Application of clean intermittent catheterization for neurogenic bladder in infants less than 1 year old

Abstract

BACKGROUND:

Neurogenic bladder (NB) is a common pediatric urological disease caused by a variety of neurological pathologies. Clean intermittent catheterization (CIC) has been the preferred method to empty bladder.

OBJECTIVE:

To investigate the effect of CIC on preserving bladder and upper urinary tract function in infants less than 1 year old with NB.

METHODS:

A retrospective analysis was conducted on 76 infants with NB. Patients were divided into two groups according to treatment initiation: the early CIC group (ECG) (<1 year old) and the late CIC group (LCG) (>3 years old).

RESULTS:

Bladder compliance (BC), safe bladder capacity (SBC) and maximum cystometric capacity (MCC) were significantly higher in the ECG than those in the LCG at 6 years of follow-up respectively (P < 0.05). The frequencies of vesicoureteral reflux (VUR) and urinary tract infection (UTI) in the ECG were significantly lower than those in the LCG (P < 0.05) at 6 years of follow-up. Two and nine patients exhibited mild renal damage in the ECG and LCG, respectively, resulting in a significant difference (P < 0.05) at 6 years of follow-up.

CONCLUSION:

Early CIC plays an important role in preserving bladder function and preventing UTI and renal deterioration in infants with NB, especially in the first year of life.

Keywords

Neurogenic bladder clean intermittent catheterization infants

1 Introduction

Neurogenic bladder (NB) is a common pediatric urological disease caused by a variety of neurological pathologies, such as spina bifida, sacral dysplasia, tethered cord, and spinal cord injury, that are difficult to cure (Liao, 2015). Normal voiding is achieved by a voluntary, continuous detrusor contraction that leads to complete emptying of the bladder within an acceptable time span. However, the main pathophysiological basis of NB includes detrusor underactivity, resulting in increased bladder post-voiding residual (PVR) volume and filling pressure. Consequently, vesicoureteral reflux (VUR) and renal damage might occur. Many patients are treated irregularly, which causes renal dysfunction (Sturm & Cheng, 2016). Up to one-third of children with NB have VUR (Sidi, Peng, & Gonzalez, 1986). Therefore, emptying the bladder in time is especially important for children with NB, because it can prevent VUR, urinary tract infection (UTI) and renal damage.

In 1947, Guttmann et al. (1947) reported that sterile intermittent catheterization could be applied in patients with spinal cord injuries to empty the bladder and decrease the risk of UTI. Lapides et al. (1974) introduced clean intermittent catheterization (CIC), which kept intermittent catheterization clean and would not increase the risk of UTI compared to sterile intermittent catheterization because they believed that UTIs were caused by bladder overexpansion leading to decreased bladder blood flow. Later, Lapides published more papers, proposing that the frequency of catheterization was more important than sterilization. Since 1971, CIC has been widespread use as a method to empty the bladder (Frimberger, Cheng, & Kropp, 2012). CIC is now recommended by the International Continence Society (ICS) as the first choice to treat NB with bladder retention because it can effectively reduce PVR, decrease UTIs, prevent or alleviate VUR, preserve renal function and improve the quality of life (Abrams et al., 2003). Although CIC is the standard procedure to treat NB, few studies have been performed to observe the long-term results of patients, especially infants, with NB (Frimberger et al., 2012; Newman & Willson, 2011).

Furthermore, when to begin CIC use in infants and children is still controversial (Kryger, 2008). CIC has been generally used in older children but rarely in infants. Most infants with NB are diagnosed early in life, but the fear of increased numbers of UTIs and urethral injury leads to the avoidance of early CIC in infants. Controversially, Di (2011) believed that older children or adults are more likely to accept this therapy due to their more developed cognitive abilities.

Kryger (2008) recommended CIC use as soon as NB with increased PVR volume is diagnosed. Guerra et al. (2014) believed that parents and children have longer periods to adapt when CIC is used in infancy because it maintains moderate bladder wall thickness and increases bladder compliance. Kochakarn et al. (2004) evaluated the long-term results of early CIC application and noted that upper urinary tract complications were decreased and renal function was improved in patients with NB. However, the urodynamic parameters of these cases were not recorded, resulting in a lack of an objective bladder function assessment. Therefore, to further study the improvement or conservation of bladder function by early CIC, recording the bladder urodynamic parameters is necessary to identify the long-term treatment response. The aim of the present study is to determine whether it is more beneficial to apply CIC when infants with NB are less than 1 year old or are older than 3 years old by assessing the treatment response with regard to bladder function evaluated by urodynamics, renal function, and related urinary tract complications.

