A consensus on the classification of hydrocephalus: its utility in the assessment of abnormalities of cerebrospinal fluid dynamics

Research into the basic causes of hydrocephalus began with Dr. Walter Dandy of Johns Hopkins University. As early as 1913 Dandy proposed a classification scheme for hydrocephalus that forms the basis of the accepted system still in use at this time. Dandy had few tools available to him at the time. The first studies in experimental animals related to the injection of a supravital dye into the ventricle and attempting to recover it from the spinal subarachnoid space (SSAS) via lumbar puncture. Based on these studies he classified hydrocephalus as either “communicating” or “obstructive or non-communicating” in nature [1]. The only other technique he could use to study what was happening in experimental animals or in affected individuals was to perform an autopsy. It was not until 1919 that Dandy was able to obtain more precise information about abnormalities of the cerebrospinal fluid (CSF) pathways by the injection of air either by lumbar puncture or its installation within the ventricle. Pneumoventriculography allowed more precise localization of the point of obstruction within the ventricular system as well as demonstrate distorted anatomy within the ventricles such as that caused by tumors in various locations [2]. The findings of Dandy’s newly developed tests related to the anatomy of CSF flow did not lead to modification of the classification of hydrocephalus.

The concepts described in the Dandy classification led to advances in the understanding of CSF dynamics and the understanding of the pathogenesis and treatment of hydrocephalus. Based on these concepts, Dandy defined the choroid plexus as the source of the production of CSF and proposed choroid plexectomy for the treatment of this condition. In patients with obstructive hydrocephalus, Dandy felt that creating an internal bypass was a likely form of treatment and performed operations in which communication between the third ventricle and the cortical subarachnoid space (CSAS) was created. This was originally done by the resection of one of the optic nerves [1]. Dandy’s 1913 classification still forms the basis of the bureaucratic methodology for physician payment in the USA. The International Classification of Diseases, Ninth Revision codes for hydrocephalus carry the same words as did Dandy’s work except for the very recent addition of the third category of Idiopathic Normal Pressure Hydrocephalus [3].

Several authors have attempted to develop more contemporary classification schemes, but none have served to improve the understanding of hydrocephalus and until now there has been no consensus as to a more contemporary classification scheme. Raimondi decided to use the translation of the term hydrocephalus as “water head” to produce a classification that included all conditions in which there were more than normal amounts of water within the intracranial compartment and thus included forms of cerebral edema, brain atrophy and intracranial cysts as well as forms of hydrocephalus. This classification is now only quoted in its historical context [4].

Mori with the encouragement and support of the Japanese ministry of health performed a study of various forms of hydrocephalus in Japanese children from many centers throughout Japan. The purpose of this study was to define “intractable hydrocephalus.” By this he meant which forms of hydrocephalus do not respond to treatment. In which of these patients is treatment futile [5]? Beni-Adani and her colleagues recognized that there was little consensus as to how one selects patients, particularly babies as to whether their hydrocephalus should be treated with a shunt or with an endoscopic third ventriculostomy. It was their intention that the proposed classification would serve to rigorously study the outcome of various treatments on various forms of hydrocephalus so that one would have a better idea as to whom to offer third ventriculostomy, and they presented the data from Israel related to these criteria [6].

Studying the relationship between what is happening in the developing brain and the pathologic processes that were occurring at that point in time led Oi to propose a classification of hydrocephalus that reflected the effect of brain distortion on the fetus and infant. He discussed its usefulness in the prediction of outcome in babies born with hydrocephalus of various causes. Early prediction of outcome is a very important issue, and the ability to define that outcome in the early mid-trimester would represent a major advance. Studies seem to be ongoing [7].

