Hydrocephalus

Last updated
Hydrocephalus
Other namesWater on the brain [1]
Hydrocephalus (cropped).jpg
Hydrocephalus as seen on a CT scan of the brain. The black areas in the middle of the brain (the lateral ventricles) are abnormally large and filled with fluid.
Pronunciation
Specialty Neurosurgery
Symptoms Babies: rapid head growth, vomiting, sleepiness, seizures [1]
Older people: Headaches, double vision, poor balance, urinary incontinence, personality changes, mental impairment [1]
Causes Neural tube defects, meningitis, brain tumors, traumatic brain injury, brain bleed during birth, intraventricular hemorrhage [1]
Diagnostic method Based on symptoms and medical imaging [1]
TreatmentSurgery [1]
Prognosis Variable, often normal life [1]
FrequencyVaries throughout the world, from 1 per 256 live births to 1 per 9,000, depending on access to prenatal health care, prenatal tests, and abortion [1] [3]

Hydrocephalus is a condition in which cerebrospinal fluid (CSF) builds up within the brain. [1] This typically causes increased pressure inside the skull. Older people may have headaches, double vision, poor balance, urinary incontinence, personality changes, or mental impairment. In babies, there may be a rapid increase in head size. Other symptoms may include vomiting, sleepiness, seizures, and downward pointing of the eyes. [1]

Contents

Hydrocephalus can occur due to birth defects (primary) or be acquired later in life (secondary). [1] Hydrocephalus can be classified via mechanism into communicating, noncommunicating, ex vacuo, and normal pressure hydrocephalus. Diagnosis is typically made by physical examination and medical imaging. [1]

Hydrocephalus is typically treated by the surgical placement of a shunt system. [1] A procedure called a third ventriculostomy is an option in some people. [1] Outcomes are variable, but many people with shunts live normal lives. [1] Without treatment, permanent disability or death may occur. [1]

About one to two per 1,000 newborns have hydrocephalus. [1] [3] Rates in the developing world may be higher. [4] Normal pressure hydrocephalus is estimated to affect about 5 per 100,000 people, with rates increasing with age. [5] Description of hydrocephalus by Hippocrates dates back more than 2,000 years. [4] The word hydrocephalus is from the Greek ὕδωρ, hydōr, meaning 'water' and κεφαλή, kephalē, meaning 'head'. [6]

Signs and symptoms

Illustration showing different effects of hydrocephalus on the brain and cranium Hydrocephalus CDC.png
Illustration showing different effects of hydrocephalus on the brain and cranium
Adult showing cranial deformity from pediatric hydrocephalus Gould Pyle 94.jpg
Adult showing cranial deformity from pediatric hydrocephalus

The clinical presentation of hydrocephalus varies with chronicity. Acute dilatation of the ventricular system is more likely to manifest with the nonspecific signs and symptoms of increased intracranial pressure (ICP). By contrast, chronic dilatation (especially in the elderly population) may have a more insidious onset presenting, for instance, with Hakim's triad (Adams' triad). [7]

Symptoms of increased ICP may include headaches, vomiting, nausea, papilledema, sleepiness, or coma. With increased levels of CSF, there have been cases of hearing loss due to CSF creating pressure on the auditory pathways or disrupting the communication of inner ear fluid. [8] Elevated ICP of different etiologies have been linked to sensorineural hearing loss (SNHL). Transient SNHL has been reported after the loss of CSF with shunt surgeries. [9] Hearing loss is a rare but well-known sequela of procedures resulting in CSF loss. [8] Elevated ICP may result in uncal or tonsillar herniation (where a portion of the brain moves out of place due to increased intracranial pressure),resulting in life-threatening brain stem compression. [10]

Hakim's triad of gait instability, urinary incontinence, and dementia is a relatively typical manifestation of the distinct entity normal-pressure hydrocephalus. Focal neurological deficits may also occur, such as abducens nerve palsy and vertical gaze palsy (Parinaud syndrome due to compression of the quadrigeminal plate, where the neural centers coordinating the conjugated vertical eye movement are located). The symptoms depend on the cause of the blockage, the person's age, and how much brain tissue has been damaged by the swelling. [10]

The "setting sun" phenomenon, where the eyes always appear to be looking downward Parinaud syndrome 2.jpg
The "setting sun" phenomenon, where the eyes always appear to be looking downward

In infants with hydrocephalus, CSF builds up in the central nervous system (CNS), causing the fontanelle (soft spot of an infant's skull) to bulge and the head to be larger than expected. Early symptoms may also include: [10]

Symptoms that may occur in older children can include: [10]

Because hydrocephalus can injure the brain, thought and behavior may be adversely affected. Learning disabilities, including short-term memory loss, are common among those with hydrocephalus, who tend to score better on verbal IQ than on performance IQ, which is thought to reflect the distribution of nerve damage to the brain. [1] Hydrocephalus that is present from birth can cause long-term complications with speech and language. Children can have issues such as nonverbal learning disorder, difficulty understanding complex and abstract concepts, difficulty retrieving stored information, and spatial/perceptual disorders. Children with hydrocephalus are often known in having the difficulty in understanding the concepts within conversation and tend to use words they know or have heard. [12] [13] However, the severity of hydrocephalus can differ considerably between individuals, and some are of average or above-average intelligence. Someone with hydrocephalus may have coordination and visual problems, or clumsiness. They may reach puberty earlier than the average child (this is called precocious puberty). About one in four develops epilepsy. [14]

Causes

Hydrocephalus can be caused by a combination of factors and is not fully understood. Any medical condition that interrupts the flow of cerebrospinal fluid (CSF) can cause this build-up of excess fluid. This occurs due to blocked pathways of cerebrospinal fluid (CSF), issues with CSF reabsorption, or increased CSF production. [15]

Hydrocephalus can be classified as primary or secondary (acquired) based on the cause. [16]

Primary

Primary hydrocephalus involves congenital, developmental, and genetic factors that lead to excess CSF build-up. [16] Up to 50% of the causes of primary hydrocephalus are genetic. [17]

Congenital hydrocephalus is defined by the presence of excess CSF at birth. It occurs due to a combination of factors, with genetic causes prior to birth, meaning the fetus developed hydrocephalus in utero during fetal development. The most common cause of congenital hydrocephalus is aqueductal stenosis, which occurs when the narrow passage between the third and fourth ventricles in the brain is blocked or too narrow to allow sufficient cerebral spinal fluid to drain. Fluid accumulates in the upper ventricles, causing hydrocephalus. [18]

