Intraventricular hemorrhage (IVH) in preterm infants

Transcription

1 J Neurosurg Pediatrics 13: , 2014 AANS, 2014 Endoscopic third ventriculostomy and choroid plexus cauterization in posthemorrhagic hydrocephalus of prematurity Clinical article Parthasarathi Chamiraju, M.D., 1 Sanjiv Bhatia, M.D., 1 David I. Sandberg, M.D., 2 and John Ragheb, M.D. 1 1 Division of Pediatric Neurosurgery, University of Miami Miller School of Medicine and Miami Children s Hospital, Miami, Florida; and 2 Departments of Pediatric Surgery and Neurosurgery, University of Texas Health Science Center at Houston, Texas Object. The aim of this study was to determine the role of endoscopic third ventriculostomy and choroid plexus cauterization (ETV/CPC) in the management of posthemorrhagic hydrocephalus of prematurity (PHHP) and to analyze which factors affect patient outcomes. Methods. This study retrospectively reviewed medical records of 27 premature infants with intraventricular hemorrhage (IVH) and hydrocephalus treated with ETV and CPC from 2008 to All patients were evaluated using MRI before the procedure to verify the anatomical feasibility of ETV/CPC. Endoscopic treatment included third ventriculostomy,, and bilateral CPC. After ETV/CPC, all patients underwent follow-up for a period of 6 40 months (mean 16.2 months). The procedure was considered a failure if the patient subsequently required a shunt. The following factors were analyzed to determine a relationship to patient outcomes: gestational age at birth, corrected age and weight at surgery, timing of surgery after birth, grade of IVH, the status of the prepontine cistern and cerebral aqueduct on MRI, need for a ventricular access device prior to the endoscopic procedure, and scarring of the prepontine cistern noted at surgery. Results. Seventeen (63%) of 27 patients required a shunt after ETV/CPC, and 10 patients did not require further CSF diversion. Several factors studied were associated with a higher rate of ETV/CPC failure: Grade IV hemorrhage, weight 3 kg or less and age younger than 3 months at the time of surgery, need for reservoir placement, and presence of a normal cerebral aqueduct. Two factors were found to be statistically significant: the patient s corrected gestational age of less than 0 weeks at surgery and a narrow prepontine cistern on MRI. The majority (83%) of ETV/CPC failures occurred in the first 3 months after the procedure. None of the patients had a complication directly related to the procedure. Conclusions. Endoscopic third ventriculostomy/cpc is a safe initial procedure for hydrocephalus in premature infants with IVH and hydrocephalus, obviating the need for a shunt in selected patients. Even though the success rate is low (37%), the lower rate of complications in comparison with shunt treatment may justify this procedure in the initial management of hydrocephalus. As several of the studied factors have shown influence on the outcome, patient selection based on these observations might increase the success rate. ( Key Words posthemorrhagic hydrocephalus of prematurity endoscopic third ventriculostomy choroid plexus cauterization Intraventricular hemorrhage (IVH) in preterm infants is one of the major causes of hydrocephalus in infants in developed countries. The incidence of IVH in premature babies weighing less than 1500 g at birth is approximately 15% 20%. 9 The grading system presently used for IVH is the modified Papile grading, in Abbreviations used in this paper: CPC = choroid plexus cauterization; ETV = endoscopic third ventriculostomy; IVH = intraventricular hemorrhage; PHHP = posthemorrhagic hydrocephalus of prematurity; VP = ventriculoperitoneal. which Grade IV is termed periventricular hemorrhagic infarction. 10,17,21 Hydrocephalus due to IVH is attributed to impaired CSF flow and impaired absorption due to inflammation obstructing the cerebral aqueduct, fibrosis of the arachnoid granulations, and meningeal and subependymal fibrosis. 6 Thus, hydrocephalus in these patients can be considered communicating, noncommunicating, or a combination thereof. The incidence of hydrocephalus in patients with IVH of prematurity is reported to be approximately 25% 30%. 7 A multicenter trial in this patient population 433

