Introduction

Hydrocephalus in early infancy can be secondary to a wide range of pathologies such as intraventricular haemorrhage [1,2,3,4,5,6,7,8,9], myelomeningocele [8, 10,11,12,13,14], aqueductal stenosis [15,16,17], intracranial cysts [18, 19] and meningitis [8]. In patients who require permanent cerebrospinal fluid (CSF) diversion, a ventriculoperitoneal (VP) shunt is usually the first-line procedure. However, shunt failure is high when inserted during the neonatal period and early infancy. Shunt dysfunction may be due to infection, blockage and overdrainage [20,21,22,23,24].

The anterior fontanelle closes at 12–24 months of age [25, 26], and there is variation in age at which an infant learns to crawl and walk [27, 28]. It is likely that non-ambulatory infants with open fontanelles represent CSF shunt physiology which is unique. The effect of different shunt valve systems on this unique neonatal CSF physiology has not been determined.

CSF drainage can be restricted by implanting either a differential pressure or flow-regulated valve. A differential pressure valve opens when the positive pressure gradient between the ventricle and peritoneum exceeds the mechanical resistance exerted by the valve. The minimum pressure needed to open the valve can be increased or decreased with the use of adjustable settings, such as in the Miethke ProGav system. Flow-regulated valves do not have an adjustable component; they are designed to maintain a constant rate of CSF drainage throughout physiological pressure changes occurring within the ventricles and peritoneum.

We sought to establish whether there is a difference in the function of a flow-regulated valve such as an Orbis-Sigma (OSV) or a differential pressure valve, such as the Miethke ProGav in neonatal hydrocephalus.

Methodology

A retrospective case series of primary shunt procedures during or immediately following the neonatal period, from August 2011 to February 2018 at Sheffield Children’s Hospital was carried out. The neonatal period was defined as the first 4 weeks of life in full-term babies. In premature babies, the inclusion criteria was extended to 3 months. Fifty-five patients were included in the study. Thirty-four had an adjustable valve (Miethke ProGav), and twenty-one had a flow-regulated valve (Orbis-Sigma) inserted. The distal catheter was placed into the peritoneum in all patients.

Clinical overdrainage was defined as the presence of one or more of the following; sunken fontanelle, overriding sutures and decreasing head circumference. In isolation, irritability and vomiting were not attributed to overdrainage; however, when associated with other signs of overdrainage, they were considered to indicate severe deterioration. Radiological signs of overdrainage included subdural collections, overriding or fused cranial sutures and collapsed ventricles.

The female to male ratio was 1:1.75. The gestational ages at birth were full term (> 37 weeks) in 38%, moderately premature (28–37 weeks) in 46% and extremely premature (< 28 weeks) in 16%. The most common causes of hydrocephalus were intraventricular haemorrhage (44%, 24/55), myelomeningocele (31%, 17/55) and aqueductal stenosis (7%, 4/55) (Table 1).

Table 1 Aetiology of hydrocephalus
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The corrected gestational age at the time of primary shunt insertion varied, ranging from 35 weeks + 6 days to 47 weeks (Table 2). The median duration from birth to primary shunt insertion was 46 days (range 3–133 days) in patients with adjustable valves and 51 days (range 4–111) in those with flow-regulated valves (Table 2).

Table 2 Patient demographics at primary shunt insertion
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The primary outcome was 1 year shunt survival. Overdrainage and shunt infections were assessed as secondary outcomes. Overdrainage was defined clinically, by the presence of sunken fontanelle, decreasing head circumference or overriding skull vault sutures. Shunt infection was defined as clinical shunt infection with a confirmed causative organism grown from the CSF or shunt tip culture. Fifty-three patients had adequate 1 year follow-up. The median duration of follow-up was 4.2 years. Statistical analysis was done using Graphpad Prism 7, and Fisher’s exact test was performed.

Results

For those with adequate follow-up, the overall 30-day and 1-year rates of shunt survival were 77% (41/53) and 34% (18/53), respectively. The 1-year shunt survival was 28% (9/32) for the adjustable valve group and 42% (9/21) for the flow-regulated valve group (p = 0.18) (Fig. 1).

Fig. 1
figure 1

One-year primary shunt survival

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The most common reasons for shunt revision were proximal blockage, distal blockage and shunt infection (Table 3). The total infection rate was 11% (6/53). Organisms grown included S. aureus (3/6, 50%), Coagulase Negative Staphylococcus (1/6, 17%), S. Epidermidis (1/6, 17%) and Pseudomonas (1/6, 16%).

Table 3 : Indications for shunt revision within the first year
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There were two mortalities within the first year of life. One patient with a thoracic myelomeningocele died due to respiratory failure secondary to lung hypoplasia and pulmonary hypertension. Furthermore, this patient had a Chiari II malformation which potentially exacerbated their respiratory dysfunction. A foramen magnum decompression was performed; however, there may still have been brainstem dysfunction contributing to the poor respiratory function. The other patient had hydraencephaly.