Developmental disorders including neural-tube defects, arachnoid cysts, Dandy–Walker syndrome, and Arnold–Chiari malformation can also cause primary hydrocephalus. About 80–90% of fetuses or newborn infants with the neural-tube defect spina bifida—often associated with meningocele or myelomeningocele—develop hydrocephalus. [19]

Secondary (Acquired)

Secondary hydrocephalus is acquired as a consequence of CNS infections, meningitis, brain tumors, head trauma, toxoplasmosis, or intracranial hemorrhage (subarachnoid or intraparenchymal). [20]

Intraventricular hemorrhage, or bleeding within the ventricles of the brain, leads to hydrocephalus in 51-89% of patients. [21] This is because the blood in the ventricles blocks the regular flow of CSF, leading to build-up of excess CSF [21]

Spontaneous intracerebral and intraventricular hemorrhage with hydrocephalus shown on CT scan Intracerebral hemorrhage.jpg
Spontaneous intracerebral and intraventricular hemorrhage with hydrocephalus shown on CT scan

Normal pressure hydrocephalus (NPH) most often occurs in elderly patients with symptoms including gait disturbance, urinary incontinence, and cognitive issues. [23] It is commonly divided into two categories, idiopathic NPH (with unknown cause) and secondary NPH (due to trauma, hemorrhage, etc.). [23]

Hydrocephalus can also be caused by overproduction of CSF (relative obstruction) (e.g., choroid plexus papilloma, villous hypertrophy). [24] [25]

Bilateral ureteric obstruction is a rare, but reported, cause of hydrocephalus.


Mechanism

Diagram showing CSF flow and neuroanatomy. CSF circulation.png
Diagram showing CSF flow and neuroanatomy.

Hydrocephalus is due to an imbalance between the amount of CSF produced and the amount reabsorbed (or removed from the ventricular system) [26] . In a person without hydrocephalus, CSF continuously circulates through the brain, its ventricles and the spinal cord and is continuously drained away into the circulatory system. Alternatively, the condition may result from an overproduction of the CSF, from a congenital malformation blocking normal drainage of the fluid, or from complications of head injuries or infections. [27]

The choroid plexus, located in the lateral ventricles, forms the majority of CSF (believed to be around 70-80%). The ependymal lining of the ventricular system, the subarachnoid space, and the blood-brain-barrier forms the rest [26] .

CSF flows through the ventricular system through the following pathway: [28]

Lateral Ventricles → Interventricular Foramen of Monro → Third Ventricle → Cerebral Aqueduct → Fourth Ventricle

The CSF then exits the fourth ventricle through the median aperture and lateral aperture. It goes into the subarachnoid space or central canal of the spinal cord. Then, it is absorbed by the vili of arachnoid granulations into the blood circulation. [28]

There is also theory about CSF drainage into the lymphatic vessel system. [28]

Mechanism of Symptoms

Compression of the brain by the accumulating fluid eventually may cause neurological symptoms such as convulsions, intellectual disability, and epileptic seizures. These signs occur sooner in adults, whose skulls are no longer able to expand to accommodate the increasing fluid volume within. Fetuses, infants, and young children with hydrocephalus show head enlargement, excluding the face, because the pressure of the fluid causes the individual skull bones—which have yet to fuse—to bulge outward at their juncture points. [29]

Elevated intracranial pressure from the excess CSF build-up may cause compression of the brain, leading to brain damage and other complications. The mechanism of ICP on hearing loss is presumed that the transmission of CSF pressure to and from the Perilymphatic space through a patent cochlear aqueduct. [30] [31] The cochlear aqueduct connects the Perilymphatic space of the inner ear with the subarachnoid space of the posterior cranial fossa. [32] A loss of CSF pressure can induce Perilymphatic loss or endolymphatic hydrops resembling the clinical presentation of Ménière's disease associated hearing loss in the low frequencies. [30]

CSF can accumulate within the ventricles, this condition is called internal hydrocephalus and may result in increased CSF pressure. The production of CSF continues, even when the passages that normally allow it to exit the brain are blocked. Consequently, fluid builds inside the brain, causing pressure that dilates the ventricles and compresses the nervous tissue. Compression of the nervous tissue usually results in irreversible brain damage. If the skull bones are not completely ossified when the hydrocephalus occurs, the pressure may also severely enlarge the head. The cerebral aqueduct may be blocked at the time of birth or may become blocked later in life because of a tumor growing in the brainstem. [33]

Classification

The classification of communicating vs. noncommunicating hydrocephalus are often used to describe the types of hydrocephalus. These terms describe the nonobstructive vs. obstructive mechanisms of the excess CSF build-up.

Communicating

In communicating hydrocephalus, there is no obstruction of CSF flow. Instead, there is either an increased production of CSF or difficulty reabsorbing CSF [34] . Reabsorption occurs at the arachnoid granulations, so issues with reabsorption can occur because of arachnoid granulation impairment. There is also evidence of the lymphatic system being involved with reabsorption, so impairments of this system can also lead to excess CSF. Damage to these reabsorption sites are commonly post-hemorrhage or post-infection (such as meningitis). [34] Scarring and fibrosis of the subarachnoid space following infectious, inflammatory, or hemorrhagic events can also prevent reabsorption of CSF, causing hydrocephalus. [35]

An adult with congenital hydrocephalus in the Philippines Hydrocephalus cranial deformity 2.jpg
An adult with congenital hydrocephalus in the Philippines

Noncommunicating

In noncommunicating hydrocephalus, there is obstruction to the CSF flow. Examples of common causes include hemorrhage, tumor, traumatic brain injury that disrupts the flow and causes build-up of CSF in the brain [34] .

