37 Treatment of PHVD with acetazolamide and furosemide was not recommended.37 One Class III study reported this treatment was not associated with VP shunt placement, but the severity of IVH (based on IVH grade) and the patient age at the time of IVH were significantly associated with the need for permanent CSF diversion.36 Kennedy et al. also noted that the ventricular index at time of entry into trial was the only factor significantly predictive of death or need for shunt, after multiple logistic regression analysis.37

TABLE 4:

Acetazolamide/furosemide: summary of evidence*

Authors & YearStudy DescriptionData Class, Quality, & ReasonsResults & Conclusions
International PHVD Drug Trial Group, 1998Use of acetazolamide & furosemide in pts w/ PHH.Class IAcetazolamide & furosemide led to higher rates of shunt placement (RR 1.42) & higher morbidity (84% vs 60%) compared w/ standard therapy
Randomized controlled multicenter, well designed.
Comparison w/ standard therapy for shunt placement & neurological outcome.
Kennedy et al., 2001Multicenter randomized controlled trial designed to test the hypothesis that treatment of PHVD w/ acetazolamide & furosemide (vs standard therapy) would reduce: 1) risk of shunt placement or death before 1 yr; & 2) death or disability at 1 yr.Class ITreatment of PHVD w/ acetazolamide & furosemide did not decrease the rate of shunt placement (64% in acetazol-amide/furosemide group vs 52% in standard therapy group; RR = 1.23, 95% CI = 0.95–1.59) & was associated w/ increased neurological morbidity (81% vs 66%).
Multicenter randomized controlled trial. Positive: Excellent subject retention. Therapeutic CSF removal in 56% of pts (equivalent in both groups).
Negative: Acetazolamide & furosemide administration was stopped in many pts due to adverse effects. Also, furosemide was given in the standard therapy group in some cases.
177 pts recruited from 55 centers world-wide.
Authors concluded: “Treatment of PHVD w/ acetazolamide & furosemide cannot be recommended.”
Kazan et al., 2005Single-center retrospective review of preterm & LBW infants diagnosed w/ IVH by ultrasonography (n = 42).Class IIIRisk factors for VP shunt included IVH grade, later EGA at birth, & age (days) at time of IVH, but not treatment for IVH/PHH (acetazolamide, furosemide, LP, or external ventricular drainage).
Small retrospective case series w/ grouping of pts despite variable treatments.
11 infants who required VP shunts were compared w/ 31 infants who did not. All pts received acetazolamide & furose-mide as an initial medical treatment.

RR = relative risk.

Timing of Shunt Placement

Strength of Recommendation: There is insufficient evidence to recommend a specific infant weight or CSF parameter to direct the timing of shunt placement in premature infants with PHH. Strength of Recommendation: Level III, unclear degree of clinical certainty.

There were two Class III studies which evaluated the lower limits of infant weight at time of initial shunt insertion (Table 5).4,8 A weight of 1500 g was safely used as a criterion for VP shunt placement in the Benzel study.8 A single Class III study showed that CSF cell count, protein, and glucose levels were not statistically related to the occurrence of shunt failure or infection in the study population.24 The authors recommended that placement of the shunt be timed when the infant's age, weight, and overall stability allow.24

TABLE 5:

Timing of shunt placement—specific weight or CSF parameter: summary of evidence

Authors & YearStudy DescriptionData Class, Quality, & ReasonsResults & Conclusions
Anwar et al., 1986Consecutive, nonrandomized study of 19 preterm infants w/ PHH who underwent placement of reservoirs for symptomatic hydrocephalus.Class IIIAuthors concluded that reservoirs provide safe & effective treatment for infants w/ PHH & symptomatic hydrocephalus.
Case series study of infants who weighed <2000 g & were treated w/ reservoirs. Data include morbidity, mortality, & need for shunt placement in these infants.
Symptomatic hydrocephalus was defined as presence of rapidly increasing OFC, ventriculomegaly, & signs of increased ICP, such as tense fontanelle, splayed sutures, apnea, bradycardia, seizure, feeding difficulties, or lethargy.
There was no comparison w/ a cohort of nontreated infants or infants treated w/ ventricular drains.
Benzel et al., 199241 pts requiring ventricular drainage for hydrocephalus/PHH were evaluated retrospectively. All drainage procedures were performed in pts w/ IVH & hydrocephalus (Grade III [25 pts]) & in pts w/ IVH & IPH (Grade IV [16 pts]) in whom medical management failed.Class IIIAuthors endorse reservoirs as an alternative to early shunts & report that this strategy may “reduce the incidence of shunt infection as well as noninfectious shunt complications.”
Retrospective case series of 41 consecutive premature infants.
There was a VP shunt &/or reservoir infection in 32% of pts.
59% of pts required a shunt revision during the 1st yr of life.
26 ventricular reservoirs were placed in neonates weighing <1500 g; 18 of these reservoirs were subsequently converted to VP shunts.
No Grade IV pts achieved normal functional level, while 10 Grade III pts did. The incidence of severe developmental delay (44% vs 28%) & death (38% vs 12%) was greater in the Grade IV than in Grade III pts.
Fulkerson et al., 2011Premature infants w/ PHH have a high risk of shunt obstruction & infection. Risk factors for complications include grade of IVH & age at shunt insertion.Class IIIAuthors concluded that neither CSF cell count nor protein or glucose levels were statistically related to the occurrence of shunt failure or infection in the study population. The authors recommend that placement of the shunt be timed when age, weight, & the overall stability of the infant allow.
Retrospective cohort study evaluating the risk factors for shunt failure in preterm infants w/ IVH & PHH.
There is anecdotal evidence that the amount of red blood cells or protein levels in the CSF may also increase shunt complications.Inclusion criteria & preintervention data points (baselines) were well documented. Outcomes reported included early shunt failure or infection w/in 3 mos of shunt.
This study examined whether any relationship exists between CSF constituents & shunt malfunction or infection.
“Each CSF parameter was modeled as a possible predictor of the presence or absence of shunt malfunction or infection. Statistical significance was set at a probability level < 0.05.”

