- Email: [email protected]
Long-Term Outcomes in Ventriculoatrial Shunt Surgery in Patients with Pediatric Hydrocephalus: Retrospective Single-Center Study
Journal Pre-proof Long-Term Outcomes in Ventriculoatrial Shunt Surgery in Patients with Pediatric Hydrocephalus: A Retrospective Single-Center Study Matthias Gmeiner, Helga Wagner, Willem J.R. van Ouwerkerk, Gracija Sardi, Wolfgang Thomae, Wolfgang Senker, Kurt Holl, Andreas Gruber PII:
S1878-8750(20)30300-4
DOI:
https://doi.org/10.1016/j.wneu.2020.02.035
Reference:
WNEU 14310
To appear in:
World Neurosurgery
Received Date: 28 November 2019 Revised Date:
4 February 2020
Accepted Date: 5 February 2020
Please cite this article as: Gmeiner M, Wagner H, van Ouwerkerk WJR, Sardi G, Thomae W, Senker W, Holl K, Gruber A, Long-Term Outcomes in Ventriculoatrial Shunt Surgery in Patients with Pediatric Hydrocephalus: A Retrospective Single-Center Study, World Neurosurgery (2020), doi: https:// doi.org/10.1016/j.wneu.2020.02.035. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.
Long-Term Outcomes in Ventriculoatrial Shunt Surgery in Patients with Pediatric Hydrocephalus: A Retrospective Single-Center Study
Matthias Gmeinera,b*, Helga Wagnerc, Willem J.R. van Ouwerkerkd, Gracija Sardia, Wolfgang Thomaea, Wolfgang Senkera, Kurt Holla, Andreas Grubera,b
a
Kepler University Hospital, Neuromed Campus, Department of Neurosurgery, Wagner-
Jauregg-Weg 15A, 4020 Linz, Austria b
Johannes Kepler University (JKU) Linz, Altenbergerstraße 69, 4040 Linz, Austria
c
Department of Applied Statistics, Johannes Kepler University Linz, 4040 Linz, Austria
d
Vrije Universitet University Medical Centre Amsterdam, Department of Neurosurgery,
Amsterdam & Princess Maxima Center for Pediatric Oncology, Utrecht, The Netherlands
*Corresponding author: Matthias Gmeiner Department of Neurosurgery, Kepler University Hospital, Wagner-Jauregg-Weg 15A, 4020 Linz, Austria Tel: +41-50-5546228453 Fax: +41-50-5546225904 Email: [email protected] Short title: VA shunt in pediatric neurosurgery
Keywords: Hydrocephalus; Long-term outcome; Shunt nephritis; Thromboembolic complications; Ventriculoatrial shunt
Abbreviations and Acronyms:APC, Abdominal pseudocysts; CSF, Cerebrospinal fluid shunting; EVD, External ventricular drainage; VA, Ventriculoatrial; VAS, VA shunt; VP, Ventriculoperitoneal
Abstract Objective: Long-term outcomes are rarely reported for patients with pediatric hydrocephalus. Ventriculoperitoneal shunting is the surgical standard; nevertheless, in selected patients, a ventriculoatrial shunt (VAS) remains an important alternative. This study aimed to analyze the causes of VAS revisions and complications. Methods: Pediatric patients who underwent their first shunt operation between 1982 and 1992 were included. The timing, cause, and modality of VAS revisions were retrospectively determined. Results. Overall, 138 patients were treated for hydrocephalus and 61 patients received a VAS during the follow-up period. A primary VAS was the first shunt type in 42 (68.85%) patients. In 19 (31.15%) patients, conversions to second-line VAS were carried out. The rate of VAS revisions performed for dysfunction or elective lengthening of a short atrial catheter was 52.2% and 22.9%, respectively. There was no difference in the number of VAS revisions between patients with primary VASs and second-line VASs. Age at VAS and etiology of hydrocephalus had no effect on the number of revisions. Specific VAS complications were observed in two patients. Deep positioning of the distal catheter led to asymptomatic tricuspid regurgitation that was reversible after shortening of the atrial catheter. Another patient presented with shunt nephritis and completely recovered after the atrial catheter was replaced with a peritoneal catheter. Conclusions. VAS remains an appropriate second-line alternative in selected patients. Specific VAS complications were rarely observed and completely reversible after treatment. However, regular and specific follow-up examinations are strongly recommended to avoid cardiopulmonary or renal complications.
Introduction After the introduction of the first modern shunt valves in the 1950s, cerebrospinal fluid shunting (CSF) has remained the surgical standard in the treatment of congenital hydrocephalus (1-3). Ventriculoatrial (VA) CSF diversions initially dominated, and ventriculoperitoneal (VP) shunting is currently regarded as the primary procedure for the surgical treatment of pediatric hydrocephalus (3-5). Studies investigating long-term outcomes in the 1960s to 1990s revealed similar shunt revision (6), durability (7), and infection (6, 8) rates for both shunt types. However, more severe complications, such as arrhythmias, thromboembolic complications, pulmonary hypertension, and shunt nephritis (3, 6, 7, 9-12), are encountered in VA shunts (VASs). Recently, long-term studies (13, 14) have reported a revision rate of >80% for pediatric VP shunts. Importantly, shunt failures are treated with multiple shunt revisions in >50% of patients (13). Further surgical treatment becomes a challenge in these patients (15). Along with specific abdominal complications (9, 15, 16), including peritoneal scarring/adhesions, abdominal pseudocysts (APC), intraperitoneal infections, and ascites, the peritoneal cavity may become unsuitable for further CSF diversion (15), thereby requiring alternative distal catheter placements. In selected patients, a VAS remains an important alternative. Therefore, studies focusing on long-term outcomes of VASs, such as the current study, are highly desired. Our study aimed to retrospectively analyze the specific causes of VAS revisions and complications in patients with pediatric hydrocephalus. We included patients who underwent their first shunt operation between 1982 and 1992 to achieve a long-term follow-up of at least 20 years. Patients who received primary VASs were compared to those who had second-line CSF diversions (conversion from another shunt type to VAS).
Materials and Methods This study was approved by the local ethics committee (Ethikkommission des Landes Oberösterreich EK-Nr.: K-25-12), and the requirement for acquisition of informed consent from patients was waived owing to the retrospective nature of the research. Patients with hydrocephalus who received their first shunt procedure (VAS, VP shunt, or external ventricular drainage [EVD]) during an 11-year period at the Children’s Hospital in Linz, Austria (January 1982 to December 1992) were retrospectively analyzed (16, 17). Follow-up data were collected and evaluated between 2013 and 2018. The number, date, and causes of shunt operations were examined using medical records and surgical reports. Data on patient characteristics (etiology of hydrocephalus, sex, type of the first surgical procedure for hydrocephalus, valve type for VAS, and age at the first surgical procedure) were obtained. Age at the first VAS (either primary VAS or conversion from another CSF diversion to a second-line VAS during follow-up) during our follow-up was additionally recorded. For final analyses, only patients who received a VAS (primary VAS or second-line VAS) during the follow-up were included. In order to focus on surgical long-term outcomes, patients who died before the age of 5 years were excluded. VAS revisions were further subdivided into the following groups based on the reason for surgery: shunt dysfunction (obstruction, underdrainage, and overdrainage), elective lengthening of the atrial catheter, shunt discontinuity (fracture or disconnection), deep positioning of the atrial catheter, shunt infection, or shunt nephritis. Shunt infection was a clinical diagnosis of infection with or without positive culture leading to either shunt revision or patient death (18). Statistical analysis included descriptive statistics for the etiology of hydrocephalus, patient characteristics, shunt operations, and revisions. Kaplan-Meier estimates and log-rank tests
were used to analyze the time to the first VAS revision. The impact of the first surgical procedure on the number of overall shunt operations (including all VA and VP shunt operations or EVDs) or only VAS operations was analyzed using the Kruskal-Wallis test. Poisson regression analysis of the overall number of operations and number of VAS revisions was performed with the following covariates: age at the first surgical procedure, age at the first VAS, and etiology of hydrocephalus. All statistical analyses were performed using R software version 3.3.1.2 (19), and statistical significance level was set at p<0.05.