Other

Hydrocephalus ex vacuo from vascular dementia as seen on MRI BrainAtrophy(exvacuo).png
Hydrocephalus ex vacuo from vascular dementia as seen on MRI

Treatments

Procedures

Baby recovering from shunt surgery Khidmat Masy Hydrocephalus (19042957419).jpg
Baby recovering from shunt surgery
Ventriculoperitoneal shunt placement in child with hydrocephalus Hydrocephalus Shunt Child.png
Ventriculoperitoneal shunt placement in child with hydrocephalus

Hydrocephalus is treated through surgery by creating creating a way for the excess fluid to drain away. An external ventricular drain (EVD), also known as an extraventricular drain or ventriculostomy, provides relief in the short term. [38] In the long term, some people will need any of the various types of cerebral shunts. It involves the placement of a ventricular catheter (a tube made of silastic) into the cerebral ventricles. This creates a way to bypass the flow obstruction/malfunctioning arachnoidal granulations. The excess fluid drains into other body cavities where it can be resorbed. Most shunts drain the fluid into the peritoneal cavity (ventriculoperitoneal shunt). Other shunts drain the fluid into the right atrium (ventriculoatrial shunt), pleural cavity (ventriculopleural shunt), and gallbladder. [39]

A shunt system can also be placed in the lumbar space of the spine. This allows the excess fluid to be redirected to the peritoneal cavity (lumbar-peritoneal shunt). [40] Another treatment for obstructive hydrocephalus is an endoscopic third ventriculostomy (ETV). This surgery creates an opening in the floor of the third ventricle so that CSF flows directly to the basal cisterns. This treatment can shortcut any obstruction like aqueductal stenosis. This may or may not be appropriate based on individual anatomy. Some infants can be treated with ETV and choroid plexus cauterization. Choroid plexus cauterization reduces the amount of cerebrospinal fluid produced by the brain. The technique, known as ETV/CPC, was pioneered in Uganda by neurosurgeon Benjamin Warf and is now in use in several U.S. hospitals. [41] [42]

External hydrocephalus

External hydrocephalus is generally seen in infants. It involves enlarged fluid spaces or subarachnoid spaces outside of the brain. The most common sign is a head circumference above the 90th percentile. In most cases, no other signs or symptoms are reported. [43] Rarely reported symptoms include a tense anterior fontanel, developmental delay, seizures, irritability, and vomiting. [44] Usually, this condition is benign. It resolves spontaneously by two to three years of age. [45] Thus, it usually does not need insertion of a shunt. If surgical treatment is required, a ventriculoperitoneal shunt is usually preferred. [44] Other treatment options include using medications like acetazolamide. [43] The condition can be diagnosed and monitored with brain sonography and CT/MRI. These tests and a good medical history can help to identify external hydrocephalus from similar conditions: subdural hemorrhages or symptomatic chronic extra-axial fluid collections which are accompanied by vomiting, headaches, and seizures. [46] [47]

Shunt complications

Some risk exists of infection being introduced into the brain through cerebral shunts, as they must be replaced as the person grows. [48] [49] Examples of possible complications include shunt malfunction, shunt failure, and shunt infection, along with infection of the shunt tract following surgery (the most common reason for shunt failure is infection of the shunt tract). Although a shunt generally works well, it may stop working if it disconnects, becomes blocked (clogged) or infected, or it is outgrown. If this happens, the CSF begins to accumulate again and a number of physical symptoms develop (headaches, nausea, vomiting, photophobia/light sensitivity), some extremely serious, such as seizures. The shunt failure rate is also relatively high (of the 40,000 surgeries performed annually to treat hydrocephalus, only 30% are a person's first surgery) and people not uncommonly have multiple shunt revisions within their lifetimes. [50]

Another complication can occur when CSF drains more rapidly than it is produced by the choroid plexus, causing symptoms of listlessness, severe headaches, irritability, light sensitivity, auditory hyperesthesia (sound sensitivity), hearing loss, [32] nausea, vomiting, dizziness, vertigo, migraines, seizures, a change in personality, weakness in the arms or legs, strabismus, and double vision to appear when the person is vertical. If the person lies down, the symptoms usually vanish quickly. A CT scan may or may not show any change in ventricle size, particularly if the person has a history of slit-like ventricles. Difficulty in diagnosing over-drainage can make treatment of this complication particularly frustrating for people and their families. Resistance to traditional analgesic pharmacological therapy may also be a sign of shunt overdrainage or failure. [51]

Following placement of a ventriculoperitoneal shunt there have been cases of a decrease in post-surgery hearing. It is presumed that the cochlea aqueduct is responsible for the decrease in hearing thresholds. The cochlea aqueduct has been considered as a probable channel where CSF pressure can be transmitted. Therefore, the reduced CSF pressure could cause a decrease in Perilymphatic pressure and cause secondary endolymphatic hydrops. [32] In addition to the increased hearing loss, there have also been findings of resolved hearing loss after ventriculoperitoneal shunt placement, where there is a release of CSF pressure on the auditory pathways. [52]

The diagnosis of CSF buildup is complex and requires specialist expertise. Diagnosis of the particular complication usually depends on when the symptoms appear, that is, whether symptoms occur when the person is upright or in a prone position, with the head at roughly the same level as the feet. [53]

Standardized protocols for inserting cerebral shunts have been shown to reduce shunt infections. [54] [55] There is tentative evidence that preventative antibiotics may decrease the risk of shunt infections. [56]

Epidemiology

It is estimated that congenital hydrocephalus occurs in 8.5 out of 10,000 live births globally. The disease burden is more concentrated in Africa, Asia, and South America. [57] A study in 2019 estimated that there are 180,000 childhood hydrocephalus cases from the African continent per year. It also reported 90,000 cases from Southeast Asia and the Western Pacific. Congenital hydrocephalus was found to be associated with many factors. Tthe health of the affected individual's mother is one factor. Exposure to medications in the prenatal period such as antibiotics is another factor. Low socioeceonomic status is also a factor. [57] In adults that are 18–64 years-old, about 11 in 100,000 cases of hydrocephalus is estimated. For adults over 65 years of age, 175 in 100,000 cases is estimated. [58]

History

Skull of a hydrocephalic child (1800s) Vimont Traite de Phrenologie 022.jpg
Skull of a hydrocephalic child (1800s)

In the pre-historic area, there were various paintings or artifacts depicting children or adults with macrocephaly (large head) or clinical findings of hydrocephalus. [59] The earliest scientific description of hydrocephalus was written by the ancient Greek physician Hippocrates, who coined the word 'hydrocephalus' from the Greek ὕδωρ, hydōr meaning 'water' and κεφαλή, kephalē meaning 'head'. [60] A more accurate description was later given by the Roman physician Galen in the second century AD. [60]

The first clinical description of an operative procedure for hydrocephalus appears in the Al-Tasrif (1,000 AD) by the Arab surgeon Abulcasis, who described the evacuation of superficial intracranial fluid in hydrocephalic children. [60] He described it in his chapter on neurosurgical disease, describing infantile hydrocephalus as being caused by mechanical compression. He wrote: [60]

The skull of a newborn baby is often full of liquid, either because the matron has compressed it excessively or for other, unknown reasons. The volume of the skull then increases daily, so that the bones of the skull fail to close. In this case, we must open the middle of the skull in three places, make the liquid flow out, then close the wound and tighten the skull with a bandage.

