In developing countries like Uganda, childhood hydrocephalus
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1 J Neurosurg Pediatrics 5: , 5: , 2010 Endoscopic third ventriculostomy in the treatment of childhood hydrocephalus in Uganda: report of a scoring system that predicts success Clinical article Be n j a m i n C. Wa r f, M.D., 1 Jo h n Mu g a m b a, M.D., 2 a n d Ab h aya V. Ku l k a r n i, M.D., Ph.D. 3 1 Department of Neurosurgery, Children s Hospital Boston, Harvard Medical School, Boston, Massachusetts; 2 CURE Children s Hospital of Uganda, Mbale, Uganda; and 3 Division of Neurosurgery, The Hospital for Sick Children, University of Toronto, Ontario, Canada Object. In Uganda, childhood hydrocephalus is common and difficult to treat. In some children, endoscopic third ventriculostomy (ETV) can be successful and avoid dependence on a shunt. This can be especially beneficial in Uganda, because of the high risk of infection and long-term failure associated with shunting. Therefore, the authors developed and validated a model to predict the chances of ETV success, taking into account the unique characteristics of a large sub-saharan African population. Methods. All children presenting with hydrocephalus at CURE Children s Hospital of Uganda (CCHU) between 2001 and 2007 were offered ETV as first-line treatment and were prospectively followed up. A multivariable logistic regression model was built using ETV success at 6 months as the outcome. The model was derived on 70% of the sample (training set) and validated on the remaining 30% (validation set). Results. Endoscopic third ventriculostomy was attempted in 1406 patients. Of these, 427 were lost to followup prior to 6 months. In the remaining 979 patients, the ETV was aborted in 281 due to poor anatomy/visibility and in 310 the ETV failed during the first 6 months. Therefore, a total of 388 of 979 (39.6% and [55.6% of completed ETVs]) procedures were successful at 6 months. The mean age at ETV was 12.6 months, and 57.8% of cases were postinfectious in origin. The authors logistic regression model contained the following significant variables: patient age at ETV, cause of hydrocephalus, and whether choroid plexus cauterization was performed. In the training set (676 patients) and validation set (303 patients), the model was able to accurately predict the probability of successful ETV (Hosmer-Lemeshow p value > 0.60 and C statistic > 0.70). The authors developed the simplified CCHU ETV Success Score that can be used in the field to predict the probability of ETV success. Conclusions. The authors model will allow clinicians to accurately identify children with a good chance of successful outcome with ETV, taking into account the unique characteristics and circumstances of the Ugandan population. (DOI: / PEDS09196) Ke y Wo r d s endoscopy hydrocephalus pediatrics developing countries logistic regression In developing countries like Uganda, childhood hydrocephalus is a very common and potentially devastating problem. Numerous socioeconomic and health care factors conspire to create populations with a greater fraction of children (50% of the Ugandan population is younger than 15 years old). 12 These children suffer a higher incidence of hydrocephalus, particularly postinfectious hydrocephalus, which is thought to result from the lack of skilled assistance during delivery, the rural perinatal environment, and cultural birth practices. 14 Based Abbreviations used in this paper: CCHU = CURE Children s Hospital for Uganda; ETV = endoscopic third ventriculostomy. J Neurosurg: Pediatrics / Volume 5 / February 2010 on the current population and crude birth rate in Uganda, the fact that postinfectious hydrocephalus accounts for 60% of hydrocephalus in infants, 1 and conservative estimates of hydrocephalus birth incidence (approximately 0.5/1000 births), 9,10 more than 1700 Ugandan infants per year can be anticipated to develop hydrocephalus. This would extrapolate to more than 45,000 new cases of hydrocephalus annually in all of sub-saharan Africa (population > 770 million). With this as the difficult background, the CCHU in Mbale, Uganda, was opened in 2001 with the mission of providing high-quality treatment of neurosurgical diseases, including hydrocephalus, for children in Uganda and 143
2 B. C. Warf, J. Mugamba, and A. V. Kulkarni neighboring nations. For over 50 years, the most common treatment for hydrocephalus has been the placement of a CSF shunt. This is, however, associated with many complications, including shunt obstruction, infection, and overdrainage of CSF. 2 More than half of all shunts fail in the first 2 years, and there is continued attrition over time often resulting in multiple shunt revisions. 2 In Uganda, dependence on a CSF shunt is especially dangerous because of the absence of the medical, social, and infrastructural safety net required for the urgent treatment of life-threatening shunt malfunctions. 13,14 Endoscopic third ventriculostomy is a relatively new treatment for hydrocephalus. 