Results Patient characteristics Over an 11-year period, 138 patients underwent primary surgery due to pediatric hydrocephalus. One patient who moved abroad at the age of 2 years was lost to follow-up and excluded from further analysis. The first surgical procedure was a VAS, VP shunt, and EVD in 53, 46, and 37 patients, respectively. A Rickham reservoir was implanted in only one patient. The first definitive shunt type was a VP shunt in 68 patients and a VAS in 64 patients. An EVD was only placed in five patients, and these patients died before they could receive a definitive shunt type. During the follow-up period, 80 patients received a VAS. In order to focus on surgical longterm outcomes, patients who died before the age of 5 years (n=19) were excluded from the final analysis. Therefore, a total of 61 patients with a VAS were included in this study. The median length of follow-up was 25.7 years (range, 21.4–35.6 years) in surviving patients. As presented in Table 1, the etiologies of hydrocephalus were meningomyelocele (15 patients), intraventricular hemorrhage (14 patients), postinfectious (11 patients), aqueductal stenosis (eight patients), posterior fossa cyst (six patients), congenital (three patients), and others (four patients). Further shunt and patient characteristics are summarized in Table 1.
Overall shunt operations The VAS was the first definitive shunt type in 42 (68.85%) patients. In 19 (31.15%) patients, conversions to second-line VAS were carried out during follow-up. Reasons for conversion were VP shunt dysfunction (n=6), VP shunt infection (n=5), EVD (n=5), or others (n=3). Conversion to a VAS was performed twice in seven patients and thrice in one patient. Overall, 451 shunt-related operations were performed in 61 patients (median, 6; range, 1–25 operations per patient) (Figure 1). The median time from birth to the first surgical procedure and from birth to the first VAS (primary or second-line VAS) was 45 days (range, 0–3.2 years) and 91 days (range, 0–19.4 years), respectively (Table 1). Within the first 6 months of life, 50 (82%) patients underwent their first surgical procedure and 41 (67.2%) received their first VAS. A fixed differential pressure valve was used in 42 patients (Hakim, n=21; SpitzHolter, n=13; Pudenz-Heyer, n=8), whereas a flow-regulated shunt valve (Orbis-Sigma) was used in 16 patients. Detailed shunt valve aspects are further summarized in Table 2. Shunt valve type was not associated with age at VAS (log-rank test, p=0.0859) and had no effect on the time to the first VAS revision (log-rank test, p=0.0801). Significantly more total shunt operations were performed in patients with a primary VP shunt (median, 10; range, 2–25 operations per patient) or EVD (median, 8; range, 3–10 operations per patient) than in patients with a primary VAS (median, 5; range, 1–16 operations per patient; Kruskal-Wallis test, p=0.04109). The first surgical procedure did not have any impact on the number of later VAS revisions (Kruskal-Wallis test, p=0.8862). Furthermore, there was no difference in the time to the first VAS revision between patients with primary VASs and second-line VASs (primary VP shunt or EVD) (log-rank test, p=0.8; Figure 2). Poisson regression analysis of the total number of operations and number of VAS revisions revealed that age at the first surgical procedure (p=0.0052) had a significant negative effect
on the total number of operations (i.e., increased age was associated with a lower number of operations); in contrast, a diagnosis of intraventricular hemorrhage (p=0.0002) had a significant positive effect on the total number of operations (i.e., it was associated with a higher number of operations). Neither age at the first surgical procedure (p=0.9518), age at the first VAS (p=0.4311), nor the etiology of hydrocephalus had a significant effect on the number of VAS revisions. The last definitive shunt type was a VP shunt in 38 (62.3%) patients or a VAS in 15 (24.6%) patients. Eight patients (13.1%) were independent of a prosthetic shunt system: the shunt was successfully explanted in six patients and an additional third ventriculostomy was performed in two patients. Seven patients died during the follow-up (median age, 14 years; range, 5.1– 24.2 years).
Causes of VAS revisions and specific complications In total, 157 operations were performed to revise a VAS in 59 (96.7%) patients (median, 2; range, 1–9 operations per patient) (Figure 3A). The causes of VAS revisions are illustrated in Figure 3B. Eighty-two operations (52.2%) were performed for VAS dysfunctions. Shunt components revised or replaced for VAS dysfunction are summarized in Table 3. For proximal dysfunction, replacement of only the ventricular catheter was performed in 37 (23.6%) revisions. Thirty-six (22.9%) operations were performed for asymptomatic elective lengthening of a short atrial catheter, either with placement of a new atrial catheter (n=19) or conversion to a peritoneal catheter (n=17). Nineteen operations (12.1%) were performed for shunt infections. Ten operations (6.4%) were needed for discontinuity. In three patients (1.9%), arrhythmias occurred perioperatively and required revision as the atrial catheter had been placed too deeply. In one patient, a deep positioning of the atrial catheter led to asymptomatic tricuspid
regurgitation 2 years after the shunt operation and this was reversible after shortening of the atrial catheter. One patient presented with shunt nephritis 3.75 years after VAS placement. This patient completely recovered after the atrial catheter was replaced with a peritoneal catheter. Further, an additional five unclassified operations were performed.
Discussion After the introduction of the Spitz-Holter valve, VAS became the standard CSF diversion in the 1950s–1960s (3). The introduction of silicone catheters significantly improved the VP shunting method. Further, due to the ease of placement of the peritoneal catheter, together with less severe specific complications, VP shunting finally became the preferred surgical treatment option (3, 7, 20). During the 1970s–1990s, several studies were performed to compare the clinical or surgical outcomes of VA and VP shunts (3, 4, 6-8, 21-23). However, there are only a few studies reporting on long-term outcomes after VA shunting with an average follow-up of more than 10 years (4, 5, 7, 8, 24). In patients with pediatric hydrocephalus, survival rates have significantly improved over time (17). Studies on the surgical long-term outcomes after VA-CSF diversions are highly warranted. Therefore, in this retrospective study, we chose a minimum follow-up of 20 years. Recently, Rymarczuk et al. have shown that VAS may be an appropriate second-line treatment alternative if the peritoneum becomes unsuitable for further CSF diversion (20) as a result of specific abdominal complications (16) or multiple VP shunt revisions (15). In this study, we demonstrated that the overall number of shunt operations was expectedly and significantly increased in patients with second-line VASs, because of shunt revisions performed before conversion to a VAS. However, there was no difference in the total number of VAS operations or the time to the first VAS revision between patients with primary VASs and second-line VASs.