Overdrainage

During the first year of the child’s life, clinical signs of overdrainage were seen in 45% (24/53) of the patients (Table 4). These clinical signs were seen in 59% (19/32) of patients primarily treated with ProGav 2 valves and 24% (5/21) of the patients treated with OSV II (p = 0.02).

Table 4 Clinical features of overdrainage
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In the Progav group, the mean initial shunt setting was 5 cmH2O (0–10). 53% (17/32) of the patients had their valve setting increased during the first year of life, and the net increase was 4 cmH2O (1–8). Valve adjustments were well tolerated except in one patient. Two patients with overdrainage had their valves changed to OSV II at ages 2 and 7 months old. One patient with a ProGav valve had a ProSA antigravity device added at 5 years old.

Five patients primarily treated with OSV II developed clinical signs of overdrainage during the first year of life; one of them had a valve change to ProGav 2.

Radiologically small ventricles were seen in 50% (16/32) and 29% (6/21) of the patients treated with ProGav and OSV valves, respectively (p = 0.25).

Two patients with ProGav valves developed scaphocephaly, and CT scans showed sagittal craniosynostosis (Fig. 2). There were no cases of craniosynostosis observed in patients treated with OSVs. The first patient’s primary valve setting was 3 cmH2O; however, by day three post op, she had developed sunken fontanelle, and at 3 months old, she had dropped centiles on her head circumference chart, and her skull vault sutures were overriding. Her valve setting was increased gradually to 10 cmH2O; nevertheless, signs of overdrainage continued to be observed, and by 12 months of age, she had developed a scaphoid head. Attempts were then made to increase the valve setting to 13 cmH2O, but this was not tolerated. The second patient’s primary valve setting was 5 cmH2O. At 3 months post op, she had developed overriding sutures and a left-sided subdural collection; therefore, the valve setting was increased to 9 cmH2O. Despite this, by 7 months old, the patient had developed sagittal craniosynostosis. Both patients have been referred to the craniofacial service and are currently being managed conservatively. However, the patients are being closely followed up in case skull vault reconstructive surgery is required in the future.

Fig. 2
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Patient two with craniosynostosis secondary to shunt overdrainage. Imaging at ages 3 months (a), 6 months (b, c) and 10 months (d) old

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Underdrainage

During the first year of life, 24% (5/21) and 28% (9/32) of patients primarily treated with OSVs and ProGavs developed pseudomeningoceles, following either primary or revision shunt surgery (p = 0.7). This was successfully managed conservatively in 11 patients via the use of head bandages and decreasing the valve settings. However, two patients with OSVs and one with a ProGav underwent further surgery due to their pseudomeningocele.

Discussion

VP shunts have a higher failure rate in the paediatric population when compared to adults [29, 30]. Reddy et al. [29] found in their study that 78% of paediatric patients (age < 17 years) required at least one shunt revision, compared to 32% of the adults. In our series, 66% of the patients had required a shunt revision within 1 year of primary insertion. Shunt failure in infants (age < 1 years old) is higher than in older children [14, 31,32,33]. In particular, neonates have been shown to have the highest rate of shunt failure [30]. Gebert et al. [31] found in patients with a mean age of 4 months at the time of shunt insertion, a 1 year shunt survival rate of 69%. Furthermore, the shunt survival was found to be lower in pre-term infants. Thomale et al. [32] found that in infants aged less than 1 year old, the overall shunt survival was 61%. We observed a higher rate of shunt failure. However, the age at primary shunt insertion in our series was young; 18% and 64% of the patients had corrected gestation ages < 37 weeks and between 37 to 42 weeks at the time of primary shunt insertion, respectively. In our series, there was no statistical difference in the 1 year shunt survival between flow-regulated and adjustable valves. Moreover, there were similar rates of confirmed infection and blockage between the two groups. However, there were complications observed only in the adjustable valve group such as catheter disconnection which lead to early revision surgery. It is unlikely that these complications were secondary to the valve technology. Given the small sample size, this may have given a false impression of inferior shunt survival.

In our series, the intraventricular haemorrhage and myelomeningoceles were the most common causes of hydrocephalus. This is in line with the literature where 57–82% of patients with myelomeningoceles repaired postnatally require a shunt [10, 11, 13]. In patients with intraventricular haemorrhage, 39–93% of those who undergo a temporizing neurosurgical procedure will require a permanent VP shunt [1,2,3,4,5,6]. The 1-year shunt survival in intraventricular haemorrhage is approximately 65–71% [2, 7]. In our series, the 1-year shunt survival observed in patients with intraventricular haemorrhage and myelomeningoceles was 30% and 33%, respectively.

Our overall shunt infection rate was 11%. Evidence has shown that the shunt infection rate in patients less than 6 months old can be up to 24% (range 11–24%) [12, 23, 24, 31, 34, 35. Younger age at the time of shunt insertion has been identified as a predictor of CSF infection [23, 36,37,38]. Inserting a VP shunt into a premature neonate was shown to be associated with a fivefold increase in the risk of shunt infection [36]. The most common causative organism in our series was Staphylococcus aureus, whereas Staphylococcus epidermidis is often the most common in other studies [37, 38]. There was no difference in the infection rate between the two valve groups in our series. We have not carried out a secondary analysis of the infections observed, for example, whether or not fontanelle taps prior to primary VP shunt insertion increased the risk of infection.

