Evolution of Scientific Efforts to Define Cystometric Bladder Morphology in Neurogenic Bladder: A Narrated Review

ABSTRACT

Children with high-pressure bladders are at an increased risk of upper tract deterioration, potentially leading to chronic renal failure if not adequately managed. Regular bladder pressure monitoring is essential, especially in patients with neurogenic bladders, often resulting from spinal dysraphism. Urodynamic studies (UDSs) are the gold standard for assessing bladder pressure but are invasive, resource-intensive, and uncomfortable for patients. Over the last many decades, there have been regular attempts to characterize the morphology of the neurogenic bladder, including the classical subjective appearance of the “Christmas Tree” bladder, to objectively define the shape of the bladder via the use of height-to-width ratio. The study explores the evolution of scientific efforts to define bladder morphology in neurogenic bladder and to describe the current state of evidence regarding the correlation of the shape of the bladder with the detrusor pressures and upper tract changes in children with neurogenic bladder.

INTRODUCTION

Children with high-pressure bladders are more susceptible to upper tract deterioration, which can result in chronic renal failure if left unaddressed. Hence, regular bladder pressure monitoring is paramount in patients with neurogenic bladders. Spinal dysraphism, the most common cause of neurogenic bladder in children, mandates urodynamic testing during follow-up. In their influential study in 1981, McGuire et al. suggested that urethral leakage pressure of more than 40 cmH₂O (centimeters of water) can make it hard for the upper tract to empty appropriately, leading to hydronephrosis.[1] They studied the clinical progress of 42 children with myelodysplasia. They found that the intravesical pressure at the time of urethral leakage was 40 cmH₂O or less in 20 patients and greater than this value in 22 patients. They demonstrated that 81% of patients in the high-pressure group had ureteral dilatation on follow-up. However, in 1993, Houle et al. attempted to define the physiological volume of urine a child can store at a safe pressure. They demonstrated that 98.1% of the total bladder capacity could be stored at a detrusor pressure of less than 20 cmH₂O, and 99.9% of the physiological storage in the bladder occurs below the pressure of 30 cmH₂O.[2]

As evidenced in multiple studies, regular monitoring of bladder pressure in patients with neurogenic bladders is vital to avoid the detrimental effects of high-pressure nonphysiological bladders. Urodynamic study (UDS), an invasive and prolonged procedure, can be cumbersome for patients and medical institutions. It also requires a significant amount of time and resources, along with patient discomfort and the risk of infection. However, we lack easily accessible screening investigations to diagnose high-pressure bladders, which can help to avoid the burden of UDS. Classical teaching has focused on the morphology of the bladder to quickly identify bladders at risk of high pressures, with vertical elongation of the bladder (i.e., a tall bladder) often being utilized as an indirect marker of a high-pressure bladder. “Christmas tree bladder,” or a “pine tree bladder,” as described for neurogenic bladder, indicates a trabeculated, vertically elongated bladder. It is believed to be due to a combination of loss of bladder sensation, inability to initiate voiding, and detrusor-external sphincter dyssynergia.[3]

Similarly, researchers have focused on evaluating and quantifying the degree of bladder trabeculations in classifying bladders and identifying bladders at high risk for upper tract deterioration. The review explores the development of scientific endeavors to define bladder morphology in neurogenic bladder and to describe the current state of evidence regarding the correlation of the shape of the bladder with the detrusor pressures and upper tract changes in children with neurogenic bladder.