These results clearly indicate that second-line VASs, although having undergone complicated or multiple prior shunt revisions, have nonetheless the same risk of surgical VAS revisions as primary VASs. Regarding the number of shunt revisions, previously challenging cases may therefore be converted to “standard-risk” cases with a second-line VAS strategy. We also analyzed specific causes of VAS revisions. Previously, it has been reported that up to 66% of revisions are performed for elective lengthening of the atrial catheter. Vernet et al. concluded that this high revision rate is a major disadvantage, favoring VP shunting as a primary procedure (4, 5). Conversely, in our study, only 22.9% of VAS revisions were performed for elective atrial catheter lengthening. In addition, 67.2% of patients received their VAS during the first 6 months of life and this fact might explain our rate of elective distal lengthening. Similarly, a prospective multicenter study showed that age <6 months at the first shunt treatment was independently associated with reduced shunt survival (25). Moreover, in a previous recent study, we analyzed specific causes of peritoneal catheter revisions in patients with VP shunts and reported a similar revision rate for elective lengthening of the peritoneal catheter (21.5% of peritoneal catheter revisions) (16). If the VAS is exclusively used as a second-line alternative, selected patients may be older, thereby reducing the eventual need for elective atrial catheter lengthening. Most revisions (82 operations) were performed for VAS dysfunctions. Interestingly, 37 (23.6%) revisions were necessary for proximal dysfunction involving the ventricular catheter. However, our results are in line with the study by Rymarczuk et al. who reported that 23% and 23.6% of VAS revisions were performed for elective lengthening and proximal failure, respectively (20). Stone et al. analyzed the long-term revision rate after pediatric VP shunting in 64 patients and reported a similar proximal failure rate (27%) (14). These results indicate that the long-term rate of elective distal lengthening and proximal shunt failure may be
comparable in patients with VA and VP shunts (14, 16, 20). Proximal shunt dysfunction remains the most important reason for shunt revision. Several studies have indicated that shunt-specific complications might be more severe after VA than after VP shunting. In particular, cardiopulmonary and thromboembolic complications, including pulmonary hypertension and arrhythmias, as well as shunt nephritis, have been reported (3, 6, 7, 9-12). In other studies that investigated adult patients, these cardiopulmonary complications were not observed (26, 27). However, Lundar et al. reported cardiopulmonary complications that occurred >10 years after atrial shunting (28). These complications are dependent on the length of follow-up and may be predominately seen in adult patients with pediatric hydrocephalus. In a large series, it was demonstrated that 8% of patients with VASs developed pulmonary hypertension (11). In general, the median survival of patients with pulmonary hypertension is estimated to be 2.8 years (29). Thus, such complications need to be regarded as relevant. A life-long follow-up that includes echocardiography and pulmonary function tests may therefore be recommended, as previously described (11). Deep positioning of the distal catheter may lead to atrial thrombus formation and may cause arrhythmias (9). We did not observe any thromboembolic complications and only one patient with a clinically asymptomatic tricuspid regurgitation that was completely reversible after shortening of the atrial catheter was seen. Four revisions were necessary for deep positioning of the atrial catheter. However, these revisions could have been avoided with improved techniques using intraoperative fluoroscopy or ultrasound and transesophageal echocardiography (27, 30). Shunt nephritis presents as a severe secondary renal disease associated with proteinuria, possibly leading to end-stage renal disease and death (9) with an overall incidence ranging from 0.7%–2.3% (9, 31). It is associated with chronic infection and may be difficult to diagnose. Thus, its diagnosis can be delayed by an average of 1.5 years after initial clinical
manifestation (31, 32). The prognosis may be favorable if the infected shunt is removed and the patient is treated with antibiotics. In this study, 19 VAS revisions (12.1%) were necessary for shunt infections. Only one patient (1.6%) presented with shunt nephritis, and the patient recovered completely after atrial catheter removal. However, distal catheter-specific complications can even occur in patients with VP shunts. Bowel perforation is a rare but serious complication after VP shunting, with reported mortality rates up to 15% (16, 33, 34). In previous studies, we reported that 0.9% of patients presented with this specific complication (16). Moreover, another 12.5% of patients developed an APC during our long-term follow-up (16). We recently analyzed the causes of death in the same patient cohort. Notably, the long-term mortality rates for VA and VP shunts were the same. Importantly, in our detailed analysis, we did not find VA (e.g. due to pulmonary hypertension, thromboembolic events or shunt nephritis) or VP (e.g. due to bowel perforation) related-deaths associated with a specific type of shunt (17). These data indicate that most VAS-specific complications are potentially serious but may be reversible with early and adequate diagnosis and treatment. A life-long follow-up for VAspecific cardiopulmonary and renal complications is strongly recommended. As in several European centers, the surgical treatment of pediatric hydrocephalus at our institution was traditionally performed by pediatric surgeons until the late 1980s. Subsequently, as pediatric neurosurgeons had become more involved, neurosurgical standards were fully adopted for the surgical treatment of pediatric hydrocephalus in the late 1990s (17). Therefore, in this patient cohort, the ratio to choose VAS as the first-line surgical treatment might be difficult to interpret retrospectively. The limitations of this study were its retrospective nature and the absence of standardized follow-up to detect specific complications in patients with VASs.
Conclusions These long-term results, supported by the results of our previous studies, indicate that the overall morbidity and mortality rates in this patient cohort may be comparable in patients treated with VA and VP shunts (16, 17). The rate of elective distal lengthening and proximal shunt failure may be comparable in patients with VA and VP shunts (14, 16, 20). Moreover, there is no difference in the total number of VAS operations or the time to the first VAS revision between patients with primary VASs and second-line VASs. In a selective group of challenging patients, a VA shunt is an adequate surgical second-line alternative to standard VP shunting. The importance of effective patient/family education and lifelong routine monitoring to avoid late shunt complications in patients treated for pediatric hydrocephalus has previously been highlighted (16, 35-38). In the case of atrial catheters, additional
specific
follow-up
examinations
are
strongly
recommended
to
avoid
cardiopulmonary (11) or renal complications.
Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Conflict of interest: The authors declare that they have no conflict of interest.
Figure Legends
Figure 1. Distribution of the overall number of shunt operations per patient
Figure 2. Kaplan-Meier estimate for the time to the first VAS revision There is no difference between patients with primary VASs and second-line VASs (primary VP shunt or EVD; log-rank test, p=0.8) VAS, ventriculoatrial shunt; VP, ventriculoperitoneal; EVD, external ventricular drainage
Figure 3. Number of VA shunt revisions per patient (A) and the causes (B) AC, atrial catheter; VA, ventriculoatrial
References 1. Aschoff A, Kremer P, Hashemi B, Kunze S. The scientific history of hydrocephalus and its treatment. Neurosurg Rev. 1999;22:67–93; discussion 4–5. 2. Reddy GK, Bollam P, Caldito G. Long-term outcomes of ventriculoperitoneal shunt surgery in patients with hydrocephalus. World Neurosurg. 2014;81:404–410. 3. Symss NP, Oi S. Is there an ideal shunt? A panoramic view of 110 years in CSF diversions and shunt systems used for the treatment of hydrocephalus: from historical events to current trends. Childs Nerv Syst. 2015;31:191–202. 4. Vernet O, Campiche R, de Tribolet N. Long-term results after ventriculoatrial shunting in children. Childs Nerv Syst. 1993;9:253–255. 5. Vernet O, Campiche R, de Tribolet N. Long-term results after ventriculo-atrial shunting in children. Childs Nerv Syst. 1995;11:176–179. 6. Ignelzi RJ, Kirsch WM. Follow-up analysis of ventriculoperitoneal and ventriculoatrial shunts for hydrocephalus. J Neurosurg. 1975;42:679–682. 7. Borgbjerg BM, Gjerris F, Albeck MJ, Hauerberg J, Borgesen SV. A comparison between ventriculo-peritoneal and ventriculo-atrial cerebrospinal fluid shunts in relation to rate of revision and durability. Acta Neurochir (Wien). 1998;140:459–464; discussion 465. 8. George R, Leibrock L, Epstein M. Long-term analysis of cerebrospinal fluid shunt infections. A 25-year experience. J Neurosurg. 1979;51:804–811. 9. Hanak BW, Bonow RH, Harris CA, Browd SR. Cerebrospinal fluid shunting complications in children. Pediatr Neurosurg. 2017;52:381–400. 10. Keucher TR, Mealey J Jr. Long-term results after ventriculoatrial and ventriculoperitoneal shunting for infantile hydrocephalus. J Neurosurg. 1979;50:179–186. 11. Kluge S, Baumann HJ, Regelsberger J, Kehler U, Gliemroth J, Koziej B, et al. Pulmonary hypertension after ventriculoatrial shunt implantation. J Neurosurg. 2010;113:1279–1283. 12. Wilkinson N, Sood S, Ham SD, Gilmer-Hill H, Fleming P, Rajpurkar M. Thrombosis associated with ventriculoatrial shunts. J Neurosurg Pediatr. 2008;2:286–291. 13. Reddy GK, Bollam P, Caldito G, Guthikonda B, Nanda A. Ventriculoperitoneal shunt surgery outcome in adult transition patients with pediatric-onset hydrocephalus. Neurosurgery. 2012;70:380–388; discussion 8–9. 14. Stone JJ, Walker CT, Jacobson M, Phillips V, Silberstein HJ. Revision rate of pediatric ventriculoperitoneal shunts after 15 years. J Neurosurg Pediatr. 2013;11:15–19. 15. Zhang J, Qu C, Wang Z, Wang C, Ding X, Pan S, et al. Improved ventriculoatrial shunt for cerebrospinal fluid diversion after multiple ventriculoperitoneal shunt failures. Surg Neurol. 2009;72 Suppl 1:S29–S33; discussion S33–34. 16. Gmeiner M, Wagner H, van Ouwerkerk WJR, Senker W, Holl K, Gruber A. Abdominal pseudocysts and peritoneal catheter revisions: surgical long-term results in pediatric hydrocephalus. World Neurosurg. 2018;111:e912–e920. 17. Gmeiner M, Wagner H, Zacherl C, Polanski P, Auer C, van Ouwerkerk WJ, et al. Long-term mortality rates in pediatric hydrocephalus-a retrospective single-center study. Childs Nerv Syst. 2017;33:101–109. 18. Vinchon M, Baroncini M, Delestret I. Adult outcome of pediatric hydrocephalus. Childs Nerv Syst. 2012;28:847–854. 19. Team RC. A language and environment for statistical computing, Vienna, Austria. http://wwwR-projectorg; 2013. 20. Rymarczuk GN, Keating RF, Coughlin DJ, Felbaum D, Myseros JS, Oluigbo C, et al. A comparison of ventriculoperitoneal and ventriculoatrial shunts in a population of 544 consecutive pediatric patients. Neurosurgery. 2019:opz387.