Endoscopic Third Ventriculostomy

Recommendation: There is insufficient evidence to recommend the use of endoscopic third ventriculostomy (ETV) in premature infants with PHH. Strength of Recommendation: Level III, unclear degree of clinical certainty.

Although ETV was discussed in several full-text articles that we reviewed, there was insufficient evidence available for us to make a recommendation for or against its use for the treatment of PHH in premature infants (Table 6). Endoscopic third ventriculostomy for the treatment of hydrocephalus in infants and children will be discussed more thoroughly in subsequent chapters (in particular, Part 4).42

TABLE 6:

Endoscopic third ventriculostomy for PHH in premature infants: summary of evidence*

Authors & YearStudy DescriptionData Class, Quality, & ReasonsResults & Conclusions
Elgamal et al., 2011Review of 52 consecutive ETV procedures in 49 infants w/ hydrocephalus not necessarily associated w/ preterm IVH.Class IIIAuthors concluded that the success rate of 69.4% indicates that ETV is safe & effective in infants w/ hydrocephalus not associated w/ PHH & prematurity.
Case series of infants treated w/ an ETV. Infants were followed up for 68 mos on average.
Most infants (n = 31) had aqueductal stenosis. The remaining infants w/ hydrocephalus had other causes for it including Chiari II, Dandy-Walker cysts, quadrigeminal lipoma, & cerebellopontine angle arachnoid cyst. Only 6 pts had PHH caused by preterm IVH.
6 of the 7 infants w/ PHH from premature birth required a shunt.Infants w/ PHH from premature birth didnot benefit from ETV.
Lipina et al., 2008Retrospective consecutive case series of 14 infants <6 mo of age presenting w/ obstructive hydrocephalus.Class IIIETV was successful in 57% of pts—the majority of them w/ primary aqueductal stenosis. In the remaining 6 pts, a VP shunt was needed.
This study included a small number of pts w/ very different etiologies for hydrocephalus.
8 of 14 pts had PHH.
ETV was considered successful when a VP shunt was not necessary.
Peretta et al., 2007Single-institution retrospective review of 18 consecutive preterm infants w/ PHH.Class IIIRecommended combining Ommaya placement w/ ETV. It reduces shunt dependency in this condition.
Small single-institution retrospective case series w/ variable treatment patterns. 3 of the surviving 17 infants (17.6%) treated w/ Ommayas did not require additional surgery. 14 of 17 required VP shunt (n = 5) or ETV (n = 9).
Pts were treated w/ placement of an Ommaya reservoir for temporizing ventricular decompression. When necessary, pts later underwent VP shunt placement (n = 5) or ETV (n = 9).
While additional surgeries were required in the majority of cases, 59% of pts were shunt free at the last follow-up.
Siomin et al., 2002Multicenter retrospective case series of 101 pts who underwent ETV for hemorrhage or infection. Both pediatric & adult pts included.Class IIIETV was successful in 52% of pts w/ PHH of prematurity.
Multicenter study w/ a minority of pts (25%) w/ PHH of prematurity.
Note: ETV was successful in 13 of 13 of pts w/ PHH who were previously treated w/ a shunt, whereas it was unsuccessful in 12 of 12 pts treated w/ ETV as the firstline treatment.
Of the 101 pts, 25 were treated for PHH of prematurity, & specific data were reported for this cohort.
Successful ETV was defined as no further hydrocephalus operations required.ETV was not successful in pts w/ both hemorrhage & infection.

Excluded Studies

We excluded 1 Class III study for low “preterm” patient representation (7 patients); in the review of 52 consecutive ETV procedures in 49 infants with hydrocephalus, most infants (31 patients) had aqueductal stenosis.20 Of the 7 infants with preterm PHH, 6 required a shunt even after ETV. Infants with PHH from premature birth did not benefit from ETV.20 We excluded another Class III study including patients with different etiologies for hydrocephalus.44 Although ETV was successful in 57% of patients (8 of 14), the majority of those infants had congenital aqueductal stenosis without PHH. In the remaining 6 patients, a VP shunt was needed. In 1 Class III single-institution retrospective case series, 18 preterm infants with PHH were treated initially with Ommaya reservoir placement: 1 patient died, 5 patients received a VP shunt, and 9 patients underwent ETV.56 Three patients did not require any further intervention. While overall, 59% were shunt free at the last follow-up, 5 of the 9 patients who were treated with ETV had to undergo repeated surgery for VP shunt placement. The authors recommended combining placement of an Ommaya reservoir with ETV to reduce shunt dependency for preterm infants with PHH.56 There was a large (101 patients) Class III multicenter, retrospective study evaluating the success rate of ETV in patients with hydrocephalus from subarachnoid hemorrhage, IVH, and/or CSF infection; a minority of the patients (25% [25 of 101]) had PHH of prematurity.65 Overall, ETV was successful in 52% of the infants with PHH of prematurity. Endoscopic third ventriculostomy was successful in 100% (13 of 13) of children with a history of preterm PHH, even though these patients were initially treated with a shunt. Endoscopic third ventriculostomy was unsuccessful in 12 of 12 infants treated with ETV as the first-line treatment, following preterm PHH. In patients with both hemorrhage and infection, ETV was not successful.65

Conclusions

Surgical Temporizing Measures

Recommendation: Ventricular access devices (VADs), external ventricular drains (EVDs), ventriculosubgaleal (VSG) shunts, or lumbar punctures (LPs) are treatment options in the management of posthemorrhagic hydrocephalus (PHH). Clinical judgment is required. Strength of Recommendation: Level II, moderate degree of clinical certainty.