1 By avoiding permanently implanted hardware, ETV has a lower risk of infection and superior long-term patency. However, there are many children for whom an ETV is physiologically unsuitable, resulting in early failure and need for a shunt. The unique concerns of shunt-dependence in Uganda, however, led us to a more aggressive use of ETV, offering it to all children with hydrocephalus to try to avoid shunt surgery. The preliminary experience suggested that ETV, 5 particularly if combined with choroid plexus cauterization, could be successful in many cases. 13,14 The challenge has been to accurately identify a priori those children who would respond to ETV. In this report, we present our analysis of a prospective cohort of several hundred children who underwent their first attempt at ETV for treatment of hydrocephalus, the largest such sample ever assembled in the literature. Our goal was to develop a regression model and simplified scoring system that could be used in sub-saharan Africa to accurately predict the probability that an ETV attempt would be successful, based on the individual characteristics of a child. This would allow practitioners to optimally select children for ETV. Methods Patient Population Between June 2001 and May 2007, we prospectively collected data in patients 20 years of age and younger who underwent ETVs performed consecutively at CCHU in Mbale. The majority of children were from Uganda, but others were from Kenya, Tanzania, Malawi, Somalia, Rwanda, Congo, and Mauritius. The cost of all treatment was subsidized. All patients had symptomatic, high-pressure hydrocephalus and underwent preoperative imaging with ultrasound and, when it became available, CT scanning. Magnetic resonance imaging, a standard preoperative imaging modality in developed countries, was not available. Endoscopic third ventriculostomy was the primary treatment offered to all children presenting with hydrocephalus, regardless of age or cause. Shunts were used only if ETV failed or could not be performed for technical reasons. Some children had undergone previous treatment with a CSF shunt and presented with a shunt malfunction for which ETV was performed. Only patients who had at least 6 months follow-up were included in this analysis. In cases of multiple ETV procedures in the same patient, only data from the first procedure were included. Data from some of these patients have appeared in previous publications. 13,14 The procedure performed in all patients was a standard ETV through a frontal bur hole trajectory, with a fenestration made either in the floor of the third ventricle and/ or lamina terminalis using a flexible endoscope. Starting in January 2003, choroid plexus cauterization was also performed, whenever feasible. 6 In all these cases, full bilateral cauterization was the goal, unless this was not technically possible. Successful ETV was defined as the absence of ETV failure within 6 months. Failure of ETV was defined as any subsequent surgical procedure for definitive CSF diversion or death related to hydrocephalus management within 6 months of the index procedure. We chose this definition because the vast majority of ETV failures occur early (within 6 months), 8,15 and this usually indicates that a patient s underlying CSF physiology is not favorable for ETV. In clinical practice, these patients are most useful to identify. Any ETV procedure that had to be aborted for technical reasons (most commonly because of poor visibility secondary to cloudy or bloody CSF) was also considered an early failure (even though many of these did have a successful second ETV at a later date after the CSF had cleared sufficiently to provide adequate endoscopic visibility). Testing Validity of a Previous Prediction Model We previously derived a logistic regression model to predict the probability of success of ETV in children treated in developed countries (hereafter referred to as the Canadian prediction model). 8 The variables in this model included patient age at ETV, cause of hydrocephalus, and presence of a previous shunt. We tested the goodness-offit of the Canadian model on the Ugandan cohort using the Hosmer-Lemeshow statistic with the cases divided by decile cut-points based on predicted probability of successful ETV. This statistic compares the number of outcomes observed with the number predicted within each decile group; a significant probability value rejects the null hypothesis that the model fits the data well. 4 We tested model discrimination by determining the area under the receiver operating characteristic curve. This is equivalent to the C statistic for binary outcomes. 11 This statistic can be interpreted as the probability that the model predicts a higher chance for ETV success in an actual successful case compared with a failed case; a value closer to 1.0 represents better model discrimination. 3 Development of a New Prediction Model To provide better prediction of ETV success, we developed a new prediction model based on the Ugandan cohort. We randomly divided the data set into a training set (roughly 70% of the sample) for model development and a validation set (roughly 30% of the sample) for testing the model s fit and discrimination. The variables considered for the model were factors that we had included in our previous model (age at ETV, cause of hydrocephalus, presence of a previous CSF shunt) with an additional variable: whether choroid plexus cauterization was performed. This was categorized as complete bilateral cauterization, partial unilateral cauterization, and no cauterization. Age was categorized as 144 J Neurosurg: Pediatrics / Volume 5 / February 2010