21. Ivan LP, Choo SH, Ventureyra EC. Complications of ventriculoatrial and ventriculoperitoneal shunts in a new children’s hospital. Can J Surg. 1980;23:566–568. 22. Mazza C, Pasqualin A, Da Pian R. Results of treatment with ventriculoatrial and ventriculoperitoneal shunt in infantile nontumoral hydrocephalus. Childs Brain. 1980;7:1–14. 23. Olsen L, Frykberg T. Complications in the treatment of hydrocephalus in children. A comparison of ventriculoatrial and ventriculoperitoneal shunts in a 20-year material. Acta Paediatr Scand. 1983;72:385–390. 24. Fernell E, von Wendt L, Serlo W, Heikkinen E, Andersson H. Ventriculoatrial or ventriculoperitoneal shunts in the treatment of hydrocephalus in children? Z Kinderchir. 1985;40 Suppl 1:12–14. 25. Riva-Cambrin J, Kestle JR, Holubkov R, Butler J, Kulkarni AV, Drake J, et al. Risk factors for shunt malfunction in pediatric hydrocephalus: a multicenter prospective cohort study. J Neurosurg Pediatr. 2016;17:382–390. 26. Al-Schameri AR, Hamed J, Baltsavias G, Winkler P, Machegger L, Richling B, et al. Ventriculoatrial shunts in adults, incidence of infection, and significant risk factors: a singlecenter experience. World Neurosurg. 2016;94:345–351. 27. McGovern RA, Kelly KM, Chan AK, Morrissey NJ, McKhann GM 2nd. Should ventriculoatrial shunting be the procedure of choice for normal-pressure hydrocephalus? J Neurosurg. 2014;120:1458–1464. 28. Lundar T, Langmoen IA, Hovind KH. Fatal cardiopulmonary complications in children treated with ventriculoatrial shunts. Childs Nerv Syst. 1991;7:215–217. 29. D'Alonzo GE, Barst RJ, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, et al. Survival in patients with primary pulmonary hypertension. Results from a national prospective registry. Ann Intern Med. 1991;115:343–349. 30. Clark DJ, Chakraborty A, Roebuck DJ, Thompson DN. Ultrasound guided placement of the distal catheter in paediatric ventriculoatrial shunts-an appraisal of efficacy and complications. Childs Nerv Syst. 2016;32:1219–1225. 31. Harland TA, Winston KR, Jovanovich AJ, Johnson RJ. Shunt nephritis: an increasingly unfamiliar diagnosis. World Neurosurg. 2018;111:346–348. 32. Babigumira M, Huang B, Werner S, Qunibi W. Delayed manifestation of shunt nephritis: a case report and review of the literature. Case Rep Nephrol. 2017;2017:1867349. 33. Sathyanarayana S, Wylen EL, Baskaya MK, Nanda A. Spontaneous bowel perforation after ventriculoperitoneal shunt surgery: case report and a review of 45 cases. Surg Neurol. 2000;54:388–396. 34. Vinchon M, Baroncini M, Laurent T, Patrick D. Bowel perforation caused by peritoneal shunt catheters: diagnosis and treatment. Neurosurgery. 2006;58:ONS76–82; discussion ONS76–82. 35. Acakpo-Satchivi L, Shannon CN, Tubbs RS, Wellons JC 3rd, Blount JP, Iskandar BJ, et al. Death in shunted hydrocephalic children: a follow-up study. Childs Nerv Syst. 2008;24:197–201. 36. Iskandar BJ, Tubbs S, Mapstone TB, Grabb PA, Bartolucci AA, Oakes WJ. Death in shunted hydrocephalic children in the 1990s. Pediatr Neurosurg. 1998;28:173–176. 37. Rekate HL, Blitz AM. Hydrocephalus in children. Handb Clin Neurol. 2016;136:1261–1273. 38. Vinchon M, Dhellemmes P. [Follow-up of adult patients treated during childhood for hydrocephalus]. Neurochirurgie. 2008;54:587–596.
Table 1. Patient and shunt characteristics in 61 patients with ventriculoatrial shunts Patient characteristics Male/female
Patients 36/25
Age at follow-up examination Median/range (years)
25.7/21.4–35.6
Etiology Meningomyelocele
15 (24.6%)
Intraventricular hemorrhage
14 (23%)
Postinfectious
11 (18%)
Aqueductal stenosis
8 (13.1%)
Posterior fossa cyst
6 (9.8%)
Congenital
3 (4.9%)
Others
4 (6.6%)
Age at the first surgical procedure Median (days)/range (years)
45/0–3.2 years
Time to the first revision Median (days)/range (days–years)
170/7 days–9.9 years
Age at the first VA shunt Median (days)/range (years)
91/0–19.4
Time to the first VA shunt revision Median (days)/range (years)
220/0–9.1
Last definitive shunt type VP
38 (62.3%)
VA
15 (24.6%)
Shunt explanation
8 (13.1%)
VA, ventriculoatrial; VP, ventriculoperitoneal
Table 2. Shunt valve aspects in patients with ventriculoatrial shunts Shunt
valve n
system Spitz-Holter
13
Age at VAS
Time to the first VAS revision
Median/range (days)
Median/range (days)
91/0–684
511.5/11–1219
Low-pressure
3
16/0–45
136/32–410
Medium-pressure
10
181/14–684
1030/11–1219
Hakim
21
45/0–1677
160/0–3318
Low-pressure
6
6.5/0–127
120.5/45–1708
Medium-pressure
15
50/2–1677
160/0–3318
Pudenz-Heyer
8
83.5/25–428
1431/66–2358
Low-pressure
4
69/38–98
784/123–1903
Medium-pressure
4
118/25–428
1541/66–2358
Orbis-Sigma
16
129/3–5089
435.5/5–1582
Others
3
4290/233–7092
457/62–852
VAS, ventriculoatrial shunt
Table 3. Revised and replaced shunt components in patients with ventriculoatrial shunt dysfunction Revised and replaced shunt components
N (%)
Ventricular catheter
37 (45.1%)
Completely new VP shunt
14 (17.1%)
Conversion to peritoneal catheter
7 (8.5%)
Shunt externalization
7 (8.5%)
Valve and atrial catheter
4 (4.9%)
Ventricular catheter and valve
3 (3.7%)
Completely new VA shunt
3 (3.7%)
Valve
3 (3.7%)
Atrial catheter
2 (2.4%)
Ventricular and atrial catheter
2 (2.4%)
VA, ventriculoatrial; VP, ventriculoperitoneal
Abbreviations and Acronyms:APC, Abdominal pseudocysts; CSF, Cerebrospinal fluid shunting; EVD, External ventricular drainage; VA, Ventriculoatrial; VAS, VA shunt; VP, Ventriculoperitoneal
Conflict of interest: The authors declare that they have no conflict of interest
Conceptualization; Data curation; Formal analysis; Funding acquisition; Investigation; Methodology; Project administration; Resources; Software; Supervision; Validation; Visualization; Roles/Writing - original draft; Writing - review & editing
S1878-8750(20)30300-4
DOI:
https://doi.org/10.1016/j.wneu.2020.02.035
Reference:
WNEU 14310
To appear in:
World Neurosurgery
Received Date: 28 November 2019 Revised Date:
4 February 2020
Accepted Date: 5 February 2020
Please cite this article as: Gmeiner M, Wagner H, van Ouwerkerk WJR, Sardi G, Thomae W, Senker W, Holl K, Gruber A, Long-Term Outcomes in Ventriculoatrial Shunt Surgery in Patients with Pediatric Hydrocephalus: A Retrospective Single-Center Study, World Neurosurgery (2020), doi: https:// doi.org/10.1016/j.wneu.2020.02.035. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Inc. All rights reserved.