In 2000 I was asked by Dr. David McLone to write a chapter on the classification of hydrocephalus for the fourth edition of Pediatric Neurosurgery: Surgery of the Developing Nervous System [8]. I had been working with the School of Engineering at Case Western Reserve University on the application of engineering principles to the study of ventricular volume regulation. This process involved the use of a mathematical model which attempted to predict what would happen to the volume of the ventricles and the pressures within those compartments produced by creating resistance elements in the pathways between the CSF compartments. Previous work on such a model was reviewed and particularly the theoretical discussion by Spertell regarding brain viscoelasticity [9]. Our multi-compartmental model led to testable hypotheses which could explain what would happen if the sagittal sinus pressure was raised or what would happen if one created a resistance element at the basal cisterns. Figure 1 is a demonstration of the CSF system as interacting compartments each with its own pressure and volume related to the flow of CSF [10, 11]. Based on this diagram experiments could be performed on animal models of hydrocephalus that would challenge the results of the mathematics from the mathematical model. The diagram led to the need to measure the pressures and volumes in the individual compartments and to attempt to define the resistances between the various compartments. The result of this thought process became a circuit diagram of the CSF pathway as a hydraulic analog of an electrical circuit [12‐14]. Figure 2 is an artist’s rendering of this circuit diagram analogous to an electrical circuit. Visualizing the flow of CSF in this way serves as a template to assess the possible treatment options that are available to treat an individual patient. What followed has been a 30-year study of hydrocephalus based on this model. It became evident to me that this model would be useful in the classification of hydrocephalus and formed the basis of the book chapter that was produced [13, 15].

Review of the inconsistencies in the criteria that were being used for the selection of patients for endoscopic third ventriculostomy led to the unassailable conclusion that simply classifying hydrocephalus as communicating or non-communicating at a time when the actual point of the obstruction or restriction of CSF flow could be determined in most cases had become inadequate. Other questions that remained to be answered and could not be using the simple classification of Dandy included why some patients who developed hydrocephalus in infancy or had arachnoid cysts treated with shunts in infancy develop severely increased intracranial pressure with no expansion of the ventricles or cyst at the time of shunt failure. A more sophisticated classification was now available but not generally known or accepted. Techniques for the study of CSF dynamics had improved dramatically since the studies of Dandy. Tools such as magnetic resonance imaging (MRI), Cine MRI flow studies, cisternography utilizing dye studies and especially long-term studies of the outcomes of treatment decisions make it possible to accurately define a point of restriction of flow.

I was then invited at the inaugural meeting of the International Society for Hydrocephalus and CSF Research by meeting president Dr. Petra Klinge to give a talk on the subject of the definition and classification of hydrocephalus. In preparation for this talk I wrote an article published in the open access on-line journal Cerebrospinal Fluid Research entitled “A Contemporary Definition and Classification of Hydrocephalus: A Straw Man to Produce Debate.” At the time of the presentation at the meeting and during the experience in Hannover, I called on the participants to challenge and discuss the classification [13].

Following the “roll-out” of the concepts a large number of recognized experts in hydrocephalus treatment and research were contacted, and two meetings were held. The first occurred in Los Angeles at the 40th annual meeting of the International Society for Pediatric Neurosurgery. The second meeting was held in Phoenix in January of 2010. The participants in the process of producing a consensus statement are listed in the addendum at the end of this discussion (“Appendix”). At the end of these discussions a consensus was reached and agreed to by all. The results of these meetings were presented at the International Hydrocephalus Symposium in Crete in May 2010 and at the International Society for Research in Hydrocephalus and Spina Bifida in June as well as the Hydrocephalus Association Convention in July of that year. There was widespread support for the classification and enthusiasm that it would serve as a platform for research and structure to analyze research using animal models.

The structure of the consensus was that the first level of classification of hydrocephalus would be based on the point where the flow of CSF is restricted. The potential sites of restriction of flow as seen in Fig. 2 would be the foramina of Monro, the aqueduct of Sylvius, the basal cisterns, the arachnoid granulations, and outflow of venous blood from the dural venous sinuses. It was also recognized that hydrocephalus could exist and progress without a point of obstruction or increased resistance to flow. This would truly be communicating hydrocephalus.

The primary classification of point of obstruction would then be modified by the etiology of the inciting condition, the chronicity or rapidity of onset, and the age of the person or experimental animal. It is expected that the point of obstruction will be sought in both experimental animals as well as patients in clinical studies so that likes can be compared.

As opposed to Dandy, we now have the ability to actually define the specific point of obstruction to the flow of CSF within the craniospinal axis utilizing MRI sequences and the injection of iodine dye or radioactive tracers. This information is valuable both in deciding among different pathologic states in the differential diagnosis as well as deciding among different treatment options. Table 1 outlines the potential diagnoses and the treatment options related to the various points of obstruction to the hydraulic circuit. This classification should prove useful in future experimental design, assessment of unexpected results of treatment of hydrocephalus and the design of prospective trials for the treatment of subtypes of hydrocephalus.