Recommendation: The evidence demonstrates that VSG shunts reduce the need for daily CSF aspiration compared with VADs. Strength of Recommendation: Level II, moderate degree of clinical certainty.

The evidence demonstrates that VADs reduce morbidity and mortality compared with EVDs.

Routine Use of Serial Lumbar Punctures

Recommendation: The routine use of serial lumbar puncture (LP) is not recommended to reduce the need for shunt placement or to avoid the progression of hydrocephalus in premature infants. Strength of Recommendation: Level I, high clinical certainty.

Nonsurgical Temporizing Measures

Recommendation: Intraventricular thrombolytic agents including tissue plasminogen activator (tPA), urokinase, or streptokinase are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

Recommendation: Acetazolamide and furosemide are not recommended as methods to reduce the need for shunt placement in premature infants with PHH. Strength of Recommendation: Level I, high clinical certainty.

Timing of Shunt Placement

Recommendation: There is insufficient evidence to recommend a specific weight or CSF parameter to direct the timing of shunt placement in premature infants with PHH. Clinical judgment is required. Strength of Recommendation: Level III, unclear clinical certainty.

Endoscopic Third Ventriculostomy

Recommendation: There is insufficient evidence to recommend the use of endoscopic third ventriculostomy (ETV) in premature infants with PHH. Strength of Recommendation: Level III, unclear clinical certainty.

Acknowledgments

We acknowledge the American Association of Neurological Surgeons (AANS)/Congress of Neurological Surgeons (CNS) Joint Guidelines Committee for the members' reviews, comments, and suggestions; the Hydrocephalus Association and Debby Buffa, patient advocate representative, for participation and input throughout the guidelines development; Pamela Shaw, research librarian, for her assistance with the literature searches; Kevin Boyer for his assistance with data analysis; and Sue Ann Kawecki for her assistance with editing.

We acknowledge the following individuals for their contributions throughout the review process: Timothy Ryken, M.D.; Kevin Cockroft, M.D.; Sepideh Amin-Hanjani, M.D.; Steven N. Kalkanis, M.D.; David P. Adelson, M.D.; Brian L. Hoh, M.D.; Mark D. Krieger, M.D.; Mark E. Linskey, M.D.; Jeffrey J. Olson, M.D.; Patricia Raskin, M.D.; Krystal L. Tomei, M.D.; and Monica Wehby, M.D.

Disclosure

Dr. Limbrick receives research funding from the National Institute of Neurological Disorders and Stroke. The systematic review and evidence-based guidelines were funded exclusively by the CNS and AANS Pediatric Section, which received no funding from outside commercial sources to support the development of this document.

Conflict(s) of Interest: None. All Pediatric Hydrocephalus Systematic Review and Evidence-Based Guidelines Task Force members declared any potential conflicts of interest prior to beginning work on this systematic review and evidence-based guidelines.

Author contributions to the study and manuscript preparation include the following. Conception and design: AANS/CNS Joint Section on Pediatrics. Acquisition of data: all authors. Analysis and interpretation of data: all authors. Drafting the article: Mazzola. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Flannery. Administrative/technical/material support: all authors. Study supervision: Flannery.

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    Harbaugh RESaunders RLEdwards WH: External ventricular drainage for control of posthemorrhagic hydrocephalus in premature infants. J Neurosurg 55:7667701981

  • 29

    Heep AEngelskirchen RHolschneider AGroneck P: Primary intervention for posthemorrhagic hydrocephalus in very low birthweight infants by ventriculostomy. Childs Nerv Syst 17:47512001

  • 30

    Horinek DCihar MTichy M: Current methods in the treatment of posthemorrhagic hydrocephalus in infants. Bratisl Lek Listy (Tlacene Vyd) 104:3473512003

  • 31

    Hudgins RJBoydston WRGilreath CL: Treatment of posthemorrhagic hydrocephalus in the preterm infant with a ventricular access device. Pediatr Neurosurg 29:3093131998

  • 32

    Hudgins RJBoydston WRHudgins PAMorris RAdler SMGilreath CL: Intrathecal urokinase as a treatment for intraventricular hemorrhage in the preterm infant. Pediatr Neurosurg 26:2812871997

  • 33

    Inagaki TKawaguchi TYamahara TKitamura NRyu TKinoshita Y: Management of intraventricular hemorrhage in preterm infants with low birth weight. Acta Neurochir Suppl 113:1731752012

  • 34

    International randomised controlled trial of acetazolamide and furosemide in posthaemorrhagic ventricular dilatation in infancy: Lancet 352:4334401998

  • 35

    James HE: Spectrum of the syndrome of the isolated fourth ventricle in posthemorrhagic hydrocephalus of the premature infant. Pediatr Neurosurg 16:3053081991

  • 36

    Kazan SGüra AUcar TKorkmaz EOngun HAkyuz M: Hydrocephalus after intraventricular hemorrhage in preterm and low-birth weight infants: analysis of associated risk factors for ventriculoperitoneal shunting. Surg Neurol 64:Suppl 2S77S812005