Long-Term Outcomes in Ventriculoatrial Shunt Surgery in Patients with Pediatric Hydrocephalus: A Retrospective Single-Center Study
Matthias Gmeinera,b*, Helga Wagnerc, Willem J.R. van Ouwerkerkd, Gracija Sardia, Wolfgang Thomaea, Wolfgang Senkera, Kurt Holla, Andreas Grubera,b
a
Kepler University Hospital, Neuromed Campus, Department of Neurosurgery, Wagner-
Jauregg-Weg 15A, 4020 Linz, Austria b
Johannes Kepler University (JKU) Linz, Altenbergerstraße 69, 4040 Linz, Austria
c
Department of Applied Statistics, Johannes Kepler University Linz, 4040 Linz, Austria
d
Vrije Universitet University Medical Centre Amsterdam, Department of Neurosurgery,
Amsterdam & Princess Maxima Center for Pediatric Oncology, Utrecht, The Netherlands
*Corresponding author: Matthias Gmeiner Department of Neurosurgery, Kepler University Hospital, Wagner-Jauregg-Weg 15A, 4020 Linz, Austria Tel: +41-50-5546228453 Fax: +41-50-5546225904 Email: [email protected] Short title: VA shunt in pediatric neurosurgery
Keywords: Hydrocephalus; Long-term outcome; Shunt nephritis; Thromboembolic complications; Ventriculoatrial shunt
Abbreviations and Acronyms:APC, Abdominal pseudocysts; CSF, Cerebrospinal fluid shunting; EVD, External ventricular drainage; VA, Ventriculoatrial; VAS, VA shunt; VP, Ventriculoperitoneal
Abstract Objective: Long-term outcomes are rarely reported for patients with pediatric hydrocephalus. Ventriculoperitoneal shunting is the surgical standard; nevertheless, in selected patients, a ventriculoatrial shunt (VAS) remains an important alternative. This study aimed to analyze the causes of VAS revisions and complications. Methods: Pediatric patients who underwent their first shunt operation between 1982 and 1992 were included. The timing, cause, and modality of VAS revisions were retrospectively determined. Results. Overall, 138 patients were treated for hydrocephalus and 61 patients received a VAS during the follow-up period. A primary VAS was the first shunt type in 42 (68.85%) patients. In 19 (31.15%) patients, conversions to second-line VAS were carried out. The rate of VAS revisions performed for dysfunction or elective lengthening of a short atrial catheter was 52.2% and 22.9%, respectively. There was no difference in the number of VAS revisions between patients with primary VASs and second-line VASs. Age at VAS and etiology of hydrocephalus had no effect on the number of revisions. Specific VAS complications were observed in two patients. Deep positioning of the distal catheter led to asymptomatic tricuspid regurgitation that was reversible after shortening of the atrial catheter. Another patient presented with shunt nephritis and completely recovered after the atrial catheter was replaced with a peritoneal catheter. Conclusions. VAS remains an appropriate second-line alternative in selected patients. Specific VAS complications were rarely observed and completely reversible after treatment. However, regular and specific follow-up examinations are strongly recommended to avoid cardiopulmonary or renal complications.
Introduction After the introduction of the first modern shunt valves in the 1950s, cerebrospinal fluid shunting (CSF) has remained the surgical standard in the treatment of congenital hydrocephalus (1-3). Ventriculoatrial (VA) CSF diversions initially dominated, and ventriculoperitoneal (VP) shunting is currently regarded as the primary procedure for the surgical treatment of pediatric hydrocephalus (3-5). Studies investigating long-term outcomes in the 1960s to 1990s revealed similar shunt revision (6), durability (7), and infection (6, 8) rates for both shunt types. However, more severe complications, such as arrhythmias, thromboembolic complications, pulmonary hypertension, and shunt nephritis (3, 6, 7, 9-12), are encountered in VA shunts (VASs). Recently, long-term studies (13, 14) have reported a revision rate of >80% for pediatric VP shunts. Importantly, shunt failures are treated with multiple shunt revisions in >50% of patients (13). Further surgical treatment becomes a challenge in these patients (15). Along with specific abdominal complications (9, 15, 16), including peritoneal scarring/adhesions, abdominal pseudocysts (APC), intraperitoneal infections, and ascites, the peritoneal cavity may become unsuitable for further CSF diversion (15), thereby requiring alternative distal catheter placements. In selected patients, a VAS remains an important alternative. Therefore, studies focusing on long-term outcomes of VASs, such as the current study, are highly desired. Our study aimed to retrospectively analyze the specific causes of VAS revisions and complications in patients with pediatric hydrocephalus. We included patients who underwent their first shunt operation between 1982 and 1992 to achieve a long-term follow-up of at least 20 years. Patients who received primary VASs were compared to those who had second-line CSF diversions (conversion from another shunt type to VAS).
Materials and Methods This study was approved by the local ethics committee (Ethikkommission des Landes Oberösterreich EK-Nr.: K-25-12), and the requirement for acquisition of informed consent from patients was waived owing to the retrospective nature of the research. Patients with hydrocephalus who received their first shunt procedure (VAS, VP shunt, or external ventricular drainage [EVD]) during an 11-year period at the Children’s Hospital in Linz, Austria (January 1982 to December 1992) were retrospectively analyzed (16, 17). Follow-up data were collected and evaluated between 2013 and 2018. The number, date, and causes of shunt operations were examined using medical records and surgical reports. Data on patient characteristics (etiology of hydrocephalus, sex, type of the first surgical procedure for hydrocephalus, valve type for VAS, and age at the first surgical procedure) were obtained. Age at the first VAS (either primary VAS or conversion from another CSF diversion to a second-line VAS during follow-up) during our follow-up was additionally recorded. For final analyses, only patients who received a VAS (primary VAS or second-line VAS) during the follow-up were included. In order to focus on surgical long-term outcomes, patients who died before the age of 5 years were excluded. VAS revisions were further subdivided into the following groups based on the reason for surgery: shunt dysfunction (obstruction, underdrainage, and overdrainage), elective lengthening of the atrial catheter, shunt discontinuity (fracture or disconnection), deep positioning of the atrial catheter, shunt infection, or shunt nephritis. Shunt infection was a clinical diagnosis of infection with or without positive culture leading to either shunt revision or patient death (18). Statistical analysis included descriptive statistics for the etiology of hydrocephalus, patient characteristics, shunt operations, and revisions. Kaplan-Meier estimates and log-rank tests
were used to analyze the time to the first VAS revision. The impact of the first surgical procedure on the number of overall shunt operations (including all VA and VP shunt operations or EVDs) or only VAS operations was analyzed using the Kruskal-Wallis test. Poisson regression analysis of the overall number of operations and number of VAS revisions was performed with the following covariates: age at the first surgical procedure, age at the first VAS, and etiology of hydrocephalus. All statistical analyses were performed using R software version 3.3.1.2 (19), and statistical significance level was set at p<0.05.