Historical specimen of an infant with severe hydrocephalus, probably untreated Hydrocephalus-baby.jpg
Historical specimen of an infant with severe hydrocephalus, probably untreated

In 1881, a few years after the landmark study of Retzius and Key, Carl Wernicke pioneered sterile ventricular puncture and external drainage of CSF for the treatment of hydrocephalus. [60] It remained an intractable condition until the 20th century, when cerebral shunt and other neurosurgical treatment modalities were developed.[ citation needed ]

The first hydrocephalus shunt was placed in 1956. [40]

Society and culture

Name

The word hydrocephalus is from the Greek ὕδωρ, hydōr meaning 'water' and κεφαλή, kephalē meaning 'head'. [6] Other names for hydrocephalus include "water on the brain", a historical name, and "water baby syndrome". [1] [61]

Awareness campaign

Hydrocephalus awareness ribbon Hydrocephalus ribbon two tone blue.jpg
Hydrocephalus awareness ribbon

September was designated National Hydrocephalus Awareness Month in July 2009 by the U.S. Congress in H.Res. 373. The resolution campaign is due in part to the advocacy work of the Pediatric Hydrocephalus Foundation. Prior to July 2009, no awareness month for this condition had been designated. Many hydrocephalus organizations, such as the One Small Voice Foundation, promote awareness and fundraising activities.[ citation needed ]

Notable cases

Related Research Articles

<span class="mw-page-title-main">Cerebrospinal fluid</span> Clear, colorless bodily fluid found in the brain and spinal cord

Cerebrospinal fluid (CSF) is a clear, colorless body fluid found within the tissue that surrounds the brain and spinal cord of all vertebrates.

<span class="mw-page-title-main">Idiopathic intracranial hypertension</span> Medical condition

Idiopathic intracranial hypertension (IIH), previously known as pseudotumor cerebri and benign intracranial hypertension, is a condition characterized by increased intracranial pressure without a detectable cause. The main symptoms are headache, vision problems, ringing in the ears, and shoulder pain. Complications may include vision loss.

<span class="mw-page-title-main">Colpocephaly</span> Brain malformation in which the lateral ventricles are enlarged

Colpocephaly is a cephalic disorder involving the disproportionate enlargement of the occipital horns of the lateral ventricles and is usually diagnosed early after birth due to seizures. It is a nonspecific finding and is associated with multiple neurological syndromes, including agenesis of the corpus callosum, Chiari malformation, lissencephaly, and microcephaly. Although the exact cause of colpocephaly is not known yet, it is commonly believed to occur as a result of neuronal migration disorders during early brain development, intrauterine disturbances, perinatal injuries, and other central nervous system disorders. Individuals with colpocephaly have various degrees of motor disabilities, visual defects, spasticity, and moderate to severe intellectual disability. No specific treatment for colpocephaly exists, but patients may undergo certain treatments to improve their motor function or intellectual disability.

<span class="mw-page-title-main">Ventricular system</span> Structures containing cerebrospinal fluid

In neuroanatomy, the ventricular system is a set of four interconnected cavities known as cerebral ventricles in the brain. Within each ventricle is a region of choroid plexus which produces the circulating cerebrospinal fluid (CSF). The ventricular system is continuous with the central canal of the spinal cord from the fourth ventricle, allowing for the flow of CSF to circulate.

<span class="mw-page-title-main">Pia mater</span> Delicate innermost layer of the meninges, the membranes surrounding the brain and spinal cord

Pia mater, often referred to as simply the pia, is the delicate innermost layer of the meninges, the membranes surrounding the brain and spinal cord. Pia mater is medieval Latin meaning "tender mother". The other two meningeal membranes are the dura mater and the arachnoid mater. Both the pia and arachnoid mater are derivatives of the neural crest while the dura is derived from embryonic mesoderm. The pia mater is a thin fibrous tissue that is permeable to water and small solutes. The pia mater allows blood vessels to pass through and nourish the brain. The perivascular space between blood vessels and pia mater is proposed to be part of a pseudolymphatic system for the brain. When the pia mater becomes irritated and inflamed the result is meningitis.

<span class="mw-page-title-main">Intracranial pressure</span> Pressure exerted by fluids inside the skull and on the brain

Intracranial pressure (ICP) is the pressure exerted by fluids such as cerebrospinal fluid (CSF) inside the skull and on the brain tissue. ICP is measured in millimeters of mercury (mmHg) and at rest, is normally 7–15 mmHg for a supine adult. This equals to 9–20 cmH2O, which is a common scale used in lumbar punctures. The body has various mechanisms by which it keeps the ICP stable, with CSF pressures varying by about 1 mmHg in normal adults through shifts in production and absorption of CSF.

<span class="mw-page-title-main">Fourth ventricle</span> One of four central brain cavities filled with cerebrospinal fluid

The fourth ventricle is one of the four connected fluid-filled cavities within the human brain. These cavities, known collectively as the ventricular system, consist of the left and right lateral ventricles, the third ventricle, and the fourth ventricle. The fourth ventricle extends from the cerebral aqueduct to the obex, and is filled with cerebrospinal fluid (CSF).

Normal pressure hydrocephalus (NPH), also called malresorptive hydrocephalus, is a form of communicating hydrocephalus in which excess cerebrospinal fluid (CSF) builds up in the ventricles, leading to normal or slightly elevated cerebrospinal fluid pressure. The fluid build-up causes the ventricles to enlarge and the pressure inside the head to increase, compressing surrounding brain tissue and leading to neurological complications. Although the cause of idiopathicNPH remains unclear, it has been associated with various co-morbidities including hypertension, diabetes mellitus, Alzheimer's disease, and hyperlipidemia. Causes of secondary NPH include trauma, hemorrhage, or infection. The disease presents in a classic triad of symptoms, which are memory impairment, urinary frequency, and balance problems/gait deviations. The disease was first described by Salomón Hakim and Raymond Adams in 1965.

