Predictors of Satisfactory Surgical Outcome in Idiopathic Normal Pressure Hydrocephalus (Review)

Stanishevskiy А.V., Gavrilov G.V., Radkov M.N., Adlejba B.G., Svistov D.V.

Key words: idiopathic normal pressure hydrocephalus; predictor; neuroimaging; tap test; invasive diagnosis.

Idiopathic normal pressure hydrocephalus is a widespread neurodegenerative disease of the elderly. If not treated surgically early, it results in a severe decrease in quality of life and disability. According to current clinical Russian and foreign guidelines the candidates for CSF shunting procedures are selected based on the results of invasive tests, though treatment outcomes are not always optimal. At the same time, in the last decade there have been published a number of studies on promising noninvasive diagnosis and prognosis of the surgical treatment of idiopathic normal pressure hydrocephalus based on neuroimaging findings.

The aim of the present systematic review is to demonstrate the most promising imaging predictors of satisfactory outcomes of CSF shunting procedures in patients with idiopathic normal pressure hydrocephalus based on published literature data.

Introduction

Idiopathic normal pressure hydrocephalus (iNPH, Hakim–Adams syndrome) is a steadily progressive neurodegenerative disease, as a rule occurring in patients over 60, and characterized by an extension of CSF-containing brain spaces against the background of normal cerebrospinal fluid pressure, and represented by a triad of symptoms: impaired gait, cognitive sphere and pelvic organs functioning (Hakim–Adams triad). A unique characteristic of iNPH is possible complete or partial regress of symptoms in case of early surgical treatment — cerebrospinal fluid (CSF) shunting procedures [1]. However, according to large series of observations [2–7], patients’ improvement after CSF shunting procedures starts on average in 70.4% cases. No dynamics in patient’s state after CSF shunting procedures can be related to both: iNPH misdiagnosis (iNPH can be easily taken for other disease with similar presentation, e.g. Alzheimer’s disease, Parkinson’s disease, Binswanger’s disease, frontotemporal dementia, etc.), as well as with the surgery performed in the period of the disease when the symptoms are irreversible [8–11]. However, CSF shunting procedures are risk-bearing of complications including severe and life-threatening ones (Table 1).

Table 1. CSF shunting procedure efficiency in idiopathic normal pressure hydrocephaly (%)

According to current clinical recommendations [1, 12, 13], a decision on performing CSF shunting procedures is taken based on invasive diagnostic techniques. A systematic review by Thavarajasingam et al. [14] showed that among invasive techniques used for CSF shunting procedure outcome prognosis, the most effective (in decreasing order) ones are: intra-cranial pressure (ICP) monitoring using a parenchymatous sensor, prolonged external lumbar drainage of cerebrospinal fluid, an infusion-loading test and a tap test. The mentioned diagnostic procedures enhance the likelihood of CSF shunting procedure favorable outcome; however, do not ensure the postoperative neurological deficit regress. Moreover, the procedures are associated with the necessity of admission to a special hospital to carry out surgeries — lumbar puncture, external lumbar drainage or ICP sensor. Therefore, according to the polling of specialists involved in the disease treatment, the development of a save noninvasive technique for iNPH diagnosis is one of priority tasks for clinical research [15]. At the same time, a detailed volumetric analysis of brain structures and compartments based on MRI is indicative of high prognostic efficiency of the method in revealing the patients, in whom CSF shunting procedures are to result in positive dynamics of symptoms [16]. Similar findings were also obtained in morphometric assessment of grey matter in patients with hydrocephaly [17]. Thus, there are there are objective grounds to believe that the brain morphology changes revealed by neuroimaging in iNPH can serve as predictors of CSF shunting procedure favorable outcome.

The aim of the present review is to analyze the literature data on the most valuable imaging symptoms of idiopathic normal pressure hydrocephalus in relation to CSF shunting procedure prognosis.

Materials and Methods

The present systematic review is carried out in accordance with PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) criteria [18]. The literature was searched in databases: RSCI, PubMed/MEDLINE, Scopus, Web of Science, as well as using a searching system Google Scholar. Furthermore, there were selected the publications referring to the articles found as cited by, or those have similar descriptions (similar articles). After excluding the works, which are doubled in several sources, the bibliographic data and abstracts of the rest articles were studied concerning inclusion criteria match.

The study is a systematic review requiring no Ethics Committee approval.

The review includes the works carried out not until 2013, in Russian and English, having access to a full text (or an abstract with all necessary data), which describe the investigations devoted to detection of imaging predictors of CSF shunting procedure favorable outcome in iNPH patients. Figure 1 demonstrates the stages of literature search.

Figure 1. Methods for literature search for a systematic review

Results

The review includes 23 [6, 9, 16, 19–38] studies (22 original works and 1 meta-analysis). The analyzed predictors of CSF shunting procedure outcome were admitted reliable in 14 publications, while 9 ones revealed no statistically significant differences in surgery outcomes between the patients with and without the studied symptoms. Table 2 represents the imaging predictors of CSF shunting procedure outcomes stated through literature data analysis and ranged by the number of studies found them.

Table 2. Rating of CSF shunting procedure outcome predictors revealed in the review

MR-signal changes in the white brain matter, cingulate gyrus size, ventricle III diameter and ventricle IV size, great longitudinal fissure extension, CSF movement artefacts, hippocampal atrophy signs, the vertical size of the lateral ventricles and their roof bulging, SILVER-index value according to literature data cannot be considered as imaging predictors of CSF shunting procedure outcome in iNPH patients. Table 3 demonstrates the generalized systematic review findings.

Table 3. Brief description of study findings included in a systemic review

Discussion

The idea of limiting or complete refusal of invasive studies for CSF shunting procedure outcome prognosis is dictated by the following reasons.

