Early postnatal bladder function in fetoscopic myelomeningocele repair patients

Abstract

PURPOSE:

Prenatal repair of myelomeningocele (MMC) via hysterotomy has demonstrated neurosurgical and motor benefits, when compared to postnatal repairs. Urologic benefits, however, remain to be seen. The purpose of this study was to review early postnatal bladder function in patients undergoing a novel endoscopic approach for MMC repair using an exteriorized uterus.

METHODS:

A prospective urologic assessment of patients undergoing fetoscopic MMC repair and receiving subsequent care at our facility, was performed. Patients were managed and urodynamic studies risk-stratified according to the Centers for Disease Control and Prevention Urologic and Renal Protocol for the Newborn and Young Child with Spina Bifida.

RESULTS:

Fetoscopic MMC repair was performed in 14 patients. No patients had hydronephrosis or bladder thickening at birth. Detrusor overactivity was observed in nine (64.3%) patients. Impaired compliance was seen in eight (57.1%) patients. No patients had a detrusor leak point pressure of $>$ 40 cm H ${}_{2}$ O or evidence of detrusor sphincter dyssynergia. Three (21.4%) patients had vesicoureteral reflux, seven (50.0%) had an open bladder neck, and none had trabeculated bladders.

CONCLUSION:

In this early experience with fetoscopic MMC repair, postnatal bladder function does not appear to be any worse than that of previously reported prenatal or postnatal closures.

Keywords

Neural tube defects spinal dysraphism neurogenic urinary bladder urodynamics

1. Introduction

Myelomeningocele (MMC), or open spina bifida, is a neural tube defect that results in the herniation of the spinal cord and meninges through unclosed vertebrae [1]. Patients born with this defect exhibit a wide gamut of lifelong disabilities involving the neurologic, gastrointestinal, urologic, and orthopedic systems. Study of the national prevalence for birth defects in the United States by the Centers for Disease Control and Prevention (CDC) estimate one case of MMC to occur in 2,858 births, making it one of the most common non-chromosomal birth defects [2]. Although the overall prevalence of neural tube defects has declined as a result of a national mandate on folic acid fortification, this was largely represented by a decline in cases of anencephaly, but not MMC [3]. This finding suggests that a subset of neural tube defects, including MMC, are not preventable despite folic acid fortification.

The introduction of postnatal surgical closure of MMC defects has historically improved the overall survival of newborns [4]. At least half of these patients will require additional ventriculoperitoneal shunting for hydrocephalus [5]. These surgeries can be complicated by future development of tethered cord syndrome or shunt infection, respectively; both of which can contribute to worsened neurologic function. The results of the Management of Myelomeningocele Study (MOMS), a randomized controlled trial, have bolstered enthusiasm for prenatal surgical closure of MMC, as it has demonstrated both a decreased need for shunting and improved mental and motor development outcomes, when compared to postnatal closures [6]. Conversely, this enthusiasm is attenuated by the increased maternal-fetal risks of preterm birth and uterine dehiscence associated with prenatal closure. Furthermore, the incidence of spinal cord tethering was higher for the prenatal closure group.

To address the shortcomings of prenatal MMC closure via hysterotomy, centers around the globe have studied and implemented fetoscopic, minimally invasive approaches to prenatal closure [7, 8, 9]. The German technique, as reported by Kohl, utilizes three to four percutaneously placed trocars and achieves closure through coverage with polytetrafluoroethylene and collagen material [7]. In Brazil, Pedreira has reported a percutaneous three-port technique to perform skin closure over a biocellulose patch [8]. At Texas Children’s Hospital, the Fetal Center has pioneered a two-port technique that involves exteriorization of the uterus [10]. Although the sample size is still nascent, preliminary results are promising, as lower rates of preterm birth are observed when compared to both published cohorts of open hysterotomy and percutaneous fetoscopic techniques. Moreover, the technique has allowed for several mothers to undergo vaginal delivery after prenatal surgical closure of MMC.

The existing literature concerning postnatal bladder function in patients has shown no benefit of prenatal open MMC closure when compared to postnatal closure [11, 12, 13, 14, 15, 16, 17, 18]. Brock et al. reported on the urologic outcomes of the MOMS trial, demonstrating that when compared to postnatal closure, prenatal open MMC closure did not reduce the need for clean intermittent catheterization (CIC) at 30 months of age [19]. The aim of this study was to review early postnatal bladder function in a cohort of infants who have undergone fetoscopic prenatal closure via an exteriorized uterus.