Overdrainage during infancy can lead to subdural haematoma [22], craniosynostosis [39,40,41,42] and the slit ventricle syndrome later in life [8, 9, 41,42,43,44]. Furthermore, slit ventricles are associated with an increased risk of shunt blockage and requirement for revision surgery [8]. Our clinical criteria for identifying overdrainage included signs which are not specific to overdrainage. For example, sunken fontanelle may also occur secondary to dehydration. This could have potentially lead to false positives for overdrainage. There is evidence to suggest that flow-regulated valves may be associated with fewer complications in relation to overdrainage [21, 45]. Re-adjusting the opening pressure on a valve has shown to be an effective treatment for overdrainage and avoids further operations in the adult population [46]. However, this finding may not be applicable to neonates and infants with hydrocephalus. Weinzierl et al. observed that adjusting the shunt valve settings may not prevent slit ventricles in patients whom are non-ambulatory [8]. Furthermore, an adjustable gravitational antisiphon device, the ProSA, can be implanted in addition to the ProGav valve to reduce overdrainage. Tschan et al. found that the addition of a ProSA device was associated with complete resolution of overdrainage symptoms in approximately 90% of cases in an adolescent population [47].

Babies are often lying flat. At approximately 9–12 months, children may be able to pull themselves upright and stand while holding onto furniture. They may be walking independently by 12–18 months. At this age, their CSF dynamics may be similar to that of an adult, because the gravitational effects of being vertical will commence. However, it is likely that babies with shunts in situ have different CSF flow dynamics. As the Miethke ProGav valve antisiphon device relies on a gravitational unit. This may not be activated in a baby who is predominantly horizontal, leading to overdrainage of CSF. Alternatively, we may have observed high rates of overdrainage because the valve settings we used were too low. Flow-regulated valves are thought to minimize the effects of CSF drainage which occur due to valsalva manoeuvres, such as sneezing. Given that babies can spend several hours per day crying, there may be an added valsalva effect leading to overdrainage of CSF in differential pressure valves which does not apply to flow-regulated valves.

A large proportion of patients with adjustable valves required an increase in their valve setting. The ideal starting opening pressure is unknown. In our study, the mean primary valve setting was 5 cmH2O. However during the first 12 months, 50% of the patients had their valve setting increased.

Given the high frequency of overdrainage, it could be argued that starting with a higher opening pressure would be more ideal. However, we had one case of a premature baby with intraventricular haemorrhage whose initial valve setting was 2 cmH2O. We did not observe any clinical signs of overdrainage in this patient, and his valve setting was not changed. Furthermore, we also observed a high rate of pseudomeningocele. In most cases, this was successfully treated via decreasing the valve setting and applying a tight head bandage or sock. If a neurosurgeon was to insert a primary VP shunt with an adjustable valve set high, they may avoid overdrainage; however, this may be complicated by pseudomeningocele formation. Regardless of the initial valve setting, it is more likely that the important aspect of management is to have a form of monitoring in place to guide your valve adjustments. In our practice, we use the World Health Organization Head Circumference growth charts as a form of monitoring. We have found that this method helps us to identify patients experiencing CSF overdrainage and adjust their valves accordingly. There are other ways to monitor patients post-operatively, such as serial cranial ultrasound imaging to detect a decreasing ventricular size. There was no set protocol for monitoring the head circumference, so measurements were taken opportunistically. Therefore, we do not have robust data to demonstrate whether flow-regulated valves are associated with macrocephaly secondary to underdrainage.

Unfortunately, there was one patient with overdrainage in whom we were unable to adjust their valve setting. This was attributed to the baby having a soft skull vault and therefore difficulty with applying the pressure against the free floating cranial bones needed to change the ProGav valve setting. This is not a common issue for children with adjustable valves.

Despite overdrainage being seen more frequently in patients with ProGav 2 valves, the option to adjust the setting proved invaluable in several patients. Whereas, when overdrainage occurs in a patient with an OSV, there are no further non-operative treatment options available. In our series, we had one patient with an OSV who required surgery due to overdrainage where the valve was changed to a ProGav 2.

The limitations of our study include the small sample size and retrospective data collection. Furthermore, treatment allocation was not randomized, and patients received a shunt valve type depending on the surgeons’ preference. There was no assessment of the patients’ neurological development. Therefore, we have not investigated whether overdrainage leads to any long-term cognitive impairment.

Conclusion

In our series, irrespective of which valve is used, shunt failure rates are high when inserted during or immediately following the neonatal period. Overdrainage may be less common in patients with flow-regulated valves. However, if overdrainage is observed, adjusting the setting of a differential pressure valve can effectively treat the overdrainage without the need for invasive shunt revision surgery.