2 Methods

2.1 Design

A retrospective analysis was conducted on 92 infants aged less than 1 year with NB diagnosed by an urodynamic study and neurological examinations in our hospital. The study was approved by the Hospital Medical Ethics Committee and conducted in accordance with the 1983 Declaration of Helsinki. Written informed consent was obtained from the parents of all patients. All responses were confidential and did not affect the subsequent treatment of the patients.

2.2 Subject selection

All parameters were recorded and analyzed after obtaining a comprehensive medical history including complaints, physical and neurological examination results, urinary ultrasound, intravenous pyelography (IVP), urine culture, and video urodynamic evaluations.

Inclusion criteria: (1) dysuria and incomplete emptying (increased PVR volume) confirmed by ultrasound; (2) increased bladder filling pressure with poor compliance; and (3) less than 1 year old at treatment initiation. All patients fulfilled these criteria; 14 patients had VUR.

Exclusion criteria: (1) UTI with fever; (2) history of severe urethral trauma; (3) obstructive diseases of the lower urinary tract; and (4) hydronephrosis, abnormal renal function or urinary malformation.

A total of 92 children underwent CIC; 76 were successfully followed up for six years. Forty patients began CIC before the age of 1 year, and 36 patients began after the age of 3 years. Late CIC was mainly the result of concerns of parents regarding damage to the urethra and increasing the risk of UTI. Consequently, these cases were divided into an early CIC group (ECG) (children who were less than 1 year old) and a late CIC group (LCG) (children who were more than 3 years old) according to CIC initiation. Among ECG patients aged 5–11 months (24 boys and 16 girls with a mean age of 8.28±1.83 months), 6 patients suffered from spina bifida manifesta, 28 patients had spina bifida occulta, 5 patients had sacral dysplasia, and 1 patient had meningitis. In this group, a total of 8 patients presented with grade I VUR, and 1 patient presented with grade II VUR when starting CIC. Bacteriuria was identified in 9 patients. The LCG included 36 patients aged 6–11 months (21 boys and 15 girls with a mean age of 8.56±1.35 months) at the time of treatment; 2 patients were suffering from spina bifida manifesta, 29 patients had spina bifida occulta, 4 patients had sacral dysplasia, and 1 patient had undergone pelvic surgery. In this group, a total of 5 patients had grade I VUR; 6 patients presented bacteriuria at the time of treatment.

2.3 Methods

It is routine to instruct parents to record information in the catheterization diary, such as recording the time, the number of times and the amount of water intake (including all liquid intake), the time and urine volume of each catheterization, the time interval between catheterizations, and urine leakage. All patients could adjust the amount of water intake according to the urine volume to prevent a UTI. It was suggested that each patient perform catheterization 4–8 times a day according to an evaluation of the voiding situation. The late treatment group used Crede’s method or Valsalva’s maneuver to assist voiding before performing CIC. Children with NB began to learn to perform the CIC technique from their parents after age 6, when they had increased cognitive and practical abilities. Noninvasive urodynamic studies (included uroflowmetry, voiding or catheterization diary, and measurement of PVR) were performed to evaluate the bladder capacity and PVR every 3 months. Invasive urodynamic examinations (included pressure-flow study and video urodynamics) were performed every 6–12 months according to the patient’s condition. Combined with the amount of water intake and the urine volume, adjustment of the catheterization interval was important to empty the bladder before reaching a SBC.

2.4 Urodynamic examination

Urodynamic testing was conducted by applying a Solar Silver (MMS International, Enschede, The Netherlands) in accordance with the ICS protocol (Schafer et al., 2002). All urodynamic parameters and symptoms are described using standardized ICS terminology. A pressure-flow study and video urodynamics analysis were performed according to a comprehensive history analysis. A glycerin enema was used to empty the rectum before testing. A 6-Fr double-lumen catheter was inserted transurethrally using lubricant or anesthetic gel. An 8-Fr feeding tube or a small rectal balloon catheter was inserted transrectally to record abdominal pressure changes. Bladder compliance (BC), maximum cystometric capacity (MCC) and SBC were recorded before and after CIC. Knowledge of normal voiding parameters as well as following ICS recommendations is important for successful testing and understanding the findings of cystometry. The expected capacity (ml) = 30+ (age in years×30) in a child >1 year old. For infants <1 year old, expected capacity (ml) = 38 + 2.5×age (months) (Martinez-Garcia, Ubeda-Sansano, Diez-Domingo, Perez-Hoyos, & Gil-Salom, 2014). The BC measures the elastic properties of the bladder; less than 10 ml/cm of H₂O indicates decreased BC, which may be the result of decreased bladder capacity, increased detrusor pressure or both.