2 P. Chamiraju et al. showed no hydrocephalus in 50% of patients, 25% developed nonprogressive ventriculomegaly, and the remaining 25% had symptomatic hydrocephalus. 16 In a 10-year single-institution study, 29% of infants with severe IVH (Grades III and IV) developed symptomatic hydrocephalus requiring surgical intervention; 21% required permanent shunt insertion. 15 Ventriculoperitoneal (VP) shunt placement is the standard treatment for symptomatic PHHP after temporizing measures have enabled the patient to reach sufficient weight for definitive CSF diversion. Many studies have shown that the complication rate of ventriculoperitoneal shunts in the PHHP population is higher than that in patients with hydrocephalus from other etiologies. 1,3 The success rate of ETV/CPC in children younger than 2 years varies from less than 50% to as high as 80% depending on the etiology of hydrocephalus. 1,4,13 In a large cohort of Ugandan children with postinfectious hydrocephalus, Warf found that adding CPC to ETV increased the success rate from 47% to 66%. 23 In the existing literature, the success rate of ETV/CPC for the PHHP population is reported to be 10% 44%. 13,26 The ETV/CPC procedure has been most extensively studied in the postinfectious hydrocephalus population; the published literature of this procedure in PHHP is limited. The importance of prepontine cistern scarring as a strong independent predictor of ETV success was reported by Warf and Kulkarni in 403 African patients with hydrocephalus. 27 In a small series of patients with PHHP, Warf et al. found that the success of the endoscopic procedure was relatively low if the prepontine cistern was narrow or scarred. 26 We add to the limited published literature on this population by reviewing this series of premature infants with PHHP who required CSF diversion and were treated with ETV/CPC and. We assessed a variety of factors to determine their relationship to the success rate of this procedure. Methods After obtaining approval from the Western Institutional Review Board, we retrospectively reviewed the medical records of all patients with PHHP who were consulted by the pediatric neurosurgery department for hydrocephalus intervention. Sixty-six patient interventions were performed during a period of 4 years ( ). Fifty patients were initially managed by placing a ventricular access device (cerebral reservoir) with serial CSF tappings. Among these 50 patients, 19 patients did not require any further interventions as their hydrocephalus improved or resolved. Of the remaining 31 patients who required further treatment for hydrocephalus, 16 patients underwent shunt placement and 15 patients underwent ETV/CPC. Among 16 patients who did not require temporary diversion, 4 patients underwent shunt treatment and 12 patients underwent ETV/CPC. Thus, of the 27 patients undergoing ETV/CPC, 15 had a prior ventricular access and 12 did not. This study was conducted to assess various clinical and radiological factors and measure the outcomes in patients with PHHP who underwent ETV/ CPC during the 4-year period. An ETV/CPC procedure was considered in these patients once their weight had reached at least 2 kg and they were medically fit for the procedure. In 15 patients hydrocephalus was initially managed by a ventricular access device (reservoir), and in the remaining patients ETV/CPC was performed as the initial procedure. All patients were evaluated with MRI of the brain before the procedure to verify the anatomical feasibility of the ETV/CPC procedure. Imaging was performed mainly to look for interthalamic adhesions and the position of the basilar artery in the prepontine space and also to plan the entry point over the scalp. Sagittal T2-weighted MR images were used to define the prepontine space. This space is divided arbitrarily into a narrow or a normal space based on the distance between the dorsum sellae and basilar artery. The amount of scarring in the prepontine space was not assessed in this study. Cerebrospinal fluid flow through the aqueduct was analyzed by phase-contrast MRI sequences. Patients with large interthalamic adhesions were not considered for this procedure. Endoscopic treatment included third ventriculostomy,, and bilateral CPC. After ETV/ CPC, patients underwent follow-up for a period of 6 40 months (mean 16.2 months). The procedure was considered a failure if the patient subsequently required a shunt. The following factors were analyzed to determine a possible relationship to patient outcomes: gestational age at birth, corrected age and weight at surgery, timing of surgery after birth, grade of IVH, status of the prepontine cistern and cerebral