Results Patient characteristics Over an 11-year period, 138 patients underwent primary surgery due to pediatric hydrocephalus. One patient who moved abroad at the age of 2 years was lost to follow-up and excluded from further analysis. The first surgical procedure was a VAS, VP shunt, and EVD in 53, 46, and 37 patients, respectively. A Rickham reservoir was implanted in only one patient. The first definitive shunt type was a VP shunt in 68 patients and a VAS in 64 patients. An EVD was only placed in five patients, and these patients died before they could receive a definitive shunt type. During the follow-up period, 80 patients received a VAS. In order to focus on surgical longterm outcomes, patients who died before the age of 5 years (n=19) were excluded from the final analysis. Therefore, a total of 61 patients with a VAS were included in this study. The median length of follow-up was 25.7 years (range, 21.4–35.6 years) in surviving patients. As presented in Table 1, the etiologies of hydrocephalus were meningomyelocele (15 patients), intraventricular hemorrhage (14 patients), postinfectious (11 patients), aqueductal stenosis (eight patients), posterior fossa cyst (six patients), congenital (three patients), and others (four patients). Further shunt and patient characteristics are summarized in Table 1.
Overall shunt operations The VAS was the first definitive shunt type in 42 (68.85%) patients. In 19 (31.15%) patients, conversions to second-line VAS were carried out during follow-up. Reasons for conversion were VP shunt dysfunction (n=6), VP shunt infection (n=5), EVD (n=5), or others (n=3). Conversion to a VAS was performed twice in seven patients and thrice in one patient. Overall, 451 shunt-related operations were performed in 61 patients (median, 6; range, 1–25 operations per patient) (Figure 1). The median time from birth to the first surgical procedure and from birth to the first VAS (primary or second-line VAS) was 45 days (range, 0–3.2 years) and 91 days (range, 0–19.4 years), respectively (Table 1). Within the first 6 months of life, 50 (82%) patients underwent their first surgical procedure and 41 (67.2%) received their first VAS. A fixed differential pressure valve was used in 42 patients (Hakim, n=21; SpitzHolter, n=13; Pudenz-Heyer, n=8), whereas a flow-regulated shunt valve (Orbis-Sigma) was used in 16 patients. Detailed shunt valve aspects are further summarized in Table 2. Shunt valve type was not associated with age at VAS (log-rank test, p=0.0859) and had no effect on the time to the first VAS revision (log-rank test, p=0.0801). Significantly more total shunt operations were performed in patients with a primary VP shunt (median, 10; range, 2–25 operations per patient) or EVD (median, 8; range, 3–10 operations per patient) than in patients with a primary VAS (median, 5; range, 1–16 operations per patient; Kruskal-Wallis test, p=0.04109). The first surgical procedure did not have any impact on the number of later VAS revisions (Kruskal-Wallis test, p=0.8862). Furthermore, there was no difference in the time to the first VAS revision between patients with primary VASs and second-line VASs (primary VP shunt or EVD) (log-rank test, p=0.8; Figure 2). Poisson regression analysis of the total number of operations and number of VAS revisions revealed that age at the first surgical procedure (p=0.0052) had a significant negative effect
on the total number of operations (i.e., increased age was associated with a lower number of operations); in contrast, a diagnosis of intraventricular hemorrhage (p=0.0002) had a significant positive effect on the total number of operations (i.e., it was associated with a higher number of operations). Neither age at the first surgical procedure (p=0.9518), age at the first VAS (p=0.4311), nor the etiology of hydrocephalus had a significant effect on the number of VAS revisions. The last definitive shunt type was a VP shunt in 38 (62.3%) patients or a VAS in 15 (24.6%) patients. Eight patients (13.1%) were independent of a prosthetic shunt system: the shunt was successfully explanted in six patients and an additional third ventriculostomy was performed in two patients. Seven patients died during the follow-up (median age, 14 years; range, 5.1– 24.2 years).
Causes of VAS revisions and specific complications In total, 157 operations were performed to revise a VAS in 59 (96.7%) patients (median, 2; range, 1–9 operations per patient) (Figure 3A). The causes of VAS revisions are illustrated in Figure 3B. Eighty-two operations (52.2%) were performed for VAS dysfunctions. Shunt components revised or replaced for VAS dysfunction are summarized in Table 3. For proximal dysfunction, replacement of only the ventricular catheter was performed in 37 (23.6%) revisions. Thirty-six (22.9%) operations were performed for asymptomatic elective lengthening of a short atrial catheter, either with placement of a new atrial catheter (n=19) or conversion to a peritoneal catheter (n=17). Nineteen operations (12.1%) were performed for shunt infections. Ten operations (6.4%) were needed for discontinuity. In three patients (1.9%), arrhythmias occurred perioperatively and required revision as the atrial catheter had been placed too deeply. In one patient, a deep positioning of the atrial catheter led to asymptomatic tricuspid
regurgitation 2 years after the shunt operation and this was reversible after shortening of the atrial catheter. One patient presented with shunt nephritis 3.75 years after VAS placement. This patient completely recovered after the atrial catheter was replaced with a peritoneal catheter. Further, an additional five unclassified operations were performed.
Discussion After the introduction of the Spitz-Holter valve, VAS became the standard CSF diversion in the 1950s–1960s (3). The introduction of silicone catheters significantly improved the VP shunting method. Further, due to the ease of placement of the peritoneal catheter, together with less severe specific complications, VP shunting finally became the preferred surgical treatment option (3, 7, 20). During the 1970s–1990s, several studies were performed to compare the clinical or surgical outcomes of VA and VP shunts (3, 4, 6-8, 21-23). However, there are only a few studies reporting on long-term outcomes after VA shunting with an average follow-up of more than 10 years (4, 5, 7, 8, 24). In patients with pediatric hydrocephalus, survival rates have significantly improved over time (17). Studies on the surgical long-term outcomes after VA-CSF diversions are highly warranted. Therefore, in this retrospective study, we chose a minimum follow-up of 20 years. Recently, Rymarczuk et al. have shown that VAS may be an appropriate second-line treatment alternative if the peritoneum becomes unsuitable for further CSF diversion (20) as a result of specific abdominal complications (16) or multiple VP shunt revisions (15). In this study, we demonstrated that the overall number of shunt operations was expectedly and significantly increased in patients with second-line VASs, because of shunt revisions performed before conversion to a VAS. However, there was no difference in the total number of VAS operations or the time to the first VAS revision between patients with primary VASs and second-line VASs.