<span class="mw-page-title-main">Median aperture</span>

The median aperture is an opening at the caudal portion of the roof of the fourth ventricle. It allows the flow of cerebrospinal fluid (CSF) from the fourth ventricle into the cisterna magna. The other openings of the fourth ventricle are the lateral apertures - one on either side. The median aperture varies in size but accounts for most of the outflow of CSF from the fourth ventricle.

<span class="mw-page-title-main">Dandy–Walker malformation</span> Congenital malformation of the cerebellar vermis

Dandy–Walker malformation (DWM), also known as Dandy–Walker syndrome (DWS), is a rare congenital brain malformation in which the part joining the two hemispheres of the cerebellum does not fully form, and the fourth ventricle and space behind the cerebellum are enlarged with cerebrospinal fluid. Most of those affected develop hydrocephalus within the first year of life, which can present as increasing head size, vomiting, excessive sleepiness, irritability, downward deviation of the eyes and seizures. Other, less common symptoms are generally associated with comorbid genetic conditions and can include congenital heart defects, eye abnormalities, intellectual disability, congenital tumours, other brain defects such as agenesis of the corpus callosum, skeletal abnormalities, an occipital encephalocele or underdeveloped genitalia or kidneys. It is sometimes discovered in adolescents or adults due to mental health problems.

<span class="mw-page-title-main">Colloid cyst</span> Medical condition

A colloid cyst is a non-malignant tumor in the brain. It consists of a gelatinous material contained within a membrane of epithelial tissue. It is almost always found just posterior to the foramen of Monro in the anterior aspect of the third ventricle, originating from the roof of the ventricle. Because of its location, it can cause obstructive hydrocephalus and increased intracranial pressure. Colloid cysts represent 0.5–1.0% of intracranial tumors.

<span class="mw-page-title-main">Cerebral shunt</span> Surgical implant to treat hydrocephalus

A cerebral shunt is a device permanently implanted inside the head and body to drain excess fluid away from the brain. They are commonly used to treat hydrocephalus, the swelling of the brain due to excess buildup of cerebrospinal fluid (CSF). If left unchecked, the excess CSF can lead to an increase in intracranial pressure (ICP), which can cause intracranial hematoma, cerebral edema, crushed brain tissue or herniation. The drainage provided by a shunt can alleviate or prevent these problems in patients with hydrocephalus or related diseases.

<span class="mw-page-title-main">Intraventricular hemorrhage</span> Bleeding into the brains ventricular system

Intraventricular hemorrhage (IVH), also known as intraventricular bleeding, is a bleeding into the brain's ventricular system, where the cerebrospinal fluid is produced and circulates through towards the subarachnoid space. It can result from physical trauma or from hemorrhagic stroke.

Endoscopic third ventriculostomy (ETV) is a surgical procedure for treatment of hydrocephalus in which an opening is created in the floor of the third ventricle using an endoscope placed within the ventricular system through a burr hole. This allows the cerebrospinal fluid to flow directly to the basal cisterns, bypassing the obstruction. Specifically, the opening is created in the translucent tuber cinereum on the third ventricular floor.

<span class="mw-page-title-main">Choroid plexus carcinoma</span> Medical condition

A choroid plexus carcinoma is a type of choroid plexus tumor that affects the choroid plexus of the brain. It is considered the worst of the three grades of chord plexus tumors, having a much poorer prognosis than choroid atypical plexus papilloma and choroid plexus papilloma. The disease creates lesions in the brain and increases cerebrospinal fluid volume, resulting in hydrocephalus.

<span class="mw-page-title-main">External ventricular drain</span> Medical device

An external ventricular drain (EVD), also known as a ventriculostomy or extraventricular drain, is a device used in neurosurgery to treat hydrocephalus and relieve elevated intracranial pressure when the normal flow of cerebrospinal fluid (CSF) inside the brain is obstructed. An EVD is a flexible plastic catheter placed by a neurosurgeon or neurointensivist and managed by intensive care unit (ICU) physicians and nurses. The purpose of external ventricular drainage is to divert fluid from the ventricles of the brain and allow for monitoring of intracranial pressure. An EVD must be placed in a center with full neurosurgical capabilities, because immediate neurosurgical intervention can be needed if a complication of EVD placement, such as bleeding, is encountered.

Bobble-head doll syndrome is a rare neurological movement disorder in which patients, usually children around age 3, begin to bob their head and shoulders forward and back, or sometimes side-to-side, involuntarily, in a manner reminiscent of a bobblehead doll. The syndrome is related to cystic lesions and swelling of the third ventricle in the brain.

A lumbar–peritoneal shunt is a technique to channelise the cerebrospinal fluid (CSF) from the lumbar thecal sac into the peritoneal cavity.

<span class="mw-page-title-main">Subependymal giant cell astrocytoma</span> Medical condition

Subependymal giant cell astrocytoma is a low-grade astrocytic brain tumor (astrocytoma) that arises within the ventricles of the brain. It is most commonly associated with tuberous sclerosis complex (TSC). Although it is a low-grade tumor, its location can potentially obstruct the ventricles and lead to hydrocephalus.

<span class="mw-page-title-main">Aqueductal stenosis</span> Narrowing of the aqueduct of Sylvius