aqueduct on MRI, need for a ventricular access device prior to the endoscopic procedure, and scarring of the prepontine cistern noted at surgery. Table 1 shows the patient demographics and the patient outcomes. All of these parameters were statistically analyzed to find a potential relationship to the surgical outcome as shown in Table 2. Surgical Technique and Follow-Up After anesthesia induction and intubation, the patient was positioned supine with the head on a padded horseshoe headrest and the neck was flexed The procedure at our institution is performed with a rigid neuroendoscope (Aesculap, Medtronic disposable, or Gaab). The skin incision was made at the lateral aspect of the fontanel, approximately cm from midline in the midpupillary line. When the septum was intact, the incision was made another 10 mm lateral to the typical incision for ETV to enable a trajectory not only to perform ETV but also to perform and contralateral CPC. A small amount of frontal and parietal bone was removed using Kerrison rongeurs to provide a generous window to maneuver the endoscope. The dura mater was opened in a small horseshoe-shaped flap toward the midline. There was no difficulty in visualization of the intraventricular anatomy using the endoscope even though the ependymal surface on almost all patients was stained with old blood products. The floor of the third ventricle was also thicker in most patients with scarring, as anticipated. The blunt-tipped probe was used to fenestrate the floor of the third ventricle at the thinnest point posterior to the dorsum sellae and anterior to the basilar artery. The 434

3 ETV and CPC in posthemorrhagic hydrocephalus of prematurity TABLE 1: Demographic details of the patients and their outcomes Case No. Gestational Age at Birth* Actual Age at Op* Total Age (corrected age) at Op* Weight (kg) Hemorrhage Grade Reservoir Procedure Performed Prepontine Cistern Cerebral Aqueductal Stenosis Prepontine Cistern Scarring Outcome (+7) 3 IV yes ETV/CPC narrow no no failure (0) 3 III no ETV/CPC + normal yes no failure (+1) 4.1 III yes ETV/CPC narrow no yes failure (+3) 3.5 IV yes ETV only normal yes no failure (+34) 6.4 III no ETV/CPC normal yes no success (+16) 4.3 III no ETV only normal yes yes success (+8) 3.5 III no ETV/CPC normal yes no success (+7) 3.4 IV yes ETV/CPC + normal yes yes failure (+1) 3.1 IV yes ETV/CPC + normal yes no success (+1) 3.9 III no ETV/CPC + normal yes no success ( 1) 2.3 IV yes ETV + narrow no yes failure ( 1) 2.8 III yes ETV/CPC normal no no failure (+3) 5.2 IV yes ETV/CPC + normal yes no success (+30) 8 III no ETV/CPC normal no no failure (+2) 2.9 IV yes ETV/CPC + normal no no success (+9) 3.7 III no ETV/CPC + normal no no failure (0) 3.2 IV no ETV/CPC narrow yes yes failure (+13) 7 III no ETV/CPC normal yes no success (+28) 8 III no ETV/CPC normal no no success (+14) 6 IV no ETV/CPC normal no no failure ( 2) 2.2 IV yes ETV/CPC + narrow no no failure ( 1) 3.5 IV yes ETV/CPC + narrow no yes failure (+1) 3.2 IV yes ETV/CPC narrow yes no failure ( 4) 2.2 IV no ETV/CPC + narrow yes no failure (+14) 6 IV yes ETV/CPC narrow no yes failure (+5) 3 III yes ETV/CPC + normal no no success (+4) 2.7 III yes ETV/CPC + narrow yes yes failure * Ages are reported as the number of weeks. Ages are as follows: gestational age is the time from conception to birth; actual age is the actual patient age after birth at surgery; total gestational age is the gestational age + age from birth; corrected age is the total age 38 (38 weeks was considered as the normal gestational age). NeuroBalloon (Integra LifeSciences) was used to enlarge the fenestration made. Great care was taken to ensure that the membrane of Liliequist was generously perforated, and notation was made of scarring in the prepontine cistern. Next, the ipsilateral choroid plexus was cauterized starting at the foramen of Monro to the temporal horn. All visualized choroid plexus was cauterized generously from the foramen of Monro to the temporal horn. Finally, a was performed, and the choroid plexus on the contralateral side was coagulated from the foramen 435