ANATOMICAL AND PHYSIOLOGICAL BASIS FOR THE BLADDER MORPHOLOGY

Many clinicians understand clearly that the shape of the bladder changes over time in children with neurogenic bladder and they often end up with a “pine tree” or “Christmas tree” appearance. However, the cause of the change, namely the anatomical and physiological basis of the change, is often obscure and unclear. The bladder can be smooth-walled or irregular-walled due to trabeculation, saccules, and diverticula. Due to a progressive decrease in compliance and raised bladder outlet pressure in the neurogenic bladder, it becomes taller, with a broad base and tapering toward the dome. This typical shape often occurs due to the morphology of the bladder muscle. The bladder has layers of the detrusor muscles arranged longitudinally in the innermost layer, circularly in the middle layer, and longitudinally in the outermost layer. It is believed that this middle layer of circular muscles constricts the globe-like bladder, leading to a vertical elongation. A few previous studies have shown changes in the detrusor smooth muscle and extracellular matrix with a high-pressure bladder, resulting in changes in morphology. Haferkamp et al., in a large and unique study analyzing the anatomical and histological basis of neurogenic bladder, found that intermediate junctions of detrusor muscle cells were absent or reduced, which instead had dominant intimate cell appositions with much narrower junctional gaps. These detrusor cells had associated muscle cell degeneration, leading to poor contractility in the majority of patients with neurogenic bladder.[4]

REVIEW AND DISCUSSION OF BLADDER MORPHOLOGY

Our review of the literature to correlate the morphology of the bladder in neurogenic bladder yielded just a handful of studies. The studies mainly focused on two different areas of the morphology of the bladder: the degree of bladder trabeculations as a measure of bladder pressure and the degree of bladder deformity.

The current state of evaluation of bladder morphology in neurogenic bladder is as follows:

1. Evaluation of bladder morphology

   1. Subjective appearance of the bladder in neurogenic bladder

   2. Objective measurements of the shape of the bladder and its correlation with bladder pressures in neurogenic bladder.

2. Degree of bladder trabeculations as a measure of bladder/detrusor pressures.

The evolution of defining the bladder morphology in neurogenic bladder progressed from defining the subjective appearance of the bladder to partially objective measures of bladder trabeculations to a more objective measure of defining the shape of the bladder in the form of height to width ratio and its correlation with detrusor pressures. The literature regarding the bladder morphology in children with neurogenic bladder can be stratified into three distinct stages:

1. Initial attempts from 1960 to 2007 – Subjective description of bladder morphology

2. Subsequent attempts from 2007 to 2020 – Addition of grade of bladder trabeculations or closed bladder neck to bladder morphology

3. Current attempts from 2020 onward – Objective measurements of bladder morphology and its correlation with detrusor pressures.

INITIAL SUBJECTIVE DESCRIPTION OF BLADDER MORPHOLOGY ON CYSTOGRAM (1960-2007)

In one of the initial and early attempts at defining bladder morphology, Friedenberg and Ney, in a study of 50 patients with neurogenic bladder in 1960, performed a detailed analysis of bladder morphology and described the radiographic findings of neurogenic bladder.[5] Using a cystourethrogram, they focused on bladder deformity in patients with neurogenic bladders. They explained various morphological patterns of the bladder, including large atonic bladder, “hourglass” deformity, “pine tree bladder,” and severely contracted bladder, along with others, and shared typical cystographic images of each type. They described the radiographic findings in the neurogenic bladder and detailed the spectrum of morphological change as follows [Figure 1]:

Figure 1.

The morphological pattern described by Friedenberg and Ney in neurogenic bladder[5]

1. Large atonic bladder

2. “Hourglass” deformity of the bladder

3. Pine-shaped bladder

4. Severely contracted hypertonic bladder.

Apart from the shape of the bladder, the authors also described the shape of the urethra as varying from a funnel-shaped urethra to a saccular dilatation of the urethra, along with the status of the bladder neck with a spastic external sphincter. This was one of the initial attempts to subjectively define bladder morphology based on descriptive terms with no attempt to make it an objective system.