Aqueductal stenosis is a narrowing of the aqueduct of Sylvius which blocks the flow of cerebrospinal fluid (CSF) in the ventricular system. Blockage of the aqueduct can lead to hydrocephalus, specifically as a common cause of congenital and/or obstructive hydrocephalus.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 "Hydrocephalus Fact Sheet". NINDS. April 5, 2016. Archived from the original on 27 July 2016. Retrieved 5 September 2016.
  2. ↑ "Hydrocephalus". Collins. Retrieved 1 April 2020.
  3. 1 2 Stevenson DK, Benitz WE (2003). Fetal and Neonatal Brain Injury: Mechanisms, Management and the Risks of Practice. Cambridge: Cambridge University Press. p. 117. ISBN   9780521806916. Archived from the original on 2016-12-21.
  4. 1 2 Ellenbogen RG, Abdulrauf SI, Sekhar LN (2012). Principles of Neurological Surgery. Elsevier Health Sciences. p. 105. ISBN   978-1-4377-0701-4.
  5. ↑ Ferri FF (2016). Ferri's Clinical Advisor 2017: 5 Books in 1. Elsevier Health Sciences. p. 621. ISBN   9780323448383. Archived from the original on 2016-12-21.
  6. 1 2 Dorland's electronic medical dictionary (29th ed.). W.B. Saunders Co. 2000. ISBN   9780721694931.
  7. ↑ Gavrilov, Gaspar V.; Gaydar, Boris V.; Svistov, Dmitry V.; Korovin, Alexander E.; Samarcev, Igor N.; Churilov, Leonid P.; Tovpeko, Dmitry V. (December 2019). "Idiopathic Normal Pressure Hydrocephalus (Hakim-Adams Syndrome): Clinical Symptoms, Diagnosis and Treatment" (PDF). Psychiatria Danubina. 31 (Suppl 5): 737–744. PMID   32160166.
  8. 1 2 Satzer D, Guillaume DJ (January 2016). "Hearing loss in hydrocephalus: a review, with focus on mechanisms". Neurosurgical Review. 39 (1): 13–24, discussion 25. doi:10.1007/s10143-015-0650-2. PMID   26280639. S2CID   24439157.
  9. ↑ Dixon JF, Jones RO (June 2012). "Hydrocephalus-associated hearing loss and resolution after ventriculostomy". Otolaryngology–Head and Neck Surgery. 146 (6): 1037–1039. doi:10.1177/0194599811431234. PMID   22166958. S2CID   38240969.
  10. 1 2 3 4 Riveros Gilardi B, Muñoz López JI, Hernández Villegas AC, Garay Mora JA, Rico Rodríguez OC, Chávez Appendini R, et al. (October 2019). "Types of Cerebral Herniation and Their Imaging Features". Radiographics. 39 (6): 1598–1610. doi:10.1148/rg.2019190018. PMID   31589570. S2CID   203924869.
  11. ↑ Kaneshiro NK, Zieve D, Black B, A.D.A.M. Editorial team. "Hydrocephalus". MedlinePlus.
  12. ↑ Barnes MA, Dennis M (February 1998). "Discourse after early-onset hydrocephalus: core deficits in children of average intelligence". Brain and Language. 61 (3): 309–334. doi:10.1006/brln.1998.1843. PMID   9570868. S2CID   13336454.
  13. ↑ Oi S (1999), "Hydrocephalus Associated with Spina Bifida: Specific Pathophysiology and Therapeutic Problems", Spina Bifida, Springer Japan, pp. 177–184, ISBN   978-4-431-70260-3
  14. ↑ Parent, Anne-Simone; Teilmann, Grete; Juul, Anders; Skakkebaek, Niels E.; Toppari, Jorma; Bourguignon, Jean-Pierre (October 2003). "Hydrocephalus". Endocrine Reviews. 24 (5): 668–693. doi:10.1210/er.2002-0019. PMID   14570750 . Retrieved 2022-05-16.
  15. ↑ Koleva, Miroslava; De Jesus, Orlando (2025), "Hydrocephalus", StatPearls, Treasure Island (FL): StatPearls Publishing, PMID   32809710 , retrieved 2025-01-15
  16. 1 2 Karimy, Jason K.; Reeves, Benjamin C.; Damisah, Eyiyemisi; Duy, Phan Q.; Antwi, Prince; David, Wyatt; Wang, Kevin; Schiff, Steven J.; Limbrick, David D.; Alper, Seth L.; Warf, Benjamin C.; Nedergaard, Maiken; Simard, J. Marc; Kahle, Kristopher T. (May 2020). "Inflammation in acquired hydrocephalus: pathogenic mechanisms and therapeutic targets". Nature Reviews Neurology. 16 (5): 285–296. doi:10.1038/s41582-020-0321-y. ISSN   1759-4758. PMC   7375440 . PMID   32152460.
  17. ↑ Hochstetler, Alexandra; Raskin, Jeffrey; Blazer-Yost, Bonnie L. (2022-09-01). "Hydrocephalus: historical analysis and considerations for treatment". European Journal of Medical Research. 27 (1): 168. doi: 10.1186/s40001-022-00798-6 . ISSN   2047-783X. PMC   9434947 . PMID   36050779.
  18. ↑ "The Hydrocephalus Association". Archived from the original on 2006-08-20.
  19. ↑ "Spina Bifida". Spinabifidamoms.com. Archived from the original on 2013-11-01. Retrieved 2014-01-29.
  20. ↑ "Acquired Hydrocephalus | Conditions & Treatments | UCSF Benioff Children's Hospital". www.ucsfbenioffchildrens.org. Retrieved 2020-04-09.
  21. 1 2 Wang, Chaoyang; Bai, Jianuo; He, Qiheng; Jiao, Yuming; Zhang, Wenqian; Huo, Ran; Wang, Jie; Xu, Hongyuan; Zhao, Shaozhi; Wu, Zhiyou; Sun, Yingfan; Yu, Qifeng; Tang, Jinyi; Zeng, Xianwei; Yang, Wuyang (2024-06-03). "Therapy management and outcome of acute hydrocephalus secondary to intraventricular hemorrhage in adults". Chinese Neurosurgical Journal. 10 (1): 17. doi: 10.1186/s41016-024-00369-0 . ISSN   2057-4967. PMC   11149196 . PMID   38831472.
  22. ↑ Yadav YR, Mukerji G, Shenoy R, Basoor A, Jain G, Nelson A (January 2007). "Endoscopic management of hypertensive intraventricular haemorrhage with obstructive hydrocephalus". BMC Neurology. 7: 1. doi: 10.1186/1471-2377-7-1 . PMC   1780056 . PMID   17204141.
  23. 1 2 Passos-Neto, Carlos Eduardo Borges; Lopes, Cesar Castello Branco; Teixeira, Mauricio Silva; Studart Neto, Adalberto; Spera, Raphael Ribeiro (May 2022). "Normal pressure hydrocephalus: an update". Arquivos de Neuro-Psiquiatria. 80 (5 suppl 1): 42–52. doi:10.1590/0004-282x-anp-2022-s118. ISSN   1678-4227. PMC   9491444 . PMID   35976308.