These results clearly indicate that second-line VASs, although having undergone complicated or multiple prior shunt revisions, have nonetheless the same risk of surgical VAS revisions as primary VASs. Regarding the number of shunt revisions, previously challenging cases may therefore be converted to “standard-risk” cases with a second-line VAS strategy. We also analyzed specific causes of VAS revisions. Previously, it has been reported that up to 66% of revisions are performed for elective lengthening of the atrial catheter. Vernet et al. concluded that this high revision rate is a major disadvantage, favoring VP shunting as a primary procedure (4, 5). Conversely, in our study, only 22.9% of VAS revisions were performed for elective atrial catheter lengthening. In addition, 67.2% of patients received their VAS during the first 6 months of life and this fact might explain our rate of elective distal lengthening. Similarly, a prospective multicenter study showed that age <6 months at the first shunt treatment was independently associated with reduced shunt survival (25). Moreover, in a previous recent study, we analyzed specific causes of peritoneal catheter revisions in patients with VP shunts and reported a similar revision rate for elective lengthening of the peritoneal catheter (21.5% of peritoneal catheter revisions) (16). If the VAS is exclusively used as a second-line alternative, selected patients may be older, thereby reducing the eventual need for elective atrial catheter lengthening. Most revisions (82 operations) were performed for VAS dysfunctions. Interestingly, 37 (23.6%) revisions were necessary for proximal dysfunction involving the ventricular catheter. However, our results are in line with the study by Rymarczuk et al. who reported that 23% and 23.6% of VAS revisions were performed for elective lengthening and proximal failure, respectively (20). Stone et al. analyzed the long-term revision rate after pediatric VP shunting in 64 patients and reported a similar proximal failure rate (27%) (14). These results indicate that the long-term rate of elective distal lengthening and proximal shunt failure may be
comparable in patients with VA and VP shunts (14, 16, 20). Proximal shunt dysfunction remains the most important reason for shunt revision. Several studies have indicated that shunt-specific complications might be more severe after VA than after VP shunting. In particular, cardiopulmonary and thromboembolic complications, including pulmonary hypertension and arrhythmias, as well as shunt nephritis, have been reported (3, 6, 7, 9-12). In other studies that investigated adult patients, these cardiopulmonary complications were not observed (26, 27). However, Lundar et al. reported cardiopulmonary complications that occurred >10 years after atrial shunting (28). These complications are dependent on the length of follow-up and may be predominately seen in adult patients with pediatric hydrocephalus. In a large series, it was demonstrated that 8% of patients with VASs developed pulmonary hypertension (11). In general, the median survival of patients with pulmonary hypertension is estimated to be 2.8 years (29). Thus, such complications need to be regarded as relevant. A life-long follow-up that includes echocardiography and pulmonary function tests may therefore be recommended, as previously described (11). Deep positioning of the distal catheter may lead to atrial thrombus formation and may cause arrhythmias (9). We did not observe any thromboembolic complications and only one patient with a clinically asymptomatic tricuspid regurgitation that was completely reversible after shortening of the atrial catheter was seen. Four revisions were necessary for deep positioning of the atrial catheter. However, these revisions could have been avoided with improved techniques using intraoperative fluoroscopy or ultrasound and transesophageal echocardiography (27, 30). Shunt nephritis presents as a severe secondary renal disease associated with proteinuria, possibly leading to end-stage renal disease and death (9) with an overall incidence ranging from 0.7%–2.3% (9, 31). It is associated with chronic infection and may be difficult to diagnose. Thus, its diagnosis can be delayed by an average of 1.5 years after initial clinical
manifestation (31, 32). The prognosis may be favorable if the infected shunt is removed and the patient is treated with antibiotics. In this study, 19 VAS revisions (12.1%) were necessary for shunt infections. Only one patient (1.6%) presented with shunt nephritis, and the patient recovered completely after atrial catheter removal. However, distal catheter-specific complications can even occur in patients with VP shunts. Bowel perforation is a rare but serious complication after VP shunting, with reported mortality rates up to 15% (16, 33, 34). In previous studies, we reported that 0.9% of patients presented with this specific complication (16). Moreover, another 12.5% of patients developed an APC during our long-term follow-up (16). We recently analyzed the causes of death in the same patient cohort. Notably, the long-term mortality rates for VA and VP shunts were the same. Importantly, in our detailed analysis, we did not find VA (e.g. due to pulmonary hypertension, thromboembolic events or shunt nephritis) or VP (e.g. due to bowel perforation) related-deaths associated with a specific type of shunt (17). These data indicate that most VAS-specific complications are potentially serious but may be reversible with early and adequate diagnosis and treatment. A life-long follow-up for VAspecific cardiopulmonary and renal complications is strongly recommended. As in several European centers, the surgical treatment of pediatric hydrocephalus at our institution was traditionally performed by pediatric surgeons until the late 1980s. Subsequently, as pediatric neurosurgeons had become more involved, neurosurgical standards were fully adopted for the surgical treatment of pediatric hydrocephalus in the late 1990s (17). Therefore, in this patient cohort, the ratio to choose VAS as the first-line surgical treatment might be difficult to interpret retrospectively. The limitations of this study were its retrospective nature and the absence of standardized follow-up to detect specific complications in patients with VASs.
Conclusions These long-term results, supported by the results of our previous studies, indicate that the overall morbidity and mortality rates in this patient cohort may be comparable in patients treated with VA and VP shunts (16, 17). The rate of elective distal lengthening and proximal shunt failure may be comparable in patients with VA and VP shunts (14, 16, 20). Moreover, there is no difference in the total number of VAS operations or the time to the first VAS revision between patients with primary VASs and second-line VASs. In a selective group of challenging patients, a VA shunt is an adequate surgical second-line alternative to standard VP shunting. The importance of effective patient/family education and lifelong routine monitoring to avoid late shunt complications in patients treated for pediatric hydrocephalus has previously been highlighted (16, 35-38). In the case of atrial catheters, additional
specific
follow-up
examinations
are
strongly
recommended
to
avoid
cardiopulmonary (11) or renal complications.
Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Conflict of interest: The authors declare that they have no conflict of interest.
Figure Legends
Figure 1. Distribution of the overall number of shunt operations per patient
Figure 2. Kaplan-Meier estimate for the time to the first VAS revision There is no difference between patients with primary VASs and second-line VASs (primary VP shunt or EVD; log-rank test, p=0.8) VAS, ventriculoatrial shunt; VP, ventriculoperitoneal; EVD, external ventricular drainage
Figure 3. Number of VA shunt revisions per patient (A) and the causes (B) AC, atrial catheter; VA, ventriculoatrial
References 1. Aschoff A, Kremer P, Hashemi B, Kunze S. The scientific history of hydrocephalus and its treatment. Neurosurg Rev. 1999;22:67–93; discussion 4–5. 2. Reddy GK, Bollam P, Caldito G. Long-term outcomes of ventriculoperitoneal shunt surgery in patients with hydrocephalus. World Neurosurg. 2014;81:404–410. 3. Symss NP, Oi S. Is there an ideal shunt? A panoramic view of 110 years in CSF diversions and shunt systems used for the treatment of hydrocephalus: from historical events to current trends. Childs Nerv Syst. 2015;31:191–202. 4. Vernet O, Campiche R, de Tribolet N. Long-term results after ventriculoatrial shunting in children. Childs Nerv Syst. 1993;9:253–255. 5. Vernet O, Campiche R, de Tribolet N. Long-term results after ventriculo-atrial shunting in children. Childs Nerv Syst. 1995;11:176–179. 6. Ignelzi RJ, Kirsch WM. Follow-up analysis of ventriculoperitoneal and ventriculoatrial shunts for hydrocephalus. J Neurosurg. 1975;42:679–682. 7. Borgbjerg BM, Gjerris F, Albeck MJ, Hauerberg J, Borgesen SV. A comparison between ventriculo-peritoneal and ventriculo-atrial cerebrospinal fluid shunts in relation to rate of revision and durability. Acta Neurochir (Wien). 1998;140:459–464; discussion 465. 8. George R, Leibrock L, Epstein M. Long-term analysis of cerebrospinal fluid shunt infections. A 25-year experience. J Neurosurg. 1979;51:804–811. 9. Hanak BW, Bonow RH, Harris CA, Browd SR. Cerebrospinal fluid shunting complications in children. Pediatr Neurosurg. 2017;52:381–400. 10. Keucher TR, Mealey J Jr. Long-term results after ventriculoatrial and ventriculoperitoneal shunting for infantile hydrocephalus. J Neurosurg. 1979;50:179–186. 11. Kluge S, Baumann HJ, Regelsberger J, Kehler U, Gliemroth J, Koziej B, et al. Pulmonary hypertension after ventriculoatrial shunt implantation. J Neurosurg. 2010;113:1279–1283. 12. Wilkinson N, Sood S, Ham SD, Gilmer-Hill H, Fleming P, Rajpurkar M. Thrombosis associated with ventriculoatrial shunts. J Neurosurg Pediatr. 2008;2:286–291. 13. Reddy GK, Bollam P, Caldito G, Guthikonda B, Nanda A. Ventriculoperitoneal shunt surgery outcome in adult transition patients with pediatric-onset hydrocephalus. Neurosurgery. 2012;70:380–388; discussion 8–9. 14. Stone JJ, Walker CT, Jacobson M, Phillips V, Silberstein HJ. Revision rate of pediatric ventriculoperitoneal shunts after 15 years. J Neurosurg Pediatr. 2013;11:15–19. 15. Zhang J, Qu C, Wang Z, Wang C, Ding X, Pan S, et al. Improved ventriculoatrial shunt for cerebrospinal fluid diversion after multiple ventriculoperitoneal shunt failures. Surg Neurol. 2009;72 Suppl 1:S29–S33; discussion S33–34. 16. Gmeiner M, Wagner H, van Ouwerkerk WJR, Senker W, Holl K, Gruber A. Abdominal pseudocysts and peritoneal catheter revisions: surgical long-term results in pediatric hydrocephalus. World Neurosurg. 2018;111:e912–e920. 17. Gmeiner M, Wagner H, Zacherl C, Polanski P, Auer C, van Ouwerkerk WJ, et al. Long-term mortality rates in pediatric hydrocephalus-a retrospective single-center study. Childs Nerv Syst. 2017;33:101–109. 18. Vinchon M, Baroncini M, Delestret I. Adult outcome of pediatric hydrocephalus. Childs Nerv Syst. 2012;28:847–854. 19. Team RC. A language and environment for statistical computing, Vienna, Austria. http://wwwR-projectorg; 2013. 20. Rymarczuk GN, Keating RF, Coughlin DJ, Felbaum D, Myseros JS, Oluigbo C, et al. A comparison of ventriculoperitoneal and ventriculoatrial shunts in a population of 544 consecutive pediatric patients. Neurosurgery. 2019:opz387.