  • 37

    Kennedy CRAyers SCampbell MJElbourne DHope PJohnson A: Randomized, controlled trial of acetazolamide and furosemide in posthemorrhagic ventricular dilation in infancy: follow-up at 1 year. Pediatrics 108:5976072001

  • 38

    Korinth MCWeinzierl MRGilsbach JM: Experience with a new concept to lower non-infectious complications in infants with programmable shunts. Eur J Pediatr Surg 13:81862003

  • 39

    Kormanik KPraca JGarton HJSarkar S: Repeated tapping of ventricular reservoir in preterm infants with post-hemorrhagic ventricular dilatation does not increase the risk of reservoir infection. J Perinatol 30:2182212010

  • 40

    Kreusser KLTarby TJTaylor DKovnar EHill AConry JA: Rapidly progressive posthemorrhagic hydrocephalus. Treatment with external ventricular drainage. Am J Dis Child 138:6336371984

  • 41

    Lam HPHeilman CB: Ventricular access device versus ventriculosubgaleal shunt in post hemorrhagic hydrocephalus associated with prematurity. J Matern Fetal Neonatal Med 22:109711012009

  • 42

    Limbrick DD JrBaird LCKlimo P JrRiva-Cambrin JFlannery AM: Pediatric hydrocephalus: systematic literature review and evidence-based guidelines. Part 4: Cerebrospinal fluid shunt or endoscopic third ventriculostomy for the treatment of hydrocephalus in children. J Neurosurg Pediatr 14:30342014

  • 43

    Limbrick DD JrMathur AJohnston JMMunro RSagar JInder T: Neurosurgical treatment of progressive posthemorrhagic ventricular dilation in preterm infants: a 10-year single-institution study. Clinical article. J Neurosurg Pediatr 6:2242302010

  • 44

    Lipina RReguli SDolezilová VKuncíková MPodesvová H: Endoscopic third ventriculostomy for obstructive hydrocephalus in children younger than 6 months of age: is it a firstchoice method?. Childs Nerv Syst 24:102110272008

  • 45

    Luciano RTortorolo LChiaretti APiastra MVelardi FPolidori G: Intraventricular streptokinase infusion in acute post-haemorrhagic hydrocephalus. Intensive Care Med 24:5265291998

  • 46

    Luciano RVelardi FRomagnoli CPapacci PDe Stefano VTortorolo G: Failure of fibrinolytic endoventricular treatment to prevent neonatal post-haemorrhagic hydrocephalus. A case-control trial. Childs Nerv Syst 13:73761997

  • 47

    Martin JAHamilton BESutton PDVentura SJMathews TJOsterman MJ: Births: final data for 2008. Natl Vital Stat Rep 59:1712010

  • 48

    Martínez-Lage JFAlmagro MJDel Rincón ISPérez-Espejo MAPiqueras CAlfaro R: Management of neonatal hydrocephalus: feasibility of use and safety of two programmable (Sophy and Polaris) valves. Childs Nerv Syst 24:5495562008

  • 49

    Mathews TJMacDorman MF: Infant mortality statistics from the 2007 period linked birth/infant death data set. Natl Vital Stat Rep 59:1302011

  • 50

    McCullough DC: A critical evaluation of continuous intracranial pressure monitoring in pediatric hydrocephalus. Childs Brain 6:2252411980

  • 51

    Ment LRDuncan CCEhrenkranz RAKleinman CSTaylor KJScott DT: Randomized low-dose indomethacin trial for prevention of intraventricular hemorrhage in very low birth weight neonates. J Pediatr 112:9489551988

  • 52

    Miranda P: Intraventricular hemorrhage and posthemorrhagic hydrocephalus in the preterm infant. Minerva Pediatr 62:79892010

  • 53

    Morimoto KHayakawa TYoshimine TWakayama AKuroda R: Two-step procedure for early neonatal surgery of fetal hydrocephalus. Neurol Med Chir (Tokyo) 33:1581651993

  • 54

    Müller WUrlesberger BMaurer UKuttnig-Haim MReiterer FMoradi G: Serial lumbar tapping to prevent posthaemorrhagic hydrocephalus after intracranial haemorrhage in preterm infants. Wien Klin Wochenschr 110:6316341998

  • 55

    Paraicz E: Successful treatment of perinatal intraventricular haemorrhage. Acta Paediatr Acad Sci Hung 20:2112141979

  • 56

    Peretta PRagazzi PCarlino CFGaglini PCinalli G: The role of Ommaya reservoir and endoscopic third ventriculostomy in the management of post-hemorrhagic hydrocephalus of prematurity. Childs Nerv Syst 23:7657712007

  • 57

    Perlman JMLynch BVolpe JJ: Late hydrocephalus after arrest and resolution of neonatal post-hemorrhagic hydrocephalus. Dev Med Child Neurol 32:7257291990

  • 58

    Pople IKGriffith HB: Control of hydrocephalus by endoscopic choroid plexus coagulation—long-term results and complications. Eur J Pediatr Surg 3:Suppl 117181993

  • 59

    Rahman NMurshid WRJamjoom ZAJamjoom A: Neurosurgical management of intraventricular haemorrhage in preterm infants. J Pak Med Assoc 43:1952001993

  • 60

    Rhodes TTEdwards WHSaunders RLHarbaugh RELittle CLMorgan LJ: External ventricular drainage for initial treatment of neonatal posthemorrhagic hydrocephalus: surgical and neurodevelopmental outcome. Pediatr Neurosci 13:2552621987