4 P. Chamiraju et al. TABLE 2: Statistical analysis of the parameters studied Parameter No. of Patients No. of Successes No. of Failures p Value gestational age at birth wks >28 wks corrected age at op wks >0 wks weight at op kg >3 kg grade of hemorrhage 0.12 III IV reservoir placement yes no prepontine cistern narrow normal aqueductal stenosis present absent prepontine cistern scarring yes no timing of op after birth (mos) > of Monro to the temporal horn. The endoscope was then returned to the ipsilateral frontal horn and removed. A small piece of Gelfoam was inserted to plug the cortical opening, and then the dura was closed in a watertight fashion with interrupted sutures before skin closure. A new ventricular reservoir with a closed subgaleal egress port was placed according to surgeon s preference. Postoperatively all infants were observed closely by monitoring the anterior fontanel, daily head circumference measurements, and ultrasound or quick brain MRI scans (limited T2 sequences) as needed. The procedure was deemed a failure in patients with progressive macrocephaly crossing percentile lines, progressive fullness of the fontanel, and/or progressive hydrocephalus postoperatively; these patients were offered shunt procedures. Statistical Analysis Statistical software (SPSS, version 19, IBM) was used to organize, validate, and analyze the collected data. Indicators of central tendency and dispersion were estimated for quantitative variables while frequencies and percentages were used for qualitative variables. The chi-square test or Fisher s exact test was used to identify associations between categorical variables. Logistic regression was selected to explore the predictive power of different variables. A level of statistical significance of 0.05 was selected for all variables. Multivariate logistic analysis was performed when the other variables were adjusted. Results Twenty-seven patients underwent ETV/CPC for PHHP from 2008 to Sixteen patients were born before 28 weeks of gestation and 11 were born between 29 and 34 weeks. Grade III hemorrhage was noted in 13 patients and Grade IV hemorrhage in 14 patients. Fifteen patients required temporary relief of hydrocephalus by ventricular reservoir placement and serial tapping. In 12 patients, a temporizing measure was not deemed to be necessary and ETV/CPC was performed without prior reservoir placement. The corrected age of the patients at the time of endoscopic procedure ranged from -4 to +34 weeks with a mean of +7 weeks (zero being considered a normal gestational age of 38 weeks). Weight ranged from 2.2 to 8 kg with mean of 4.0 kg at the time of procedure. On MRI scans, 10 patients were found to have a narrow prepontine cistern and 17 patients had a normal cistern. The definition of a narrow prepontine cistern was based on the neurosurgeon s assessment of this space on T2-weighted sagittal MRI rather than specific measurements. Stenosis of the cerebral aqueduct was observed in 14 of 27 patients. Among the factors analyzed, corrected age at surgery more than 0 weeks (p = 0.026) and normal prepontine cistern on MRI (p = 0.003) were found to have a significant influence on the outcome (Table 2). Among 27 patients, 7 underwent ETV/CPC at or before 38 weeks of total age (that is, gestational age + age from birth), and all subsequently required a shunt. In patients older than 38 weeks of total age at surgery, a shunt was avoided in 50% of patients (10 of 20). In patients with a normal prepontine cistern on MRI, the success rate was 56% (10 of 17). The procedure failed in all 10 patients who had a narrow prepontine cistern, and these children required shunts. On multivariate logistic regression analysis, none of the studied factors were found to be significant. Reservoir placement was considered in patients who were not fit for anesthesia or those who weighed less than 2 kg or if there were significant blood products still visible on preoperative imaging studies. Patients who developed delayed hydrocephalus with no retained blood products on imaging underwent ETV/CPC without reservoir placement. The success rate was greater in patients who did not require reservoir placement (50%) prior to the endoscopic procedure than in patients who required a reservoir (26%), although this did not reach statistical significance (p = 0.257). Septostomy was performed in 13 patients to access the choroid plexus on the other side, and 8 of these patients subsequently required a shunt. In 14 patients the septum pellucidum was deficient, and only ETV/CPC was performed; 9 of these patients subsequently required a shunt. In 3 patients, only an ETV was 436