3 Hydrocephalus in Uganda younger than 6 months, 6 to younger than 12 months, and at least 1 year, based on a preliminary assessment of ETV success across several age groups. The cause of hydrocephalus was categorized as postinfectious, myelomeningocele, and other. Given the limited brain imaging available, it was difficult to accurately classify the cause of the hydrocephalus beyond these 2 easily identifiable groups. Postinfectious hydrocephalus was designated if there was 1) no history consistent with hydrocephalus at birth, and either 2) a history of febrile illness and/or seizures preceding the onset of clinically obvious hydrocephalus, or 3) convincing findings at the time of endoscopy indicative of prior ventriculitis. Patients without an apparent infectious origin of the hydrocephalus were classified as other with the exception of the myelomeningocele group. We built a multivariable logistic regression model using a backward elimination process beginning with all 4 independent variables. Successful ETV at 6 months was the dependent variable. A variable was removed if its p value was > A more stringent cutoff was not used to avoid eliminating potentially important predictor variables. Multicollinearity was assessed with variance inflation factors, which is a measure of the degree to which a single predictor variable can be expressed as a linear combination of the remaining predictor variables; values > 10 are cause for concern. 7 To aid practitioners at the bedside, we developed a simplified summative scoring system based on the regression model. The values for each of the variables in the score were simple whole numbers that maintained the approximate proportion of the odds ratio from the regression model. We called this the CCHU ETV Success Score. We tested the adequacy of the CCHU ETV Success Score on the training set, as described above, and then, to test the internal validity of the model, we recalculated the score for each case in the validation set. All analyses were done using SPSS Advanced Statistics 13.0 (SPSS Inc.). This study received ethical approval from the CCHU institutional review board. Results The flow of recruited patients is shown in Fig. 1. The status of 979 patients was known definitively at 6 months post-etv, and they formed the basis of our analysis. Their characteristics are listed in Table 1. Of the 591 ETV failures, 12 (2.0%) were due to death and 281 (47.5%) were due to procedures that were aborted intraoperatively for technical reasons (poor visibility or difficult anatomy). Although patients in many of these aborted cases did go on to have a successful repeat attempt at ETV, these later attempts were excluded from this analysis. Of those having an ETV completed at the first operation, 55.6% were successful at 6 months. The long-term survival curve for ETV success is shown in Fig. 2. For the 388 patients in whom ETV was successful at 6 months, the 3-year ETV success rate was 95% (Kaplan-Meier method). The Canadian prediction model 8 was poorly predictive of ETV success in the Ugandan cohort. The model demonstrated poor fit (Hosmer-Lemeshow statistic, p < ) and poor discrimination (C statistic = 0.57). Development of a New Prediction Model A training set (676 patients) was randomly selected from the Ugandan cohort, and a logistic regression model was built that contained the following 3 variables: age (p < 0.001), cause of hydrocephalus (p = 0.01), and choroid Fig. 1. Diagram showing the flow of all patients recruited during the study. N = number of patients. J Neurosurg: Pediatrics / Volume 5 / February
4 B. C. Warf, J. Mugamba, and A. V. Kulkarni TABLE 1: Characteristics in 979 patients who underwent ETV No. of Patients (%) Variable Total Sample Training Set Validation Set no. of patients age at ETV <6 mos 632 (64.6) 421 (62.3) 211 (69.6) 6 to <12 mos 202 (20.6) 146 (21.6) 56 (18.5) 1 yr 145 (14.8) 109 (16.1) 36 (11.9) cause of hydrocephalus postinfectious 566 (57.8) 389 (57.5) 177 (58.4) myelomeningocele 117 (12.0) 79 (11.7) 38 (12.5) other 296 (30.2) 208 (30.8) 88 (29.0) previous CSF shunt in place 25 (2.6) 20 (3.0) 5 (1.7) choroid plexus cauterization performed no 602 (61.5) 420 (62.1) 182 (60.1) partial unilat 43 (4.4) 35 (5.2) 8 (2.6) complete bilat 334 (34.1) 221 (32.7) 113 (37.3) successful ETV at 6 mos 388 (39.6) 267 (39.5) 121 (39.9) plexus cauterization (p < 0.001). Presence of a previous shunt was eliminated (p = 0.73). Variance inflation factors were all < 2, suggesting that multicollinearity was not a concern. Parameter estimates (unstandardized regression coefficients) and odds ratios are shown in Table 2. From this regression model, we developed the simplified CCHU ETV Success Score (Fig. 3), which ranges from 0 (ETV least likely to succeed) to 9 (most likely to succeed). This CCHU ETV Success Score performed well in the training set. The mean score in the successful cases (267 ETVs) was significantly higher than in those that were not (409 ETVs) (4.0 ± 2.1 vs 2.2 ± 1.9 [± SD], p < 0.001). The Hosmer-Lemeshow statistic was not significant (p = 0.61), suggesting adequate model fit. The C statistic was 0.73, suggesting good model discrimination. Model Validation The CCHU ETV Success Score was calculated for each patient in the validation set (303 patients) and maintained good predictive properties. The mean score in the cases that were successful (121 ETVs) was significantly higher than in those that were not (182 ETVs) (mean 4.0 ± Fig. 2. Survival curve showing the long-term success of ETV for all 979 patients. Note the very steep drop-off at time zero, representing cases that had to be aborted intraoperatively. Many of these patients went on to receive successful ETV during a second procedure, but these second attempts were excluded from this analysis. Fig. 3. Diagram displaying the CCHU ETV system. 