Firstly, their use is risky, since the complication rate of external lumbar CSF drainage reaches 8.2%, and among them 3% are severe complications (subdural hematomas, infectious complications, etc.) [26].

Secondly, a positive result of the studies does not ensure any improvement in patient’s CSF shunting procedure postoperative state, while a negative result does not always enable to rule out iNPH. For instance, the presence of marked degenerative and dystrophic spinal changes in elderly patients can result in false results of tap-test, infusion-loading test and prolonged external lumbar CSF drainage [39].

Thirdly, the use of invasive studies requires inpatient treatment. Based on the analysis of cost-effectiveness and complication risks when using invasive iNPH diagnostic techniques, Eide et al. [40] indicated the necessity to search for other ways of CSF shunting procedure outcome prognosis.

Fourthly, the necessity to perform an invasive procedure for diagnostic purposes frequently decreases medication adherence and increases the time interval between the onset of iNPH symptoms and CSF shunting procedures. Moreover, some researchers prove conclusively that this parameter has a great influence on treatment result [9, 10, 41]. The patients operated on within the first 3 months after iNPH diagnosis is made appear to have the best outcome [10]. This fact also indicates the necessity of early disease detection and reduction of decision making period of CSF shunting procedures.

The third edition of Guidelines for management of iNPH by the Japanese Society of Normal Pressure Hydrocephalus [13] for the first time has assigned the possibility to make an iNPH diagnosis without invasive studies: DESH syndrome is recognized to be a diagnostic criterion equally ranking with a spinal tap test and prolonged lumbar CSF drainage.

Apart from DESH syndrome, various neuroimaging criteria were studied concerning CSF shunting procedure outcome prognosis. They are accepted to be distinguished into morphological and physiological [42]. Morphological symptoms include the changes of brain structures and spatial relationship of its parts (Evans index, DESH syndrome, callosal angle variation, periventricular changes, irregular extension of convexital subarachnoid spaces, the extension of temporal horns of lateral ventricles, etc.) revealed, as a rule, by routine procedures methods — CT and standard sequences of brain MRI. Physiological symptoms include the changes of the parameters determined by complex specialized techniques — CT- and MR-perfusion, MR-CSF dynamics, lymph MRI, as well as the changes in blood flow parameters in cerebral arteries and veins [43] and others.

According to the findings of meta-analysis performed by Thavarajasingam et al. [28], among the analyzed radiological symptoms (DESH syndrome, callosal angle, periventricular changes, cerebral blood flow, and cisternography findings) only callosal angle value and periventricular changes significantly differed between patients groups with positive and negative CSF shunting procedure outcome, except that the prognostic value of the parameters is not high. The authors marked the necessity to study the capabilities of a complex evaluation of neuroimaging symptoms for CSF shunting procedure outcome prognosis. A systematic review by Carlsen et al. [42] based on the analyzed 27 publications showed similar data. The findings of the present review correspond to the data: Table 2 and Table 3 demonstrate that just few imaging symptoms under study significantly differ in a group of patients with positive CSF shunting procedure outcome.

In an effort to improve efficiency of CSF shunting procedure outcome prognosis some authors tried to unite some neuroimaging iNPH symptoms into systems and scales. Ishii et al. [44] were the first who had an attempt to evaluate neuroimaging parameters for iNPH differential diagnosis. As follows from the correlation of Evans index values and colossal angle, the authors to a high precision succeeded in differentiating patients with iNPH, Alzheimer’s disease and those from a control group [44]. The best known scale for iNPH diagnosis by imaging data is iNPH Radscale including 7 parameters evaluated on brain computed tomograms [45]. The scale peculiarities are the assessment of morphological changes of brain structures according to CT, as well as no analysis of “contribution” of each parameter into iNPH diagnosis. It is just the thing related to the criticism by some researchers [19, 21, 33].

Gavrilov et al. [33] had an attempt to group the most informative neuroimaging iNPH predictors and unify them into differential diagnostic system using statistical methods of discriminant analysis and classification. The developed system enables to a high precision differentiate between iNPH and the diseases having similar presentation based on a complex assessment of MRI data. Further studies in this sphere aim at assembling to a similar system the predictors of CSF shunting procedure positive outcomes and on the obtained base forming an advanced algorithm of taking clinical decision limiting or completely excluding invasive procedures. Based on the data analysis made in systematic review the authors suggest the following iNPH diagnostic algorithm and candidates’ selection to perform CSF shunting procedures, which unites currently available knowledge (Figure 2).

Figure 2. Suggested diagnostic algorithm of idiopathic normal pressure hydrocephalus (iNPH) and selection of candidates for CSF shunting procedures, based on a systemic review

The next stage of improving iNPH diagnosis and the selection of candidates for CSF shunting procedures according to neuroimaging data can be the implementation of systems using artificial intelligence and computer-aided learning algorithms [46].

Conclusion

The analysis of the present systemic review established 12 predictors of the positive CSF shunting procedure outcome; the predictors proved their efficiency in the course of clinical studies. Further efforts should aim at uniting the revealed predictors into a system for CSF shunting procedure outcome prognosis. Establishing such system will enable to restrict or completely exclude the necessity to use invasive techniques.

Authors' contributions: A.V. Stanishevskiy, concept and design of the study, literature search, data analysis, writing the text of the article; G.V. Gavrilov, concept of the study, editing the text of the article; M.N. Radkov, literature search; B.G. Adlejba, literature search, writing the text of the article; D.V. Svistov, concept of the study, editing the text of the article.

Study funding. The study had no funding.

Conflict of interest. The authors declare no conflict of interest.

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