  • 61

    Richard ECinalli GAssis DPierre-Kahn ALacaze-Masmonteil T: Treatment of post-haemorrhage ventricular dilatation with an Ommaya's reservoir: management and outcome of 64 preterm infants. Childs Nerv Syst 17:3343402001

  • 62

    Robinson S: Neonatal posthemorrhagic hydrocephalus from prematurity: pathophysiology and current treatment concepts. A review. J Neurosurg Pediatr 9:2422582012

  • 63

    Sasidharan PMarquez EDizon ESridhar CV: Developmental outcome of infants with severe intracranial-intraventricular hemorrhage and hydrocephalus with and without ventriculoperitoneal shunt. Childs Nerv Syst 2:1491521986

  • 64

    Scavarda DBednarek NLitre FKoch CLena GMorville P: Acquired aqueductal stenosis in preterm infants: an indication for neuroendoscopic third ventriculostomy. Childs Nerv Syst 19:7567592003

  • 65

    Siomin VCinalli GGrotenhuis AGolash AOi SKothbauer K: Endoscopic third ventriculostomy in patients with cerebrospinal fluid infection and/or hemorrhage. J Neurosurg 97:5195242002

  • 66

    Tubbs RSBanks JTSoleau SSmyth MDWellons JC IIIBlount JP: Complications of ventriculosubgaleal shunts in infants and children. Childs Nerv Syst 21:48512005

  • 67

    Tubbs RSSmyth MDWellons JC IIIBlount JPGrabb PAOakes WJ: Alternative uses for the subgaleal shunt in pediatric neurosurgery. Pediatr Neurosurg 39:22242003

  • 68

    Warf BCCampbell JWRiddle 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 FIESTA MRI imaging. Childs Nerv Syst 27:106310712011

  • 69

    Weninger MSalzer HRPollak ARosenkranz MVorkapic PKorn A: External ventricular drainage for treatment of rapidly progressive posthemorrhagic hydrocephalus. Neurosurgery 31:52581992

  • 70

    Whitelaw A: Repeated lumbar or ventricular punctures in newborns with intraventricular hemorrhage. Cochrane Database Syst Rev 1CD0002162001

  • 71

    Whitelaw AEvans DCarter MThoresen MWroblewska JMandera M: Randomized clinical trial of prevention of hydrocephalus after intraventricular hemorrhage in preterm infants: brain-washing versus tapping fluid. Pediatrics 119:e1071e10782007

  • 72

    Whitelaw AJary SKmita GWroblewska JMusialik-Swietlinska EMandera M: Randomized trial of drainage, irrigation and fibrinolytic therapy for premature infants with posthemorrhagic ventricular dilatation: developmental outcome at 2 years. Pediatrics 125:e852e8582010

  • 73

    Whitelaw AKennedy CRBrion LP: Diuretic therapy for newborn infants with posthemorrhagic ventricular dilatation. Cochrane Database Syst Rev 2CD0022702001

  • 74

    Whitelaw AOdd DE: Intraventricular streptokinase after intraventricular hemorrhage in newborn infants. Cochrane Database Syst Rev 4CD0004982007

  • 75

    Whitelaw APople ICherian SEvans DThoresen M: Phase 1 trial of prevention of hydrocephalus after intraventricular hemorrhage in newborn infants by drainage, irrigation, and fibrinolytic therapy. Pediatrics 111:7597652003

  • 76

    Whitelaw ARivers RPCreighton LGaffney P: Low dose intraventricular fibrinolytic treatment to prevent posthaemorrhagic hydrocephalus. Arch Dis Child 67:12141992

  • 77

    Whitelaw ASaliba EFellman VMowinckel MCAcolet DMarlow N: Phase I study of intraventricular recombinant tissue plasminogen activator for treatment of posthaemorrhagic hydrocephalus. Arch Dis Child Fetal Neonatal Ed 75:F20F261996

  • 78

    Willis BJavalkar VVannemreddy PCaldito GMatsuyama JGuthikonda B: Ventricular reservoirs and ventriculoperitoneal shunts for premature infants with posthemorrhagic hydrocephalus: an institutional experience. Clinical article. J Neurosurg Pediatr 3:941002009

  • 79

    Yapicioğlu HNarli NSatar MSoyupak SAltunbaşak S: Intraventricular streptokinase for the treatment of posthaemorrhagic hydrocephalus of preterm. J Clin Neurosci 10:2972992003

  • 80

    Yu BLi SLin ZZhang N: Treatment of posthemorrhagic hydrocephalus in premature infants with subcutaneous reservoir drainage. Pediatr Neurosurg 45:1191252009

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Article Information

Address correspondence to: Ann Marie Flannery, M.D., Department of Neurological Surgery, Saint Louis University, 3565 Vista Ave., St. Louis, MO 63110. email: flanneam@slu.edu.

Please include this information when citing this paper: DOI: 10.3171/2014.7.PEDS14322.

© AANS, except where prohibited by US copyright law.

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    Flowchart showing the process involved in identifying relevant literature. The criteria for “records excluded” and “fulltext articles excluded with reasons” are detailed in Part 1 of the Guidelines.