We compared the BC, SBC, MCC, PVR, serum creatinine, and blood urea nitrogen (BUN) levels, and the frequency of UTI and VUR between the two groups after 3 years and 6 years of follow-up.

2.5 Statistical analyses

The measurement data were analyzed by a t test and expressed as the mean±SD. The differences between rates were analyzed by a Chi-square test or Fisher’s exact test, as appropriate. P values < 0.05 were considered statistically significant. SPSS version 21 for Windows (SPSS Inc., Chicago, IL, USA) was used to process all statistical analyses.

3 Results

The BC, SBC and MCC in the ECG were significantly higher than those in the LCG at 3 and 6 years of follow-up (Table 1). At 3 years of follow-up, increased BUN or serum creatinine levels were observed in 1 patients (2.5%) in the ECG and 7 patients (19.4%) in the LCG, resulting in a significant difference between the two groups (P < 0.05). Six patients (15.0%) in the ECG and 14 patients (38.9%) in the LCG had UTIs at 3 years of follow-up, resulting in a significant difference between the two groups (P < 0.05). At 6 years of follow-up, 2 patients (5.0%) with increased BUN or serum creatinine levels in the ECG and 9 patients (25.0%) in the LCG were identified, resulting in a significant difference between the two groups (P < 0.05). UTIs were found in 10 patients (25.0%) in the ECG and 19 patients (52.8%) in the LCG, resulting a significant difference between the two groups (P < 0.05) (Table 2). At 6 years of follow-up in the ECG, the grade I reflux that was observed in 6 patients (15%) was resolved; 28 patients (70.0%) remained stable (27 with no reflux and 1 with grade I); 1 patient (2.5%) with grade II decreased to grade I; and reflux in 4 patients (10.0%) was aggravated (3 with no reflux and 1 with grade I). In the LCG, resolution of reflux occurred in one grade I case (2.8%); 21 patients (58.3%) remained unchanged (20 with no reflux and 1 with grade I); and reflux was exacerbated in 14 patients (38.9%) (11 with no reflux and 3 with grade I) (Tables 2, 3).

Table 1
Urodynamic parameters (BC, SBC, MCC) in the two groups during follow-up

ECG LCG t value P value

BC (ml/cmH₂O)

At the first visit 2.43±0.91 2.46±0.59 –0.234 0.815

After 3 years 5.74±2.02 3.81±0.73 5.672 <0.001

After 6 years 8.71±2.27 5.91±1.17 6.858 <0.001

SBC (ml)

At the first visit 46.10±5.17 47.83±2.29 –1.921 0.060

After 3 years 108.75±13.38 93.61±15.97 4.493 <0.001

After 6 years 206.15±20.27 182.47±19.78 5.143 <0.001

MCC (ml)

At the first visit 51.28±4.47 52.17±3.60 –0.952 0.344

After 3 years 121.45±9.99 113.22±8.99 3.757 <0.001

After 6 years 216.90±12.86 205.58±9.47 4.397 <0.001

	ECG	LCG	t value	P value
BC (ml/cmH₂O)
At the first visit	2.43±0.91	2.46±0.59	–0.234	0.815
After 3 years	5.74±2.02	3.81±0.73	5.672	<0.001
After 6 years	8.71±2.27	5.91±1.17	6.858	<0.001
SBC (ml)
At the first visit	46.10±5.17	47.83±2.29	–1.921	0.060
After 3 years	108.75±13.38	93.61±15.97	4.493	<0.001
After 6 years	206.15±20.27	182.47±19.78	5.143	<0.001
MCC (ml)
At the first visit	51.28±4.47	52.17±3.60	–0.952	0.344
After 3 years	121.45±9.99	113.22±8.99	3.757	<0.001
After 6 years	216.90±12.86	205.58±9.47	4.397	<0.001

Urodynamic parameters were compared by t tests. ECG: early clean intermittent catheterization group; LCG: late clean intermittent catheterization group; BC: bladder compliance; SBC: safe bladder capacity; MCC: maximum cystometric capacity.