21. Ivan LP, Choo SH, Ventureyra EC. Complications of ventriculoatrial and ventriculoperitoneal shunts in a new children’s hospital. Can J Surg. 1980;23:566–568. 22. Mazza C, Pasqualin A, Da Pian R. Results of treatment with ventriculoatrial and ventriculoperitoneal shunt in infantile nontumoral hydrocephalus. Childs Brain. 1980;7:1–14. 23. Olsen L, Frykberg T. Complications in the treatment of hydrocephalus in children. A comparison of ventriculoatrial and ventriculoperitoneal shunts in a 20-year material. Acta Paediatr Scand. 1983;72:385–390. 24. Fernell E, von Wendt L, Serlo W, Heikkinen E, Andersson H. Ventriculoatrial or ventriculoperitoneal shunts in the treatment of hydrocephalus in children? Z Kinderchir. 1985;40 Suppl 1:12–14. 25. Riva-Cambrin J, Kestle JR, Holubkov R, Butler J, Kulkarni AV, Drake J, et al. Risk factors for shunt malfunction in pediatric hydrocephalus: a multicenter prospective cohort study. J Neurosurg Pediatr. 2016;17:382–390. 26. Al-Schameri AR, Hamed J, Baltsavias G, Winkler P, Machegger L, Richling B, et al. Ventriculoatrial shunts in adults, incidence of infection, and significant risk factors: a singlecenter experience. World Neurosurg. 2016;94:345–351. 27. McGovern RA, Kelly KM, Chan AK, Morrissey NJ, McKhann GM 2nd. Should ventriculoatrial shunting be the procedure of choice for normal-pressure hydrocephalus? J Neurosurg. 2014;120:1458–1464. 28. Lundar T, Langmoen IA, Hovind KH. Fatal cardiopulmonary complications in children treated with ventriculoatrial shunts. Childs Nerv Syst. 1991;7:215–217. 29. D'Alonzo GE, Barst RJ, Ayres SM, Bergofsky EH, Brundage BH, Detre KM, et al. Survival in patients with primary pulmonary hypertension. Results from a national prospective registry. Ann Intern Med. 1991;115:343–349. 30. Clark DJ, Chakraborty A, Roebuck DJ, Thompson DN. Ultrasound guided placement of the distal catheter in paediatric ventriculoatrial shunts-an appraisal of efficacy and complications. Childs Nerv Syst. 2016;32:1219–1225. 31. Harland TA, Winston KR, Jovanovich AJ, Johnson RJ. Shunt nephritis: an increasingly unfamiliar diagnosis. World Neurosurg. 2018;111:346–348. 32. Babigumira M, Huang B, Werner S, Qunibi W. Delayed manifestation of shunt nephritis: a case report and review of the literature. Case Rep Nephrol. 2017;2017:1867349. 33. Sathyanarayana S, Wylen EL, Baskaya MK, Nanda A. Spontaneous bowel perforation after ventriculoperitoneal shunt surgery: case report and a review of 45 cases. Surg Neurol. 2000;54:388–396. 34. Vinchon M, Baroncini M, Laurent T, Patrick D. Bowel perforation caused by peritoneal shunt catheters: diagnosis and treatment. Neurosurgery. 2006;58:ONS76–82; discussion ONS76–82. 35. Acakpo-Satchivi L, Shannon CN, Tubbs RS, Wellons JC 3rd, Blount JP, Iskandar BJ, et al. Death in shunted hydrocephalic children: a follow-up study. Childs Nerv Syst. 2008;24:197–201. 36. Iskandar BJ, Tubbs S, Mapstone TB, Grabb PA, Bartolucci AA, Oakes WJ. Death in shunted hydrocephalic children in the 1990s. Pediatr Neurosurg. 1998;28:173–176. 37. Rekate HL, Blitz AM. Hydrocephalus in children. Handb Clin Neurol. 2016;136:1261–1273. 38. Vinchon M, Dhellemmes P. [Follow-up of adult patients treated during childhood for hydrocephalus]. Neurochirurgie. 2008;54:587–596.
Table 1. Patient and shunt characteristics in 61 patients with ventriculoatrial shunts Patient characteristics Male/female
Patients 36/25
Age at follow-up examination Median/range (years)
25.7/21.4–35.6
Etiology Meningomyelocele
15 (24.6%)
Intraventricular hemorrhage
14 (23%)
Postinfectious
11 (18%)
Aqueductal stenosis
8 (13.1%)
Posterior fossa cyst
6 (9.8%)
Congenital
3 (4.9%)
Others
4 (6.6%)
Age at the first surgical procedure Median (days)/range (years)
45/0–3.2 years
Time to the first revision Median (days)/range (days–years)
170/7 days–9.9 years
Age at the first VA shunt Median (days)/range (years)
91/0–19.4
Time to the first VA shunt revision Median (days)/range (years)
220/0–9.1
Last definitive shunt type VP
38 (62.3%)
VA
15 (24.6%)
Shunt explanation
8 (13.1%)
VA, ventriculoatrial; VP, ventriculoperitoneal
Table 2. Shunt valve aspects in patients with ventriculoatrial shunts Shunt
valve n
system Spitz-Holter
13
Age at VAS
Time to the first VAS revision
Median/range (days)
Median/range (days)
91/0–684
511.5/11–1219
Low-pressure
3
16/0–45
136/32–410
Medium-pressure
10
181/14–684
1030/11–1219
Hakim
21
45/0–1677
160/0–3318
Low-pressure
6
6.5/0–127
120.5/45–1708
Medium-pressure
15
50/2–1677
160/0–3318
Pudenz-Heyer
8
83.5/25–428
1431/66–2358
Low-pressure
4
69/38–98
784/123–1903
Medium-pressure
4
118/25–428
1541/66–2358
Orbis-Sigma
16
129/3–5089
435.5/5–1582
Others
3
4290/233–7092
457/62–852
VAS, ventriculoatrial shunt
Table 3. Revised and replaced shunt components in patients with ventriculoatrial shunt dysfunction Revised and replaced shunt components
N (%)
Ventricular catheter
37 (45.1%)
Completely new VP shunt
14 (17.1%)
Conversion to peritoneal catheter
7 (8.5%)
Shunt externalization
7 (8.5%)
Valve and atrial catheter
4 (4.9%)
Ventricular catheter and valve
3 (3.7%)
Completely new VA shunt
3 (3.7%)
Valve
3 (3.7%)
Atrial catheter
2 (2.4%)
Ventricular and atrial catheter
2 (2.4%)
VA, ventriculoatrial; VP, ventriculoperitoneal
Abbreviations and Acronyms:APC, Abdominal pseudocysts; CSF, Cerebrospinal fluid shunting; EVD, External ventricular drainage; VA, Ventriculoatrial; VAS, VA shunt; VP, Ventriculoperitoneal
Conflict of interest: The authors declare that they have no conflict of interest
Conceptualization; Data curation; Formal analysis; Funding acquisition; Investigation; Methodology; Project administration; Resources; Software; Supervision; Validation; Visualization; Roles/Writing - original draft; Writing - review & editing