It was in 1991 that the initial attempts to correlate the bladder morphology with the severity of the neurogenic bladder were demonstrated. Ogawa, in his study, evaluated bladder deformity in patients with neurogenic bladder dysfunction and studied 231 patients.[6] He correlated the shape and morphology of the bladder with the degree of upper tract damage. He described a measure of the severity of bladder deformity based on the incidence of upper tract deterioration. They subjectively classified the bladder deformity in cystogram images into mild, moderate, and severe and correlated it with upper tract deterioration [Figure 2]. The moderate (Grade II) and severely deformed bladders (Grade III) had the classical appearance of a tall, vertically elongated bladder. He demonstrated that only 8% of children with Grade 1 bladder deformity had upper tract deterioration, while 52% and 62% of children with Grade II and Grade III, respectively, had upper tract deterioration. However, although the authors objectively attempted to correlate the deformity with clinical results, the grading system, at its heart, relied mainly on the subjective appearance of bladder deformity.[6]

Figure 2.

Grading of bladder deformity as described by Ogawa[6]

SUBSEQUENT ADDITION OF GRADE OF BLADDER TRABECULATIONS/CLOSED BLADDER NECK TO BLADDER MORPHOLOGY (2007-2020)

A study by Khoury et al. (2008) attempted to utilize the degree of bladder trabeculation as a gauge of outlet resistance.[7] They took it into account when deciding on a surgical procedure to enhance the neurogenic bladder and address incontinence. They graded the bladder trabeculation as mild and severe but used no objective method to describe the degree of trabeculation. However, the presence of severe trabeculation in incontinent neurogenic bladder indicated high intrinsic outlet resistance without any objective measure to assess the bladder pressure.[7]

Khoury’s definition of trabeculation into mild and severe was a broad and ephemeral definition which depended upon the judgment of the person doing the grading and is depicted in Figure 3.[7] Selby et al. attempted to make a more scientific and objective system with better inter-rater reliability.[8] Selby et al. established a grading system for trabeculation and validated it in an attempt to describe the neurogenic bladder based on its morphology.[8] They developed three grades of trabeculation using psychometric scientific methodology, which had good intra-rater reliability. A panel with eight reviewers agreed upon the grading of the bladder trabeculation into three grades. Grade 0 is a bladder with a smooth wall, Grade 1 is a bladder with wall showing shallow cellules, or diverticula, or saccules without necks, and Grade 2 is a bladder which demonstrates deep cellules, or diverticula, or saccules with necks [Figure 4]. However, the study did not correlate the grades of trabeculation with bladder pressure.[8] This was one of the first attempts to grade the bladder morphology objectively and attempted to give an implicit definition for an inherently subjective measure like trabeculations.

Figure 3.

Classification of trabeculation into mild and severe by Khoury et al.[7]

Figure 4.

Grading of bladder trabeculation as given by Selby et al.[8]

Ghanem et al., in 2013, attempted to correlate bladder neck morphology (closed vs. open bladder neck) in patients of myelodysplasia following augmentation cystoplasty. They found that an open bladder neck was associated with urinary incontinence in their cohort. However, this study was on a very specific cohort of patients of neurogenic bladder after augmentation with ileocystoplasty.[9]

Despite multiple studies trying to establish objective methods to define trabeculation and the degree of bladder deformity, it is still inherently subjective. There was still a pressing need to develop objective measures to define bladder morphology in children with neurogenic bladder and to actually correlate the changes in bladder morphology with the detrusor pressures and upper tract deteriorations.

CURRENT PHASE OF OBJECTIVE MEASUREMENTS OF BLADDER MORPHOLOGY AND ITS CORRELATION WITH DETRUSOR PRESSURES (2020 ONWARD)

A method of measuring the height and width of the bladder at the maximum cystometric capacity (MCC) and taking the ratio of them can be an alternative objective measure of bladder deformity. Since the neurogenic bladder tends to be vertically elongated, such a ratio can better define the deformity. A literature review suggested that two studies were done about the objective measurement of bladder deformity using the height-to-width ratio (HWR) of the bladder in children with neurogenic bladder. Kumano et al. in 2020 and Aithal et al. in 2024 demonstrated that the HWR of the bladder at MCC can be used as a screening tool to identify the high-pressure bladder.[10,11] The taller the bladder, the higher the HWR and higher the detrusor pressure. This finding objectively defines the vertically elongated tall bladder in the neurogenic bladder and correlates it with bladder pressures.