Table 2

VUR and UTI in 76 children with neurogenic bladder during follow-up

	n	Number of patients with VUR	χ ²	P value	_{Numbersof UTIs}	χ ²	P value
At the first visit
ECG	40	9 (22.5%)	0.450	0.503	5(12.5%)	0.036	0.850
LCG	36	5(13.9%)			6(11.1%)
After 3 years
ECG	40	8(20.0%)	6.302	0.012	6(15.0%)	4.155	0.041
LCG	36	18(50.0%)			14(38.9%)
After 6 years
ECG	40	7(17.5%)	4.269	0.039	10(25.0%)	5.074	0.024
LCG	36	15(41.7%)			19(52.8%)

Comparison of rates between the two groups using a Chi-square test. VUR: vesicoureteral reflux; UTI: urinary tract infection.

Table 3

Comparison of vesicoureteral reflux grade in the two groups during follow-up

	n	Grade I	Grade II	Grade III	Total
At the first visit
ECG	40	8 (20.0%)	1(2.5%)	0	9(22.5%)
LCG	36	5(13.9%)	0	0	5(13.9%)
After 3 years
ECG	40	8 (20.0%)	0	0	8 (20.0%)
LCG	36	10(27.8%)	5(13.9%)	3(8.3%)	18(50.0%)
After 6 years
ECG	40	5(12.5%)	2(5.0%)	0	7(17.5%)
LCG	36	7(19.4%)	4(11.1%)	4(11.1%)	15(41.7%)

4 Discussion

CIC has been the preferred method recommended by the ICS to empty bladder (Seth, Haslam, & Panicker, 2014). Joseph et al. (1989) reported that infants less than 1 year old could undergo CIC with good effects. Parents can help infants perform CIC after training.

The literature is limited regarding the long-term follow-up of early CIC in NB patients less than 1 year old. Joseph et al. (1989) found that 89% of patients had a stable upper urinary tract, 42% of patients had bacteriuria, no patients had been hospitalized because of UTI, and no further complications were identified after examining 38 patients with long-term CIC use. Guys et al. (2011) noted that children with NB initiate catheterization without age restriction. Recently, Larijani et al. (2013) highlighted that all infants with NB should undergo catheterization in principle to maintain safe bladder pressure. Wu et al. (1997) compared the effect in 98 patients of different ages without upper urinary tract dilatation after CIC application; they found that, after CIC, fewer young children required cystoplasty than older children. Early catheterization reduced the risk of irreversible harm to the bladder. Most of these studies discussed the effect of early and late catheterization on upper urinary tract complications and kidney function but lacked follow-up regarding urodynamic parameters and bladder function. In the present study, urodynamic parameters, bladder function, urinary tract complications and kidney function were all followed up and analyzed. This study demonstrated that urodynamic parameters, including BC, SBC, and MCC, in the ECG were significantly better than those in the LCG at 3 years of follow-up, indicating that bladder function exhibits a good response to CIC. At 6 years of follow-up, the three urodynamic parameters were also significantly better in the ECG than those in the LCG, showing that bladder function is improved if CIC is used before the age of 1 year. Although bladder function is still decreased compared to normal children, early CIC application can obviously reduce the gap and improve bladder function.

Edelstein et al. (1995) compared the effects between early and late treatment in patients with upper urinary tract dilatation and found that 80% of the patients in the late treatment group had progressive renal injury, whereas only 15% had kidney damage in the early treatment group. Their studies lacked patients with a normal upper urinary tract. We chose both normal upper urinary tract and VUR patients to follow up and to record their bladder and renal functions. The study suggested that more children had VUR in the LCG than that in the ECG at 3 years of follow-up; the numbers of patients with increased BUN or serum creatinine levels were significantly different between the two groups. At 6 years of follow-up, the numbers of patients with VUR, increased BUN or serum creatinine levels in the ECG were obviously lower than those in the LCG. The bladders of children in the LCG had a high-pressure status for a long time, leading to ischemia of the bladder wall and fibrosis of the bladder, causing decreases in BC and damage to the bladder contraction function. However, children in the ECG could empty their bladders in time to protect bladder function and prevent upper urinary tract damage. However, some of the early CIC patients also had elevated VUR, BUN or serum creatinine levels as a result of a long catheterization interval that caused high bladder filling pressure. Mcguire et al. (1981, 1983) suggested that persistent intravesical filling pressures of more than 40 cmH₂O are damaging the upper urinary tract. Consequently, the catheterization time interval is critical for the effect of CIC. The catheterization interval was determined according to the safe bladder pressure and residual urine volume. CIC needs to be performed before bladder filling pressure exceeds 40 cmH₂O to minimize the risk of upper urinary damage. The liquid intake of children with NB will directly affect urine volume and catheterization times. Therefore, an appropriate amount and regular water intake is particularly important for the results of CIC. Furthermore, patients can adjust the catheterization time according to the catheterization volume (Nazarko, 2012). If the frequency of catheterization is too high and the interval time is short, excessive bladder filling is avoided, but the patient’s inconvenience and risk of the urinary tract injury will be increased. However, if the amount of catheterization is not sufficient, the risk of UTI is elevated as a result of the increasing residual urine volume.