  24. ↑ Adunka O, Buchman C (11 October 2010). Otology, Neurotology, and Lateral Skull Base Surgery: An Illustrated Handbook. Thieme. pp. 353–. ISBN   978-3-13-149621-8. Archived from the original on 5 July 2014. Retrieved 12 August 2013.
  25. ↑ Nimjee SM, Powers CJ, McLendon RE, Grant GA, Fuchs HE (April 2010). "Single-stage bilateral choroid plexectomy for choroid plexus papilloma in a patient presenting with high cerebrospinal fluid output". Journal of Neurosurgery. Pediatrics. 5 (4): 342–345. doi:10.3171/2009.10.peds08454. PMID   20367337.
  26. 1 2 Bramall, Alexa N.; Anton, E.S.; Kahle, Kristopher T.; Fecci, Peter E. (April 2022). "Navigating the ventricles: Novel insights into the pathogenesis of hydrocephalus". eBioMedicine. 78: 103931. doi:10.1016/j.ebiom.2022.103931. PMC   8933686 . PMID   35306341.
  27. ↑ "Hydrocephalus Fact Sheet". National Institute of Neurological Disorders and Stroke. August 2005. Archived from the original on 2016-07-27.
  28. 1 2 3 Leinonen, Ville; Vanninen, Ritva; Rauramaa, Tuomas (2018), "Cerebrospinal fluid circulation and hydrocephalus", Handbook of Clinical Neurology, vol. 145, Elsevier, pp. 39–50, doi:10.1016/b978-0-12-802395-2.00005-5, ISBN   978-0-12-802395-2 , retrieved 2025-01-15
  29. ↑ Cabot RC (1919). Physical diagnosis (7th ed.). New York: William Wood and Company. p. 5 – via Google Books.
  30. 1 2 Pogodzinski MS, Shallop JK, Sprung J, Weingarten TN, Wong GY, McDonald TJ (March 2008). "Hearing loss and cerebrospinal fluid pressure: case report and review of the literature". Ear, Nose, & Throat Journal. 87 (3): 144–147. doi: 10.1177/014556130808700308 . PMID   18404909.
  31. ↑ Marchbanks RJ, Reid A (June 1990). "Cochlear and cerebrospinal fluid pressure: their inter-relationship and control mechanisms". British Journal of Audiology. 24 (3): 179–187. doi:10.3109/03005369009076554. PMID   2194603.
  32. 1 2 3 Lim HW, Shim BS, Yang CJ, Kim JH, Cho YH, Cho YS, et al. (August 2014). "Hearing loss following ventriculoperitoneal shunt in communicating hydrocephalus patients: a pilot study". The Laryngoscope. 124 (8): 1923–1927. doi:10.1002/lary.24553. PMID   24318317. S2CID   24667376.
  33. ↑ "Hydrocephalus: Causes, symptoms, and treatments". www.medicalnewstoday.com. 2017-12-07. Retrieved 2022-05-18.
  34. 1 2 3 Mirkhaef, Sarah A; Harbaugh, Lauren; Nagra, Gurjit (2024-09-03). "Hydrocephalus: A Review of Etiology-Driven Treatment Strategies". Cureus. 16 (9): e68516. doi: 10.7759/cureus.68516 . ISSN   2168-8184. PMC   11448269 . PMID   39364470.
  35. ↑ Kaye A, Fox C, Diaz J (2014). Essentials of Pediatric Anesthesiology. Cambridge University Press. p. 106.
  36. ↑ Martin BA, Loth F (December 2009). "The influence of coughing on cerebrospinal fluid pressure in an in vitro syringomyelia model with spinal subarachnoid space stenosis". Cerebrospinal Fluid Research. 6 (1): 17. doi: 10.1186/1743-8454-6-17 . PMC   2806373 . PMID   20043856.
  37. 1 2 Hemanshu P (2016-02-29). Complications in neuroanesthesia. Elsevier Science. ISBN   9780128040751. OCLC   939553425.
  38. ↑ Navaei, Amir; Hanaei, Sara; Habibi, Zohreh; Jouibari, Morteza; Heidari, Vahid; Naderi, Soheil; Nejat, Farideh (December 2018). "Controlled trial to compare therapeutic efficacy of endoscopic third ventriculostomy plus choroid plexus cauterization with ventriculoperitoneal shunt in infants with obstructive hydrocephalus". Asian Journal of Neurosurgery. 13 (4): 1042–1047. doi: 10.4103/ajns.AJNS_63_17 . ISSN   1793-5482. PMC   6208245 . PMID   30459864.
  39. ↑ Bue, Enrico Lo; Morello, Alberto; Bellomo, Jacopo; Bradaschia, Leonardo; Lacatena, Filippo; Colonna, Stefano; Fiumefreddo, Alessandro; Stieglitz, Lennart; Regli, Luca; Lanotte, Michele Maria; Garbossa, Diego; Cofano, Fabio (2024-08-09). "Ventriculoatrial shunt remains a safe surgical alternative for hydrocephalus: a systematic review and meta-analysis". Scientific Reports. 14 (1): 18460. Bibcode:2024NatSR..1418460B. doi:10.1038/s41598-024-62366-8. ISSN   2045-2322. PMC   11310213 . PMID   39117692.
  40. 1 2 Ho, Yi-Jen; Chiang, Wen-Chun; Huang, Hsin-Yi; Lin, Shinn-Zong; Tsai, Sheng-Tzung (March 2023). "Effectiveness and safety of ventriculoperitoneal shunt versus lumboperitoneal shunt for communicating hydrocephalus: A systematic review and meta-analysis with trial sequential analysis". CNS Neuroscience & Therapeutics. 29 (3): 804–815. doi:10.1111/cns.14086. ISSN   1755-5930. PMC   9928545 . PMID   36650662.
  41. ↑ "An American surgeon pioneers surgery for kids in Uganda that helps kids in the US". Public Radio International. 22 April 2015. Archived from the original on 2016-03-02. Retrieved 2016-02-10.
  42. ↑ Burton A (August 2015). "Infant hydrocephalus in Africa: spreading some good news". The Lancet. Neurology. 14 (8): 789–790. doi:10.1016/S1474-4422(15)00138-6. PMID   26091960. S2CID   35920581.
  43. 1 2 Khosroshahi, N (Autumn 2018). "Benign Enlargement of Subarachnoid Space in Infancy: "A Review with Emphasis on Diagnostic Work-Up"". Iranian Journal of Child Neurology. 12 (4): 7–15. PMC   6160631 . PMID   30279704.