2. Methods

The Texas Children’s Hospital Fetal Center performed its first fetoscopic repair for MMC in 2014. This two-port endoscopic procedure was developed by a maternal-fetal medicine obstetrician (MAB) and pediatric neurosurgeon (WEW). Inclusion and exclusion criteria for patients undergoing this procedure were adapted from those reported in the MOMS trial [6]. The technique utilized a low, transverse abdominal incision to exteriorize the uterus and allow for primary endoscopic closure of the defect through two ports [9, 10]. Relaxing incisions are performed to facilitate primary closure, if needed, obviating the use of patch materials. Advantages of this approach, when compared to previously described techniques, include better control over membrane closure and the potential for subsequent vaginal delivery.

This study is a review of early postnatal bladder function assessment performed in patients who have undergone fetoscopic repair and subsequent management at Texas Children’s Hospital between 2014 and 2017. Permission to review these records was granted by the Baylor College of Medicine Institutional Review Board. During the study period, all newborns with MMC were prospectively evaluated and managed based on the CDC Urologic and Renal Protocol for the Newborn and Young Child with Spina Bifida [20]. Descriptive statistics were performed using Prism 7 (GraphPad Software, La Jolla, CA).

Table 1
Risk stratification of bladder based on urodynamic findings

	NDO	DSD	DLPP or EFP	PVR
			(cm H ${}_{2}$ O)
Hostile or high-risk ${}^{*}$	X	X	$\geqslant$ 40	$\uparrow$
Intermediate-risk	X	–	25–40	$\uparrow$
Abnormal but safe	X	–	$<$ 25	$\uparrow$
Normal	–	–	$<$ 15	–

${}^{*}$ Initiated on CIC and anticholinergic; NDO (neurogenic detrusor overactivity), DSD (detrusor sphincter dyssynergia), DLPP (detrusor leak point pressure), EFP (end filling pressure), PVR (post-void residual).

Table 2

Fetoscopic repair and neurosurgical details, in addition to clinical urologic endpoints

	Fetoscopic repair and neurosurgical				Clinical
Patient	GA at repair	GA at birth	Defect	Treatment for	Follow-up	Requires	Febrile
	(wks)	(wks)	level	hydrocephalus	(months)	CIC	UTI
1	23.3	30.9	L3	–	30.7	–	–
2	24.9	39	L3	–	20.5	–	–
3	25.9	38.1	L2	–	19.7	–	–
4	22.9	35.7	L3	ETV	16.3	–	–
5	23.9	38.3	L4	–	15.9	–	–
6	24.6	31.4	L4	–	13.9	–	–
7	22.7	37	L3	–	12.3	–	–
8	25.6	35.9	L5	–	8.5	–	–
9	25.1	38	T11	VPS	6.9	–	–
10	24.9	37.1	T12	–	4.6	–	–
11	25.4	35.3	L5	–	3.9	–	–
12	24.4	39	L2	–	3.7	–	–
13	25.4	39.9	L5	–	3.6	–	–
14	25.6	40	L3	–	2.2	–	–
N (%)				2 (14.3)		0 (0)	0 (0)
Mean (SD)	24.6 (1.0)	36.8 (2.8)			11.6 (8.4)

GA (gestational age), CIC (clean intermittent catheterization), UTI (urinary tract infection), ETV (endoscopic third ventriculostomy), VP (ventriculoperitoneal shunt).

Upon admission to the neonatal intensive care unit, a CIC protocol was initiated every six hours. If volumes returned over 24 hours were $<$ 30 mL, intervals were spaced to eight hours. If the next 24 hours yielded $<$ 30 mL with most catheterizations, intervals were lengthened to 12 hours. If the following 24 hours yielded $<$ 30 mL volumes, CIC was discontinued. Within one week of birth, a renal and bladder ultrasound was performed. In the first three months of life, a dimercaptosuccinic acid (DMSA) scan, voiding cystourethrogram (VCUG), and urodynamics were performed. Bladder wall thickness was defined on ultrasound as normal if $<$ 3 mm when full or $<$ 5 mm when empty [21]. Hydronephrosis was classified based on the Society for Fetal Urology grading system [22]. Renal scarring on DMSA scans was categorized based on the grading system described by the Randomized Intervention for Children with Vesicoureteral Reflux (RIVUR) study [23]. Vesicoureteral reflux was graded as described by the International Reflux Study Committee [24]. Presence of an open bladder neck during filling was determined based on spot films taken during the filling phase of the VCUG.