The most common complication of CIC is UTI, which will exhibit increased incidence due to destruction of the delicate urethra of infants (Chaudhry et al., 2017; Forster, Haslam, Jackson, & Goldstein, 2017; Wyndaele et al., 2012). In addition, the presence of residual urine or VUR in children with NB may also contribute to UTI. Kochakarn et al. (2004) compared the long-term results between an early CIC group (<3 years old) and a late CIC group (>3 years old). They found no significant difference regarding UTIs between the two groups. Joseph et al. (1989) believed that bacteriuria was frequently present but easy to cure and did not cause sequela in CIC of infants. This research showed that the incidence of UTI in the ECG was significantly lower than that in the LCG at 3 and 6 years of follow-up, indicating that early application of CIC reduces the incidence of UTI as a result of decreasing PVR volume and upper urinary tract complications.

5 Conclusion

In summary, we believe that CIC is an appropriate alternative for children with NB who need to empty their bladders within a specific time. Furthermore, early CIC greatly improved bladder function and prevented UTI and upper urinary tract function impairment in infants with NB who were less than 1 year old. At the same time, the incidence of UTI decreased with the early application of CIC. However, further research with a larger number of cases and with longer follow-up is needed to investigate the effect of early CIC. Unfortunately, insufficient attention has been focused on increasing the use of CIC in China. We advocate that children with NB who meet the CIC criteria should be recommended to utilize CIC as soon as possible, especially in the first year of life, to improve their quality of life and lighten the burden on the family.

Conflict of interest

The authors declare no conflict of interest.

Footnotes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant No. 81670689).

References

Abrams

, Cardozo

, Fall

, Griffiths

, Rosier

, & Ulmsten

(2003). Standardisation Sub-Committee of the International Continence, S. The standardisation of terminology in lower urinary tract function: Report from the standardisation sub-committee of the International Continence Society. Urology, 61 (1), 37–49.

Chaudhry

, Balsara

Z. R.

, Madden-Fuentes

R. J.

, Wiener

J. S.

, Routh

J. C.

, Seed

, & Ross

S. S.

(2017). Risk Factors Associated With Recurrent Urinary Tract Infection in Neurogenic Bladders Managed by Clean Intermittent Catheterization. Urology, 102, 213–218. doi:10.1016/j.urology.2016.12.049

Di Benedetto

(2011). Clean intermittent self-catheterization in neuro-urology. Eur J Phys Rehabil Med, 47 (4), 651–659.

Edelstein

R.A.

, Bauer

S. B.

, Kelly

M. D.

, Darbey

M. M.

, Peters

C. A.

, Atala

, & Retik

A. B.

(1995). The long-term urological response of neonates with myelodysplasia treated proactively with intermittent catheterization and anticholinergic therapy. J Urol, 154 (4), 1500–1504.

Forster

C.S.

, Haslam

D. B.

, Jackson

, & Goldstein

S. L.

(2017). Utility of a routine urinalysis in children who require clean intermittent catheterization. J Pediatr Urol. doi:10.1016/j.jpurol.2017.01.016

Frimberger

, Cheng

, & Kropp

B. P.

(2012). The current management of the neurogenic bladder in children with spina bifida. Pediatr Clin North Am, 59 (4), 757–767. doi:s10.1016/j.pcl.2012.05.006

Guerra

, Leonard

, & Castagnetti

(2014). Best practice in the assessment of bladder function in infants. Ther Adv Urol, 6 (4), 148–164. doi:10.1177/1756287214528745

Guttmann

, Riches

E.W.