146 J Neurosurg: Pediatrics / Volume 5 / February 2010
5 Hydrocephalus in Uganda TABLE 2: Logistic regression model derived from the training set Variable Parameter Estimate OR for Successful ETV (95% CI) No. of Successful ETVs (%) age at ETV <6 mos ( ) 143 (34.0) 6 to <12 mos ( ) 60 (41.0) 1 yr reference reference 64 (58.7) cause of hydrocephalus postinfectious ( ) 148 (38.0) myelomeningocele ( ) 44 (55.7) other reference reference 75 (36.1) choroid plexus cauterization performed no reference reference 116 (27.6) partial unilat ( ) 14 (40.0) complete bilat ( ) 137 (62.0) 2.4 vs 2.2 ± 2.0, p < 0.001). The Hosmer-Lemeshow statistic was not significant (p = 0.68). The C statistic was 0.71, indicating little difference from the training set (0.73). The CCHU ETV Success Score was able to effectively stratify both the training and validation sets into high (> 0.70), moderate ( ), and low (< 0.50) chance of ETV success (Table 3). Discussion We have shown, in the largest prospective series to date, the efficacy of ETV, especially with choroid plexus cauterization, in the treatment of childhood hydrocephalus in sub-saharan Africa. We have also shown that early success of the procedure portends a very high chance of long-term success (successful ETV at 6 months was associated with a 3-year success rate of 95%). Importantly, we have developed and validated the CCHU ETV Success Score that can be used to confidently predict the probability that ETV will be successful for a given child. Our results are particularly important because they are derived from a protocol of nonselective use of ETV for all children with hydrocephalus, eliminating the selection bias that is present in virtually all other series from developed nations. 1,6 Hydrocephalus is the most common neurosurgical disorder in children, and it is very difficult to treat, especially in sub-saharan Africa. An ETV has the potential to revolutionize the treatment of these children because, aside from start-up equipment costs, there are no other equipment costs that must be borne by the family. The risk of infection is also much lower (< 1% in the CCHU experience 13 ), since no implanted foreign hardware is left in place, and, when initially successful, the long-term patency appears to be excellent. There is, however, great uncertainty over which children will respond to ETV. Given the difficulties these children can face in reaching appropriate medical attention at the time of an acute ETV failure, the CCHU ETV Success Score will serve an important clinical purpose in helping to confidently identify those with a good chance of long-term success after discharge from the hospital. There are significant differences between the Ugandan hydrocephalus population and those in developed countries. There is a much greater preponderance of a postinfectious origin than in developed countries. There is also a lack of reliable primary medical care, which results in children often presenting late with very advanced disease. In addition, the environment poses strict technological and financial limitations in diagnosis and treatment. For example, there is no access to preoperative MR imaging, which makes a preoperative detailed assessment of the brain anatomy virtually impossible. It is, therefore, not surprising that our previously derived Canadian model was poorly predictive of outcome in the Ugandan population. The newly derived CCHU ETV Success Score accounts for the unique characteristics of sub-saharan Africa, including the fact that nearly half of all ETV failures were due to technical difficulties at surgery that precluded successful completion of the procedure. In developed countries, many of these technical failures would have been avoided because of the use of high-resolution preoperative MR imaging, which would TABLE 3: Comparison of predicted and actual ETV success stratified by CCHU ETV Success Score Training Set (676 patients) Validation Set (303 patients) CCHU ETV Success Score No. of Cases Actual Proportion of Successful ETV Mean Predicted Probability of Successful ETV No. of Cases Actual Proportion of Successful ETV Mean Predicted Probability of Successful ETV 7 9 (high chance of success) (moderate chance of success) (low chance of success) J Neurosurg: Pediatrics / Volume 5 / February