References

1

Adams-Chapman IHansen NIStoll BJHiggins R: Neurodevelopmental outcome of extremely low birth weight infants with posthemorrhagic hydrocephalus requiring shunt insertion. Pediatrics 121:e1167e11772008

2

Albright ALHHaines SJTaylor FH: Function of parietal and frontal shunts in childhood hydrocephalus. J Neurosurg 69:8838861988

3

Anwar MDoyle AJKadam SHiatt IMHegyi T: Management of posthemorrhagic hydrocephalus in the preterm infant. J Pediatr Surg 21:3343371986

4

Anwar MKadam SHiatt IMHegyi T: Serial lumbar punctures in prevention of post-hemorrhagic hydrocephalus in preterm infants. J Pediatr 107:4464501985

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Bada HSSalmon JHPearson DH: Early surgical intervention in posthemorrhagic hydrocephalus. Childs Brain 5:1091151979

6

Behjati SEmami-Naeini PNejat FEl Khashab M: Incidence of hydrocephalus and the need to ventriculoperitoneal shunting in premature infants with intraventricular hemorrhage: risk factors and outcome. Childs Nerv Syst 27:9859892011

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Benzel ECReeves JDKesterson LHadden TA: Slit ventricle syndrome in children: clinical presentation and treatment. Acta Neurochir (Wien) 117:7141992

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Benzel ECReeves JPNguyen PKHadden TA: The treatment of hydrocephalus in preterm infants with intraventricular haemorrhage. Acta Neurochir (Wien) 122:2002031993

9

Berger AWeninger MReinprecht AHaschke NKohlhauser CPollak A: Long-term experience with subcutaneously tunneled external ventricular drainage in preterm infants. Childs Nerv Syst 16:1031102000

10

Boynton BRBoynton CAMerritt TAVaucher YEJames HEBejar RF: Ventriculoperitoneal shunts in low birth weight infants with intracranial hemorrhage: neurodevelopmental outcome. Neurosurgery 18:1411451986

11

Brouwer AJGroenendaal Fvan den Hoogen AVerboon-Maciolek MHanlo PRademaker KJ: Incidence of infections of ventricular reservoirs in the treatment of post-haemorrhagic ventricular dilatation: a retrospective study (1992–2003). Arch Dis Child Fetal Neonatal Ed 92:F41F432007

12

Bruinsma NStobberingh EEHerpers MJVles JSWeber BJGavilanes DA: Subcutaneous ventricular catheter reservoir and ventriculoperitoneal drain-related infections in preterm infants and young children. Clin Microbiol Infect 6:2022062000

13

Burstein JPapile LABurstein R: Intraventricular hemorrhage and hydrocephalus in premature newborns: a prospective study with CT. AJR Am J Roentgenol 132:6316351979

14

Chaparro MJPritz MBYonemura KS: Broviac ventriculostomy for long-term external ventricular drainage. Pediatr Neurosurg 17:2082121992

15

Chaplin ERGoldstein GWMyerberg DZHunt JVTooley WH: Posthemorrhagic hydrocephalus in the preterm infant. Pediatrics 65:9019091980

16

Choudhury AR: Infantile hydrocephalus: management using CT assessment. Childs Nerv Syst 11:2202261995

17

Cornips EVan Calenbergh FPlets CDevlieger HCasaer P: Use of external drainage for posthemorrhagic hydrocephalus in very low birth weight premature infants. Childs Nerv Syst 13:3693741997

18

de Vries LSLiem KDvan Dijk KSmit BJSie LRademaker KJ: Early versus late treatment of posthaemorrhagic ventricular dilatation: results of a retrospective study from five neonatal intensive care units in The Netherlands. Acta Paediatr 91:2122172002

19

Dykes FDDunbar BLazarra AAhmann PA: Posthemorrhagic hydrocephalus in high-risk preterm infants: natural history, management, and long-term outcome. J Pediatr 114:6116181989

20

Elgamal EAEl-Dawlatly AAMurshid WREl-Watidy SMJamjoom ZA: Endoscopic third ventriculostomy for hydrocephalus in children younger than 1 year of age. Childs Nerv Syst 27:1111162011

21

Felderhoff-Mueser UBuhrer CGroneck PObladen MBartmann PHeep A: Soluble Fas (CD95/Apo-1), soluble Fas ligand, and activated caspase 3 in the cerebrospinal fluid of infants with posthemorrhagic and nonhemorrhagic hydrocephalus. Pediatr Res 54:6596642003

22

Fernell EHagberg GHagberg B: Infantile hydrocephalus in preterm, low-birth-weight infants—a nationwide Swedish cohort study 1979–1988. Acta Paediatr 82:45481993

23

Flannery AMMitchell L: Pediatric hydrocephalus: systematic literature review and evidence-based guidelines. Part 1: Introduction and methodology. J Neurosurg Pediatr 14:372014

24

Fulkerson DHSivaganesan AHill JDEdwards JRShoja MMBoaz JC: Progression of cerebrospinal fluid cell count and differential over a treatment course of shunt infection. Clinical article. J Neurosurg Pediatr 8:6136192011

25

Gaskill SJMarlin AERivera S: The subcutaneous ventricular reservoir: an effective treatment for posthemorrhagic hydrocephalus. Childs Nerv Syst 4:2912951988

26

Gurtner PBass TGudeman SKPenix JOPhilput CBSchinco FP: Surgical management of posthemorrhagic hydrocephalus in 22 low-birth-weight infants. Childs Nerv Syst 8:1982021992

27

Haines SJLapointe M: Fibrinolytic agents in the management of posthemorrhagic hydrocephalus in preterm infants: the evidence. Childs Nerv Syst 15:2262341999

28

Harbaugh RESaunders RLEdwards WH: External ventricular drainage for control of posthemorrhagic hydrocephalus in premature infants. J Neurosurg 55:7667701981

29

Heep AEngelskirchen RHolschneider AGroneck P: Primary intervention for posthemorrhagic hydrocephalus in very low birthweight infants by ventriculostomy. Childs Nerv Syst 17:47512001