, Whitteridge

, & Jonason

P. H. A.

(1947). Discussion on the Treatment and Prognosis of Traumatic Paraplegia. Proc R Soc Med, 40 (5), 219–232.

Guys

J.M.

, Hery

, Haddad

, & Borrionne

(2011). Neurogenic bladder in children: Basic principles, new therapeutic trends. Scand J Surg, 100 (4), 256–263. doi:10.1177/145749691110000405

10.

Joseph

D.B.

, Bauer

S. B.

, Colodny

A. H.

, Mandell

, & Retik

A. B.

(1989). Clean, intermittent catheterization of infants with neurogenic bladder. Pediatrics, 84 (1), 78–82.

11.

Kochakarn

, Ratana-Olarn

, Lertsithichai

, & Roongreungsilp

(2004). Follow-up of long-term treatment with clean intermittent catheterization for neurogenic bladder in children. Asian J Surg, 27 (2), 134–136. doi:10.1016/S1015-9584(09)60327-4

12.

Kryger

(2008). Nonsurgical management of the neurogenic bladder in children. ScientificWorldJournal, 8, 1177–1186. doi:10.1100/tsw.2008.146

13.

Lapides

, Diokno

A.C.

, Lowe

B. S.

, & Kalish

M. D.

(1974). Followup on unsterile intermittent self-catheterization. J Urol, 111 (2), 184–187.

14.

Larijani

F.J.

, Moghtaderi

, Hajizadeh

, & Assadi

(2013). Preventing kidney injury in children with neurogenic bladder dysfunction. Int J Prev Med, 4 (12), 1359–1364.

15.

Liao

(2015). Evaluation and Management of Neurogenic Bladder: What Is New in China? Int J Mol Sci, 16 (8), 18580–18600.

16.

Martinez-Garcia

, Ubeda-Sansano

M.I.

, Diez-Domingo

, Perez-Hoyos

, & Gil-Salom

(2014). It is time to abandon “expected bladder capacity.” Systematic review and new models for children’s normal maximum voided volumes. Neurourol Urodyn, 33 (7), 1092–1098. doi:10.1002/nau.22452

17.

McGuire

E.J,

, Woodside

J. R.

, & Borden

T. A.

(1983). Upper urinary tract deterioration in patients with myelodysplasia and detrusor hypertonia: A followup study. J Urol, 129 (4), 823–826.

18.

McGuire

E.J.

, Woodside

J. R.

, Borden

T. A.

, & Weiss

R. M.

(1981). Prognostic value of urodynamic testing in myelodysplastic patients. J Urol, 126 (2), 205–209.

19.

Nazarko

(2012). Intermittent self-catheterisation: Past, present and future. Br J Community Nurs, 17 (9), 408, 410–412. doi:10.12968/bjcn.2012.17.9.408

20.

Newman

D.K.

, & Willson

M. M.

(2011). Review of intermittent catheterization and current best practices. Urol Nurs, 31 (1), 12–28, 48; quiz 29.

21.

Schafer

, Abrams

. Liao

, Mattiasson

, Pesce

, Spangberg

, International Continence, S. (2002). Good urodynamic practices: Uroflowmetry, filling cystometry, and pressure-flow studies. Neurourol Urodyn, 21 (3), 261–274.

22.

Seth

J.H.

, Haslam

, & Panicker

J. N.

(2014). Ensuring patient adherence to clean intermittent self-catheterization. Patient Prefer Adherence, 8, 191–198. doi:10.2147/PPA.S49060

23.

Sidi

A.A.

, Peng

, & Gonzalez

(1986). Vesicoureteral reflux in children with myelodysplasia: Natural history and results of treatment. J Urol, 136 (1 Pt 2), 329–331.

24.

Sturm

R.M.

, & Cheng

E. Y.

(2016). The Management of the Pediatric Neurogenic Bladder. Curr Bladder Dysfunct Rep, 11, 225–233. doi:10.1007/s11884-016-0371-6

25.

, Baskin

, Kogan

. (1997). Neurogenic bladder dysfunction due to myelomeningocele: Neonatal versus childhood treatment. J Urol, 157 (6), 2295–2297.

26.

Wyndaele

J.J.

, Brauner

, Geerlings

S. E.

, Bela

, Peter

, & Bjerklund-Johanson

T. E.

(2012). Clean intermittent catheterization and urinary tract infection: Review and guide for future research. BJU Int, 110 (11 Pt C), E910–917, doi:10.1111/j.1464-410X.2012.11549.x