6 B. C. Warf, J. Mugamba, and A. V. Kulkarni have alerted the surgeon to difficult anatomical variations, and an ETV likely would not have been even attempted in such cases. Preoperative MR imaging remains unavailable for this patient population. We recognize the limitations in our study. The realities of the patient population in Uganda made follow-up very difficult, despite our conscientious attempts. Approximately 30% of the initial patient sample was lost to follow-up before 6 months, and these patients were not included in our analysis. Although there was good follow-up of the remaining patients to 12 months, at 3 years the status of only 68 patients in whom ETV did not fail was known. This is attributable to the wide geographic area from which these patients arrived and the steep financial and transportation barriers for many families to make return visits to CCHU, particularly for a child who was doing well. The strength of our conclusion regarding the long durability of ETV in this population is, therefore, somewhat limited. These results, however, largely confirm what we have shown about long-term patency in developed countries. 8 The technique of ETV is currently not in widespread use in many centers in Africa, and there is a learning curve associated with this. Our results, therefore, might not be applicable to all new centers just learning the technique. 5 During the course of our study, the surgeries were performed primarily by 2 surgeons, both of whom learned the procedure for the first time at CCHU. These results are particular to sub-saharan Africa and might not be applicable to other developing areas of the world, due to differences in the underlying patient population and causes of hydrocephalus. Based on our promising experience in Uganda, we are creating centers in other sub-saharan African nations where the ETV procedure will be available. Thus far, neurosurgeons in 5 African countries have been trained in and equipped with the technique. Their results will be followed prospectively, with rigorous attempts made to have long-term follow-up in all children, to allow us to externally validate the CCHU ETV Success Score. We recognize that our prediction score cannot yet be used, in isolation, to definitively determine when ETV should or should not be used as the primary treatment. This issue is complex, and our future prospective work will help us determine the optimal threshold for choosing between ETV and shunt for these children. Conclusions We have developed and validated the CCHU ETV Success Score that accurately predicts the chance that an ETV will succeed for children with hydrocephalus treated in sub-saharan African. This is a very unique and challenging population and our results can be used to better select children for ETV, thereby avoiding the need for a permanent shunt. 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: BC Warf and J Mugamba acquired data and critically reviewed and contributed to the final manuscript; and AV Kulkarni performed and interpreted the data analysis, and drafted the final manuscript. Dr. Kulkarni had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. References 1. Drake JM: Endoscopic third ventriculostomy in pediatric patients: the Canadian experience. Neurosurgery 60: , Drake JM, Kestle JR, Milner R, Cinalli G, Boop F, Piatt J Jr, et al: Randomized trial of cerebrospinal fluid shunt valve design in pediatric hydrocephalus. Neurosurgery 43: , Hanley JA, McNeil BJ: The meaning and use of the area under a receiver operating characteristic (ROC) curve. 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J Pediatr 155: , Msamati BC, Igbigbi PS, Chisi JE: The incidence of cleft lip, cleft palate, hydrocephalus and spina bifida at Queen Elizabeth Central Hospital, Blantyre, Malawi. Cent Afr J Med 46: , Stein SC, Feldman JG, Apfel S, Kohl SG, Casey G: The epidemiology of congenital hydrocephalus. A study in Brooklyn, N.Y Childs Brain 8: , Steyerberg EW, Harrell FE Jr, Borsboom GJ, Eijkemans MJ, Vergouwe Y, Habbema JD: Internal validation of predictive models: efficiency of some procedures for logistic regression analysis. J Clin Epidemiol 54: , United Nations Statistics Division: Social Indicators: Indicators on Youth and Elderly Populations. org/unsd/demographic/products/socind/youth.htm [Accessed September 24, 2009] 13. Warf BC: Comparison of endoscopic third ventriculostomy alone and combined with choroid plexus cauterization in infants younger than 1 year of age: a prospective study in 550 African children. J Neurosurg 103 (6 Suppl): , Warf BC: Hydrocephalus in Uganda: the predominance of infectious origin and primary management with endoscopic third ventriculostomy. J Neurosurg 102 (1 Suppl):1 15, Warf BC, Campbell JW: Combined endoscopic third ventriculostomy and choroid plexus cauterization as primary treatment of hydrocephalus for infants with myelomeningocele: long-term results of a prospective intent-to-treat study in 115 East African infants. J Neurosurg Pediatr 2: , 2008 Manuscript submitted April 21, Accepted September 21, Address correspondence to: Abhaya V. Kulkarni, M.D., Ph.D., Division of Neurosurgery, The Hospital for Sick Children, University of Toronto, Room 1503, 555 University Avenue, Toronto, Ontario, Canada M5G 1X8. abhaya.kulkarni@sickkids.ca. 148 J Neurosurg: Pediatrics / Volume 5 / February 2010
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