30

Horinek DCihar MTichy M: Current methods in the treatment of posthemorrhagic hydrocephalus in infants. Bratisl Lek Listy (Tlacene Vyd) 104:3473512003

31

Hudgins RJBoydston WRGilreath CL: Treatment of posthemorrhagic hydrocephalus in the preterm infant with a ventricular access device. Pediatr Neurosurg 29:3093131998

32

Hudgins RJBoydston WRHudgins PAMorris RAdler SMGilreath CL: Intrathecal urokinase as a treatment for intraventricular hemorrhage in the preterm infant. Pediatr Neurosurg 26:2812871997

33

Inagaki TKawaguchi TYamahara TKitamura NRyu TKinoshita Y: Management of intraventricular hemorrhage in preterm infants with low birth weight. Acta Neurochir Suppl 113:1731752012

34

International randomised controlled trial of acetazolamide and furosemide in posthaemorrhagic ventricular dilatation in infancy: Lancet 352:4334401998

35

James HE: Spectrum of the syndrome of the isolated fourth ventricle in posthemorrhagic hydrocephalus of the premature infant. Pediatr Neurosurg 16:3053081991

36

Kazan SGüra AUcar TKorkmaz EOngun HAkyuz M: Hydrocephalus after intraventricular hemorrhage in preterm and low-birth weight infants: analysis of associated risk factors for ventriculoperitoneal shunting. Surg Neurol 64:Suppl 2S77S812005

37

Kennedy CRAyers SCampbell MJElbourne DHope PJohnson A: Randomized, controlled trial of acetazolamide and furosemide in posthemorrhagic ventricular dilation in infancy: follow-up at 1 year. Pediatrics 108:5976072001

38

Korinth MCWeinzierl MRGilsbach JM: Experience with a new concept to lower non-infectious complications in infants with programmable shunts. Eur J Pediatr Surg 13:81862003

39

Kormanik KPraca JGarton HJSarkar S: Repeated tapping of ventricular reservoir in preterm infants with post-hemorrhagic ventricular dilatation does not increase the risk of reservoir infection. J Perinatol 30:2182212010

40

Kreusser KLTarby TJTaylor DKovnar EHill AConry JA: Rapidly progressive posthemorrhagic hydrocephalus. Treatment with external ventricular drainage. Am J Dis Child 138:6336371984

41

Lam HPHeilman CB: Ventricular access device versus ventriculosubgaleal shunt in post hemorrhagic hydrocephalus associated with prematurity. J Matern Fetal Neonatal Med 22:109711012009

42

Limbrick DD JrBaird LCKlimo P JrRiva-Cambrin JFlannery AM: Pediatric hydrocephalus: systematic literature review and evidence-based guidelines. Part 4: Cerebrospinal fluid shunt or endoscopic third ventriculostomy for the treatment of hydrocephalus in children. J Neurosurg Pediatr 14:30342014

43

Limbrick DD JrMathur AJohnston JMMunro RSagar JInder T: Neurosurgical treatment of progressive posthemorrhagic ventricular dilation in preterm infants: a 10-year single-institution study. Clinical article. J Neurosurg Pediatr 6:2242302010

44

Lipina RReguli SDolezilová VKuncíková MPodesvová H: Endoscopic third ventriculostomy for obstructive hydrocephalus in children younger than 6 months of age: is it a firstchoice method?. Childs Nerv Syst 24:102110272008

45

Luciano RTortorolo LChiaretti APiastra MVelardi FPolidori G: Intraventricular streptokinase infusion in acute post-haemorrhagic hydrocephalus. Intensive Care Med 24:5265291998

46

Luciano RVelardi FRomagnoli CPapacci PDe Stefano VTortorolo G: Failure of fibrinolytic endoventricular treatment to prevent neonatal post-haemorrhagic hydrocephalus. A case-control trial. Childs Nerv Syst 13:73761997

47

Martin JAHamilton BESutton PDVentura SJMathews TJOsterman MJ: Births: final data for 2008. Natl Vital Stat Rep 59:1712010

48

Martínez-Lage JFAlmagro MJDel Rincón ISPérez-Espejo MAPiqueras CAlfaro R: Management of neonatal hydrocephalus: feasibility of use and safety of two programmable (Sophy and Polaris) valves. Childs Nerv Syst 24:5495562008

49

Mathews TJMacDorman MF: Infant mortality statistics from the 2007 period linked birth/infant death data set. Natl Vital Stat Rep 59:1302011

50

McCullough DC: A critical evaluation of continuous intracranial pressure monitoring in pediatric hydrocephalus. Childs Brain 6:2252411980

51

Ment LRDuncan CCEhrenkranz RAKleinman CSTaylor KJScott DT: Randomized low-dose indomethacin trial for prevention of intraventricular hemorrhage in very low birth weight neonates. J Pediatr 112:9489551988

52

Miranda P: Intraventricular hemorrhage and posthemorrhagic hydrocephalus in the preterm infant. Minerva Pediatr 62:79892010

53

Morimoto KHayakawa TYoshimine TWakayama AKuroda R: Two-step procedure for early neonatal surgery of fetal hydrocephalus. Neurol Med Chir (Tokyo) 33:1581651993

54

Müller WUrlesberger BMaurer UKuttnig-Haim MReiterer FMoradi G: Serial lumbar tapping to prevent posthaemorrhagic hydrocephalus after intracranial haemorrhage in preterm infants. Wien Klin Wochenschr 110:6316341998