Table 3

Baseline radiographic studies

	Ultrasound		DMSA Scan	VCUG
Patient	Thickened bladder	Hydronephrosis	Scarring	VUR	Open bladder neck	Trabeculated bladder
1	–	–	–	–	Yes	–
2	–	–	–	–	–	–
3	–	–	–	–	–	–
4	–	–	–	Right grade 1	–	–
5	–	–	–	–	–	–
6	–	–	–	Left grade 4	Yes	–
7	–	–	–	–	Yes	–
8	–	–	–	–	Yes	–
9	–	–	–	–	–	–
10	–	–	–	Right grade 1	Yes	–
11	–	–	–	–	Yes	–
12	–	–	–	–	–	–
13	–	–	–	–	–	–
14	–	–	–	–	Yes	–
N (%)	0 (0)	0 (0)	0 (0)	3 (21.4%)	7 (50.0)	0 (0)

DMSA (dimercaptosuccinic acid), VCUG (voiding cystourethrogram), VUR (vesicoureteral reflux).

Table 4

Urodynamic findings

	Urodynamics
Patient	Age at	Expected	Cystometric	DO	Impaired	Leak	DLPP	DSD	Post-UDS	Risk
	UDS	capacity	capacity		compliance		$>$ 40 cm		residual
	(months)	(mL)	(mL)				H ${}_{2}$ O		(mL)
1	7	51.7	61	Yes	Yes	Yes	–	–	50	Intermediate
2	3	55.5	61	Yes	Yes	Yes	–	–	0	Intermediate
3	3	56.1	60	–	–	Yes	–	–	0	Safe
4	2	32.8	60	Yes	Yes	Yes	–	–	24	Intermediate
5	2	37.4	73	–	Yes	Yes	–	–	50	Intermediate
6	3	33.3	44	Yes	Yes	Yes	–	–	11	Intermediate
7	3	47.0	74	Yes	Yes	Yes	–	–	0	Intermediate
8	3	53.1	73	–	Yes	Yes	–	–	0	Safe
9	3	41.7	70	–	–	Yes	–	–	13	Safe
10	4	45.7	31	Yes	–	Yes	–	–	21	Safe
11	2	32.8	63	–	–	Yes	–	–	0	Normal
12	2	33.0	55	Yes	Yes	Yes	–	–	0	Safe
13	2	45.6	36	Yes	–	Yes	–	–	0	Intermediate
14	2	40.0	30	Yes	–	Yes	–	–	0	Safe
N (%)				9 (64.3)	8 (57.1)	14 (100)	0 (0)	0 (0)
Mean (SD)	2.9 (1.3)	43.2 (8.7)	56.5 (15.4)						12.1 (18.1)

UDS (urodynamics), DO (detrusor overactivity), DLPP (detrusor leak point pressure), DSD (detrusor sphincter dyssynergia).

Urodynamic studies were performed on a Laborie Triton (Mississauga, Ontario, Canada) using room temperature saline at a fill rate of 10–15 mL per minute through a 5 Fr urodynamic catheter. A 9 Fr rectal catheter was used for monitoring abdominal pressures. Cystometric bladder capacity was defined as the volume during filling at which continuous leakage occurred with or without a contraction. Normal compliance was defined as $<$ 15 cm H ${}_{2}$ O change while filling from empty to cystometric bladder capacity. Bladders were risk stratified per protocol as normal, safe but abnormal, intermediate-risk, or high-risk (Table 1). Patients with high-risk bladders were managed with a combination of CIC and oxybutynin (0.2 mg/kg TID). The remainder of patients underwent routine follow-up and were started on CIC and anticholinergic management if a high-risk bladder was identified on a subsequent study.