5 ETV and CPC in posthemorrhagic hydrocephalus of prematurity performed without CPC as the amount of choroid plexus in the lateral ventricles was minimal and was closely adherent to thalamostriate veins. Among these 3 patients, 2 patients subsequently required a shunt procedure because hydrocephalus progressed after ETV. Many of the studied factors have shown a trend toward better outcomes even though they were not found to be statistically significant. The success of ETV/CPC was higher (50%) when the procedure was performed 3 months after birth compared with patients who underwent surgery at or before 3 months after birth (18.2%). Similar outcomes were noted when the patient weighed more than 3 kg (47% success) compared with patients who weighed 3 kg or less (20% success). Patients with Grade III hemorrhage had higher success rates (53.8%) than patients with Grade IV hemorrhage (21.4%). Patients who required reservoir placement did poorly with 26.7% success compared with 50% success for those who did not require prior reservoir placement. When the prepontine cistern was normal at surgery, a higher success rate was noted (47.4%) compared with patients who had a scarred cistern (12.5%). All infants underwent follow-up for a period of 6 40 months (mean 16.2 months). Among the procedures in 27 patients, 10 (37%) were deemed successful because further CSF diversion was not required for the duration of follow-up. Endoscopic management failed in 17 patients (63%) and these patients required shunt placement at a mean of 7.9 weeks after the endoscopic procedure. The majority of these failures occurred within 3 months (82%) after surgery. Two of these 17 patients experienced failure at 4 months and 1 experienced failure at the end of 5 months but within 6 months postoperatively. Discussion In the US and other developed countries, hydrocephalus associated with IVH of prematurity is a common indication for CSF diversion. Ventriculoperitoneal shunting is the most common definitive treatment for hydrocephalus in this population after temporizing measures have been performed. Alternatives to shunting are desirable to avoid the complications of shunting. Long-term failure of VP shunt treatment occurs in 50% of patients in the initial 2 years after shunt placement and in up to 80% in the 12-year follow-up. 8,19 Endoscopic third ventriculostomy is an increasingly used alternative to shunt placement in selected patients. Adding CPC to ETV may increase the success of ETV in selected patients, especially in those with postinfectious hydrocephalus. 23 Endoscopic third ventriculostomy and CPC have shown promising results in hydrocephalus due to pathologies other than PHHP. Even though the success rates are not high in the literature, there is a bias toward utilizing ETV for hydrocephalus in patients younger than 2 years to avoid a shunt. 11,12 In a large published series of Ugandan patients, the morbidity and mortality for ETV/CPC for postinfectious hydrocephalus was less than 1%. 23 The rate of infection was 9% in the VP shunt group compared with less than 1% in ETV group published by the same author. 22 An infection rate of 5% 13% for VP shunt treatment for hydrocephalus has been reported recently from a multiinstitutional study. 28 The present study is the largest series in the published English-language literature assessing the outcome of ETV/CPC in patients with PHHP. We analyzed the clinical and radiological factors that might have influenced the outcome. As mentioned by Warf et al. in their 10 patients with PHHP treated by ETV/CPC, the status of the prepontine cistern on MRI appears to correlate well with the scarring intraoperatively. If this cistern was scarred, the outcome of the procedure was poor. 26 Adding CPC to reduce the production of CSF may potentially increase the success of ETV in patients with scarring of the prepontine cistern. In our study, of 10 patients in whom the prepontine cistern was narrow, none had a successful endoscopic procedure. The ETV/CPC procedure was successful in 10 of 17 patients who had a normal prepontine cistern (p = 0.003). The greater success in patients who underwent surgery at 38 weeks of corrected age may be due to maturation of the absorptive surface for the CSF as the patient grows and gains weight. Even though there was no statistical significance in several studied factors due to the relatively small sample size, some demonstrated a trend toward better outcomes. Contrary to the findings of Warf et al. 26 in their series of 10 patients with PHHP, the outcomes in our series were better in patients with associated aqueductal