Kumano et al.’s study revealed a significantly higher HWR for children with high-pressure bladders (MDP >40 cmH₂O). They studied the video urodynamic studies of 81 myelomeningocele patients and found an HWR of 1.5 in children with high-pressure bladder. HWR was 1.37 in children with low-pressure bladder and was statistically significant (P = 0.004). Kumano et al. suggested that with a cutoff of 1.4, HWR had a sensitivity of 87% and a specificity of 56.9% to identify the high-pressure bladder[10] [Table 1]. The study defined an objective measure to define the morphology and supports the age-old description of the “Christmas tree bladder” as a neurogenic bladder.

Table 1.

Comparing the two studies describing height-to-width ratio of the bladder in cystogram and correlating with the bladder pressure

	High pressure (cmH2O)	HWR in high-pressure bladder	HWR in low-pressure bladder	Cut off HWR to detect high-pressure bladder
Kumano Y et al.[9]	>40	1.5	1.37	1.4
Aithal S et al.[10]	>30	1.55	1.26	1.3

HWR: Height-to-width ratio

However, the morphological changes in a high-pressure bladder can take time to appear, potentially delaying the diagnosis of the condition. Hence, it is necessary to identify abnormal pressure of the bladder earlier so that appropriate treatment can be initiated. In an attempt by Aithal et al., the authors tried to clarify whether the HWR could be correlated with nonphysiological bladder pressures (>30 cmH₂O).[2,11] They tried to identify the morphological changes in the bladder when the storage pressure is in a nonphysiological range (>30 cmH2O) [Figure 5]. In a population of 53 patients with neurogenic bladder secondary to spinal dysraphism, 24 patients (45.3%) had nonphysiological bladder pressure. The mean value of HWR among the patients with nonphysiological pressure was 1.55 and among the children with physiological pressure was 1.26. HWR, with a cutoff value of 1.3, had a sensitivity of 87.5% and a specificity of 48.28% in identifying bladders with nonphysiological pressure (>30 cmH₂O) [Table 1]. Hence, the authors suggested that a simple measure of the HWR of the bladder at the MCC can be used as an objective measure and a screening tool to diagnose a high-pressure bladder. A bladder with a height 30% longer than its width is a simple, easily reproducible measure that can be employed whenever we look at a cystogram. However, performing a UDS is mandatory to confirm the bladder pressure.[11]

Figure 5.

Demonstration of measurement of height-to-width ratio by Aithal et al.[11]

Thus, the morphological study of the bladder in children with neurogenic bladder has evolved over the last 50 years. It started with simple descriptive nomenclature of the shape of the bladder. Subsequently, the shape of the bladder was correlated with an increased risk of upper tract damage. To add some measure of objectivity to an inherently subjective classification, grading of bladder trabeculations was added to the morphological description of the bladder over the last 20 years. In the last 5 years, objective measurements of the HWR of the bladder defined the neurogenic bladder have been studied, and it could be directly correlated with higher detrusor pressures, which appears to be an extremely promising measure for screening for bladders which are at risk of upper tract damage.

CONCLUSION

Early identification of high bladder pressure in children with neurogenic bladder is required to initiate appropriate therapeutic measures. Delay in diagnosis and treatment can lead to upper tract deterioration and land children with chronic kidney disease earlier. In children who are prone to developing neurogenic bladder including those operated on for spinal dysraphism, earlier diagnosis of nonphysiological bladder storage pressure can help initiate appropriate measures. This review demonstrated the evolution of the scientific efforts to define the morphology of the neurogenic bladder over the last 50 years. It has evolved from the simple subjective description of morphology to partially objective measures like grading of bladder trabeculations to more concrete objective measures of bladder morphology. A simple measure of a tall bladder (HWR) can be an objective measure and a screening tool to identify bladders with high storage pressures.

Conflicts of interest

There are no conflicts of interest.

Funding Statement

Nil.