3. Results

Characteristics of fetoscopic repair, neurosurgical details, and clinical urologic parameters are summarized in Table 2. Fetoscopic MMC repair was performed in 14 patients at a mean gestational age of 24.6 $\pm$ 1.0 (SD) weeks. Mean gestational age at birth was 36.8 $\pm$ 2.8 (SD) weeks. Four (28.6%) mothers had a vaginal delivery. Two (14.3%) patients required treatment for hydrocephalus (one endoscopic third ventriculostomy and one ventriculoperitoneal shunt). Mean urologic follow-up was 11.6 $\pm$ 8.4 (SD) months. No patients required CIC upon discharge from the neonatal intensive care unit and no febrile urinary tract infections occurred within the follow-up period.

Baseline radiographic studies are summarized in Table 3. No patients had hydronephrosis or bladder thickening at birth. No scarring was identified on baseline DMSA scan. Three (21.4%) patients had vesicoureteral reflux, seven (50.0%) had an open bladder neck, and none had trabeculated bladders.

Urodynamic study findings are summarized in Table 4. Baseline urodynamic evaluation was performed at a mean age of 2.9 $\pm$ 1.3 (SD) months. Mean bladder capacity was 56.5 $\pm$ 15.4 (SD) mL. Detrusor overactivity was observed in nine (64.3%) patients. Impaired compliance was seen in eight (57.1%) patients. No patients had a detrusor leak point pressure of $>$ 40 cm H ${}_{2}$ O or evidence of detrusor sphincter dyssynergia. One (7.1%) patient had a normal tracing, six (42.9%) had abnormal but safe, and seven (50.0%) had intermediate-risk bladders.

4. Discussion

The rate of survival for newborns with MMC has improved from a meager 10% before 1960 to a favorable $>$ 90% in contemporary decades [25, 26]. Advancements in medical care, including the introduction of antibiotics, ventriculoperitoneal shunts, and CIC have all contributed significantly to decreasing mortality rates [4]. As a result, current research efforts have increasingly focused on the transitional care of a new population of aging patients with MMC, as well as quality of life issues [27]. The importance of bladder function cannot be underestimated, as urinary continence in patients with MMC has been demonstrated to be associated with higher scores for both general and health-specific quality of life [28]. Moreover, this effect was found to be independent of the type and level of spinal dysraphism, as well as shunt status.

The first prenatal repair of MMC was performed at Vanderbilt in 1997, and the institution subsequently provided the urologic community with the first reported series of urologic outcomes for 16 patients [13]. Both this initial report and a more recent report detailing the long-term follow-up of 28 patients showed no apparent differences in urodynamic data and urologic outcomes for those closed prenatally versus postnatally [11]. Consequent reports from University of California San Francisco and Boston Children’s Hospital similarly identified no evidence of urologic benefit with prenatal MMC closure [12, 16]. The group at Boston Children’s Hospital examined the activity of the external urethral sphincter by needle electromyography during urodynamic study and interestingly identified that all five patients tested who had undergone prenatal closure demonstrated complete denervation of the external sphincter, as compared to 34 of 88 (39%) patients who were closed postnatally [14]. The finding, however, is limited by its small number of prenatally closed patients and has not been substantiated by any subsequent studies.

Arguably the best data currently available that systematically examines bladder function in prenatally versus postnatally closed MMC patients comes from the substudy of the MOMS trial cohort [19]. The primary outcome was defined as death or meeting criteria for CIC at 30 months of age. No significant difference was identified between the prenatal (29 of 56, 52%) and postnatal (39 of 59, 66%) groups (RR: 0.78; 95% CI: 0.57–1.07), with regards to reaching the primary outcome (death occurred in one patient in each group). However, a few notable secondary outcome findings were identified, including the association of less bladder trabeculation and fewer open bladder necks in the prenatal surgery group. At 12 months, bladder trabeculation was present in 15% and 28%, and open bladder neck in 33% and 39% of prenatal and postnatal closure patients, respectively. Initial VCUG in the present study identified no patients with a trabeculated bladder and 50% of patients with an open bladder neck. The clinical significance of a trabeculated bladder and open bladder neck on initial imaging will need to be examined with further longitudinal follow-up. Increasing incidence of upper urinary tract deterioration has been associated with worsening severity of bladder shape and trabeculation [29].