stenosis (50% success rate [7 of 14]). Only 3 (23%) of 13 patients improved when hydrocephalus was not associated with aqueductal stenosis (p = 0.236). We hypothesize that in patients with PHHP when the obstruction is at the level of the aqueduct, ETV/CPC carries better results. In patients with a normal aqueduct, there may be an obstruction beyond the aqueduct, with diffuse scarring and poor absorption of CSF by the arachnoid villi. The lower success rate in patients who had prior reservoir placement may be due to younger age or a greater quantity of blood products predisposing to scarring. The intraoperative finding of scarring in the prepontine cistern correlated with the MRI finding of a narrow cistern in 8 of 10 patients. Among 8 patients with a scarred cistern, only 1 patient avoided a shunt despite the endoscopic procedure. The procedure failed in 17 of the 27 patients in less than 6 months, with 82% of failures occurring before 3 months postoperatively. It is well known that VP shunt failure continues over time compared with failure of ETV/CPC, which typically occurs in the first few months. Early failure is considered safe in infants with an open fontanel, where an acute increase in intracranial pressure is unlikely to cause clinical herniation. 5,20,26 The effects of failed ETV/CPC on long-term cognitive and developmental outcomes are unknown. Long-term neurocognitive outcome of premature babies with IVH and hydrocephalus is often poor. 23 Adding a shunt to this problem may be detrimental in patients who develop complications from shunt procedures. 14,18 Similar to postinfectious hydrocephalus, the success of ETV/CPC in the PHHP population is significantly less than when this procedure is performed for hydrocephalus of other etiologies. The outcome is similar to that in patients with postinfectious hydrocephalus where the obstruction is 437

6 P. Chamiraju et al. also due to inflammation, scarring, and loculation. 2,24 The ventricle size after ETV/CPC remains large compared with ventricle size in shunt-treated patients in whom the ventricular system often becomes small. Some patients end up having slit ventricles. 27 In postinfectious hydrocephalus, shunt failure in patients who had a shunt placed after a failed endoscopic procedure was low compared with failure in patients who were treated primarily by a shunt. 25 The same might pertain to patients with PHHP who had shunts after ETV/CPC failure as the scarring of the subarachnoid spaces in these patients is similar to that seen in cases of postinfectious hydrocephalus. There is a good possibility in these patients that the continuous irrigation used while performing the endoscopic procedure helped to clear the old blood products, thereby at least partially reducing the ongoing scarring. We believe that, even though the success rate is low (37%), the complication rate is much lower than that associated with shunt treatment. In the current series, there were no CSF leaks, hemorrhages, wound complications, new neurological deficits, or any other recognized complication other than failure of the procedure. Even if the procedure fails and a shunt is required, will likely eliminate the need for bilateral shunts, which were historically necessary in some patients prior to the era of endoscopic management. Considering clinical and radiological factors preoperatively may predict which patients are likely to avoid further CSF diversion after ETV/CPC, but a larger population of patients will be needed to study such factors. As endoscopic techniques are not performed aggressively in PHHP patients in many centers, pooling data from various centers or comparing ETV/CPC with shunt procedures in a randomized controlled fashion is advised. Conclusions The ETV/CPC procedure is a reasonable treatment option to avoid shunt treatment in some patients with PHHP. Selecting patients depending on various factors might increase the success rate of this procedure. Older gestational age and a normal prepontine cistern on preoperative MRI are the most favorable factors for this procedure. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Chamiraju, Bhatia. Acquisition of data: Chamiraju. Analysis and interpretation of data: Chamiraju, Sandberg. Drafting the article: Chamiraju, Bhatia, Sandberg. 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: Chamiraju. Study supervision: Bhatia, Ragheb. References 1. 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