  44. 1 2 Zahl, Sverre Morten; Egge, Arild; Helseth, Eirik; Wester, Knut (October 2011). "Benign external hydrocephalus: a review, with emphasis on management". Neurosurgical Review. 34 (4): 417–432. doi:10.1007/s10143-011-0327-4. ISSN   0344-5607. PMC   3171652 . PMID   21647596.
  45. ↑ Greenberg MS (2010-02-15). Handbook of Neurosurgery. Thieme. ISBN   9781604063264. Archived from the original on 2023-07-08.
  46. ↑ "Subdural Hematomas in the Elderly: The Great Neurological Imitator | 2000-03-01 | AHC Media: Continuing Medical Education Publishing | Relias Media - Continuing Medical Education Publishing". www.reliasmedia.com. Retrieved 2022-05-17.
  47. ↑ Ravid, Sarit; Maytal, Joseph (February 2003). "External hydrocephalus: a probable cause for subdural hematoma in infancy". Pediatric Neurology. 28 (2): 139–141. doi:10.1016/s0887-8994(02)00500-3. PMID   12699866.
  48. ↑ Pople IK (September 2002). "Hydrocephalus and shunts: what the neurologist should know". Journal of Neurology, Neurosurgery, and Psychiatry. 73 (suppl 1): i17 –i22. doi:10.1136/jnnp.73.suppl_1.i17 (inactive 1 November 2024). PMC   1765598 . PMID   12185257.{{cite journal}}: CS1 maint: DOI inactive as of November 2024 (link)
  49. ↑ Engelhard III HH, Sahrakar K, Pang D (2022-03-03). Talavera F (ed.). "Neurosurgery for Hydrocephalus Treatment & Management: Approach Considerations, Medical Therapy, Surgical Therapy". Medscape.
  50. ↑ Benner KW, Spellen S, Jeske A. "Pharmacology of Shunt Infections". www.uspharmacist.com. Retrieved 2022-05-18.
  51. ↑ Nagahama Y, Peters D, Kumonda S, Vesole A, Joshi C, J Dlouhy B, Kawasaki H (2017-01-24). "Delayed diagnosis of shunt overdrainage following functional hemispherotomy and ventriculoperitoneal shunt placement in a hemimegalencephaly patient". Epilepsy & Behavior Case Reports. 7: 34–36. doi:10.1016/j.ebcr.2016.12.003. PMC   5357741 . PMID   28348960.
  52. ↑ Sammons VJ, Jacobson E, Lawson J (October 2009). "Resolution of hydrocephalus-associated sensorineural hearing loss after insertion of ventriculoperitoneal shunt". Journal of Neurosurgery. Pediatrics. 4 (4): 394–396. doi:10.3171/2009.4.PEDS09103. PMID   19795973.
  53. ↑ Krishnan SR, Arafa HM, Kwon K, Deng Y, Su CJ, Reeder JT, et al. (2020-03-06). "Continuous, noninvasive wireless monitoring of flow of cerebrospinal fluid through shunts in patients with hydrocephalus". npj Digital Medicine. 3 (1): 29. doi:10.1038/s41746-020-0239-1. PMC   7060317 . PMID   32195364.
  54. ↑ Yang MM, Hader W, Bullivant K, Brindle M, Riva-Cambrin J (February 2019). "Calgary Shunt Protocol, an adaptation of the Hydrocephalus Clinical Research Network shunt protocol, reduces shunt infections in children". Journal of Neurosurgery. Pediatrics. 23 (5): 559–567. doi:10.3171/2018.10.PEDS18420. PMID   30797206. S2CID   73507028.
  55. ↑ Kestle JR, Riva-Cambrin J, Wellons JC, Kulkarni AV, Whitehead WE, Walker ML, et al. (July 2011). "A standardized protocol to reduce cerebrospinal fluid shunt infection: the Hydrocephalus Clinical Research Network Quality Improvement Initiative". Journal of Neurosurgery. Pediatrics. 8 (1): 22–29. doi:10.3171/2011.4.PEDS10551. PMC   3153415 . PMID   21721884.
  56. ↑ Arts SH, Boogaarts HD, van Lindert EJ (June 2019). "Route of antibiotic prophylaxis for prevention of cerebrospinal fluid-shunt infection". The Cochrane Database of Systematic Reviews. 6 (6): CD012902. doi:10.1002/14651858.CD012902.pub2. PMC   6548496 . PMID   31163089.
  57. 1 2 Gili, Juan Antonio; López-Camelo, Jorge Santiago; Nembhard, Wendy N.; Bakker, Marian; de Walle, Hermien E. K.; Stallings, Erin B.; Kancherla, Vijaya; ECEMC Peripheral Group; Contiero, Paolo; Dastgiri, Saeed; Feldkamp, Marcia L.; Nance, Amy; Gatt, Miriam; Martínez, Laura; Canessa, María Aurora (2022-07-15). "Analysis of early neonatal case fatality rate among newborns with congenital hydrocephalus, a 2000–2014 multi-country registry-based study". Birth Defects Research. 114 (12): 631–644. doi:10.1002/bdr2.2045. ISSN   2472-1727. PMC   9288486 . PMID   35633200.
  58. ↑ Tullberg, Mats; Toma, Ahmed K.; Yamada, Shigeki; Laurell, Katarina; Miyajima, Masakazu; Watkins, Laurence D.; Wikkelsø, Carsten (2024-03-01). "Classification of Chronic Hydrocephalus in Adults: A Systematic Review and Analysis". World Neurosurgery. 183: 113–122. doi:10.1016/j.wneu.2023.12.094. ISSN   1878-8750. PMID   38143036.
  59. ↑ Cinalli, G (2019). "History of Hydrocephalus and Its Surgical Treatment". In Cinalli, Giuseppe; Özek, M. Memet; Sainte-Rose, Christian (eds.). Pediatric Hydrocephalus. Cham: Springer International Publishing. p. 3. doi:10.1007/978-3-319-27250-4. ISBN   978-3-319-27248-1. S2CID   128359318.
  60. 1 2 3 4 5 Aschoff A, Kremer P, Hashemi B, Kunze S (October 1999). "The scientific history of hydrocephalus and its treatment". Neurosurgical Review. 22 (2–3): 67–93, discussion 94–5. doi:10.1007/s101430050035. PMID   10547004. S2CID   10077885.
  61. ↑ Åhrén E (2009). Death, Modernity, and the Body: Sweden 1870-1940. Rochester, New York: University of Rochester Press. p. 53. ISBN   9781580463126.
  62. ↑ "Oilers forward Colby Cave dies after suffering brain bleed". CBC. April 11, 2020. Retrieved 4 May 2021.
  63. ↑ "Man of many tribes". Star Tribune. Archived from the original on 2013-05-20. Retrieved 2014-01-29.
  64. ↑ Somerset, p. 116[ full citation needed ]
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.