Where the MOMS trial cohort is limited by its heterogeneous urologic follow-up and management, the Federal University of São Paulo has published its single-investigator prospective urologic assessments of prenatal MMC closures [15, 17, 18]. In their most recent series of 48 patients with urodynamic data, 27 (56.2%) were found to have a high-risk bladder (defined as overactivity with detrusor leak point pressure and/or filling pressures $>$ 40 cm H ${}_{2}$ O). In the present study, no patients were identified to have a high-risk bladder; 42.9% and 50.0% had abnormal but safe and intermediate-risk bladders, respectively. Overactivity was identified in 79.2% of bladders in the Brazilian series, which is similar to the 64.3% in the present series. A similar prevalence of vesicoureteral reflux was noted between the São Paulo cohort (26.2%) and the present study (28.6%).

Because of the increased incidence of premature birth observed in prenatal MMC closure, the same Brazilian group examined if gestational age at birth of $<$ 34 weeks versus $\geqslant$ 34 weeks influenced urologic outcomes [18]. At a mean follow-up of 27.9 and 24.3 months for the $<$ 34 weeks and $\geqslant$ 34 weeks gestational age at birth groups, respectively, urologic outcomes were not significantly different. Mean gestational age at birth for the Brazilian cohort is 33 weeks compared to 36.8 weeks in the present cohort. Although the initial fetoscopic data for Texas Children’s has already found a lower rate of neonatal respiratory distress syndrome resulting from less preterm deliveries, its effect on urologic outcomes will require further study [10].

In moving forward with future studies, defining successful outcomes for the urinary tract will require multifaceted consideration. Initial evaluation with radiographic imaging and urodynamic study, as reviewed in the present study, is only the beginning, as a multitude of other factors ultimately contribute to successful management of the urinary tract. Although a functionally normal bladder is ideal, the ability to manage a neurogenic bladder is also dependent on cognitive and motor development [30]. For example, the reduced need for shunting and improved neurologic outcomes observed in prenatal closures may ultimately result in improved independence in the long-term. The application of prenatal MMC closure, both via hysterotomy and fetoscopically, should be cautiously implemented, as careful study is still necessary to ensure a genuine benefit for the mother and infant, while mitigating preventable risks.

5. Limitations

The results of this study should not be interpreted without consideration of its limitations. The current sample size is small, as this cohort represents a new and growing population. Because patients often travel long distances to pursue a novel surgical technique, local urologic follow-up is often unfeasible, a limitation shared by both the MOMS trial and Boston Children’s series [14, 19]. Current efforts are being made to standardize the follow-up and management for patients being followed at outside institutions. The urodynamic studies performed in this series were limited by the use of electromyography pads. Needle electromyography is less prone to artifact and has demonstrated that external urethral sphincter function can evolve over the first three years of life, which emphasizes the need for follow-up beyond the initial urodynamic findings in isolation, as reported in this series [31]. A fill rate of 10–15 mL per minute was utilized for patients in this study period, though concerns for artificially induced detrusor overactivity has since prompted changes to the protocol to fill at a rate of 10% of expected bladder capacity per minute. Lastly, due to scheduling limitations, the first urodynamic evaluation in the present series was performed with a separate VCUG, in lieu of a videourodynamics study. For this reason, evaluating the bladder neck during filling was accomplished using VCUG films, in contrast to the videourodynamics studies utilized in the MOMS trial [19].

6. Conclusions

This report represents the first urologic evaluation of early postnatal bladder function after prenatal fetoscopic MMC closure. Early postnatal bladder function does not appear to be any worse than that of previously reported prenatal or postnatal closures. Although we would not expect improved bladder outcomes with this modified technique, it is reassuring in moving forth with recruiting patients for fetoscopic repair at our institution. Longer follow-up and assessment of children following up at outside institutions is imperative in appraising this approach to myelomeningocele repair.

Footnotes

Acknowledgments

The authors of this manuscript would like to thank the nurses of the spina bifida and urology clinic at Texas Children’s Hospital, including Rhonda Bolin, Ana Perez, Eva Acosta, and Imelda Salcedo for their tireless dedication to our patients – without their compassion and devotion, care for our patients would not be possible.

Conflict of interest

There are no conflicts of interest to report.

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Early postnatal bladder function in fetoscopic myelomeningocele repair patients

Abstract

PURPOSE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Methods

Table 1 Risk stratification of bladder based on urodynamic findings

4. Discussion

5. Limitations

6. Conclusions

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Risk stratification of bladder based on urodynamic findings