55

Paraicz E: Successful treatment of perinatal intraventricular haemorrhage. Acta Paediatr Acad Sci Hung 20:2112141979

56

Peretta PRagazzi PCarlino CFGaglini PCinalli G: The role of Ommaya reservoir and endoscopic third ventriculostomy in the management of post-hemorrhagic hydrocephalus of prematurity. Childs Nerv Syst 23:7657712007

57

Perlman JMLynch BVolpe JJ: Late hydrocephalus after arrest and resolution of neonatal post-hemorrhagic hydrocephalus. Dev Med Child Neurol 32:7257291990

58

Pople IKGriffith HB: Control of hydrocephalus by endoscopic choroid plexus coagulation—long-term results and complications. Eur J Pediatr Surg 3:Suppl 117181993

59

Rahman NMurshid WRJamjoom ZAJamjoom A: Neurosurgical management of intraventricular haemorrhage in preterm infants. J Pak Med Assoc 43:1952001993

60

Rhodes TTEdwards WHSaunders RLHarbaugh RELittle CLMorgan LJ: External ventricular drainage for initial treatment of neonatal posthemorrhagic hydrocephalus: surgical and neurodevelopmental outcome. Pediatr Neurosci 13:2552621987

61

Richard ECinalli GAssis DPierre-Kahn ALacaze-Masmonteil T: Treatment of post-haemorrhage ventricular dilatation with an Ommaya's reservoir: management and outcome of 64 preterm infants. Childs Nerv Syst 17:3343402001

62

Robinson S: Neonatal posthemorrhagic hydrocephalus from prematurity: pathophysiology and current treatment concepts. A review. J Neurosurg Pediatr 9:2422582012

63

Sasidharan PMarquez EDizon ESridhar CV: Developmental outcome of infants with severe intracranial-intraventricular hemorrhage and hydrocephalus with and without ventriculoperitoneal shunt. Childs Nerv Syst 2:1491521986

64

Scavarda DBednarek NLitre FKoch CLena GMorville P: Acquired aqueductal stenosis in preterm infants: an indication for neuroendoscopic third ventriculostomy. Childs Nerv Syst 19:7567592003

65

Siomin VCinalli GGrotenhuis AGolash AOi SKothbauer K: Endoscopic third ventriculostomy in patients with cerebrospinal fluid infection and/or hemorrhage. J Neurosurg 97:5195242002

66

Tubbs RSBanks JTSoleau SSmyth MDWellons JC IIIBlount JP: Complications of ventriculosubgaleal shunts in infants and children. Childs Nerv Syst 21:48512005

67

Tubbs RSSmyth MDWellons JC IIIBlount JPGrabb PAOakes WJ: Alternative uses for the subgaleal shunt in pediatric neurosurgery. Pediatr Neurosurg 39:22242003

68

Warf BCCampbell JWRiddle 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 FIESTA MRI imaging. Childs Nerv Syst 27:106310712011

69

Weninger MSalzer HRPollak ARosenkranz MVorkapic PKorn A: External ventricular drainage for treatment of rapidly progressive posthemorrhagic hydrocephalus. Neurosurgery 31:52581992

70

Whitelaw A: Repeated lumbar or ventricular punctures in newborns with intraventricular hemorrhage. Cochrane Database Syst Rev 1CD0002162001

71

Whitelaw AEvans DCarter MThoresen MWroblewska JMandera M: Randomized clinical trial of prevention of hydrocephalus after intraventricular hemorrhage in preterm infants: brain-washing versus tapping fluid. Pediatrics 119:e1071e10782007

72

Whitelaw AJary SKmita GWroblewska JMusialik-Swietlinska EMandera M: Randomized trial of drainage, irrigation and fibrinolytic therapy for premature infants with posthemorrhagic ventricular dilatation: developmental outcome at 2 years. Pediatrics 125:e852e8582010

73

Whitelaw AKennedy CRBrion LP: Diuretic therapy for newborn infants with posthemorrhagic ventricular dilatation. Cochrane Database Syst Rev 2CD0022702001

74

Whitelaw AOdd DE: Intraventricular streptokinase after intraventricular hemorrhage in newborn infants. Cochrane Database Syst Rev 4CD0004982007

75

Whitelaw APople ICherian SEvans DThoresen M: Phase 1 trial of prevention of hydrocephalus after intraventricular hemorrhage in newborn infants by drainage, irrigation, and fibrinolytic therapy. Pediatrics 111:7597652003

76

Whitelaw ARivers RPCreighton LGaffney P: Low dose intraventricular fibrinolytic treatment to prevent posthaemorrhagic hydrocephalus. Arch Dis Child 67:12141992

77

Whitelaw ASaliba EFellman VMowinckel MCAcolet DMarlow N: Phase I study of intraventricular recombinant tissue plasminogen activator for treatment of posthaemorrhagic hydrocephalus. Arch Dis Child Fetal Neonatal Ed 75:F20F261996

78

Willis BJavalkar VVannemreddy PCaldito GMatsuyama JGuthikonda B: Ventricular reservoirs and ventriculoperitoneal shunts for premature infants with posthemorrhagic hydrocephalus: an institutional experience. Clinical article. J Neurosurg Pediatr 3:941002009

79

Yapicioğlu HNarli NSatar MSoyupak SAltunbaşak S: Intraventricular streptokinase for the treatment of posthaemorrhagic hydrocephalus of preterm. J Clin Neurosci 10:2972992003

80

Yu BLi SLin ZZhang N: Treatment of posthemorrhagic hydrocephalus in premature infants with subcutaneous reservoir drainage. Pediatr Neurosurg 45:1191252009

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