Children with nocturnal enuresis have posture and balance disorders

Accepted Manuscript Children with nocturnal enuresis have posture and balance disorders R.P. Rodrigues Pereira, S. Nascimento Fagundes, A. Surry Lebl, L. Azevedo Soster, M.G. Machado, V.H. Koch, C. Tanaka PII:

S1477-5131(16)30047-X

DOI:

10.1016/j.jpurol.2016.05.003

Reference:

JPUROL 2186

To appear in:

Journal of Pediatric Urology

Received Date: 24 November 2015 Accepted Date: 4 May 2016

Please cite this article as: Pereira RPR, Fagundes SN, Lebl AS, Soster LA, Machado MG, Koch VH, Tanaka C, Children with nocturnal enuresis have posture and balance disorders, Journal of Pediatric Urology (2016), doi: 10.1016/j.jpurol.2016.05.003. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Children with nocturnal enuresis have posture and balance disorders

Sosterc, M. G. Machadod, V. H. Kochb, C. Tanakaa

a

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R. P. Rodrigues Pereiraa,*, S. Nascimento Fagundesb, A. Surry Leblb, L. Azevedo

Department of Physiotherapy, Communication Science & Disorders, Occupational

Pediatric Nephrology Unit, Instituto da Criança do Hospital das Clínicas, University of

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b

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Therapy, University of Sao Paulo - School of Medicine, Sao Paulo, Brazil

Sao Paulo - School of Medicine, Sao Paulo, Brazil c

Pediatric Sleep Laboratory, Instituto da Criança do Hospital das Clínicas, University of

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Sao Paulo - School of Medicine, Sao Paulo, Brazil

Pediatric Urology Unit, Hospital das Clínicas, University of Sao Paulo - School of

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Medicine, Sao Paulo, Brazil

* Corresponding author. Divisão de Fisioterapia - Instituto Central do Hospital das

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Clínicas da Faculdade de Medicina da Universidade de São Paulo Avenida Dr. Enéas de Carvalho Aguiar, 155, 4º Andar/Bloco 2, Prédio dos Ambulatórios, CEP: 05403-000, Cerqueira César, São Paulo, SP, Brasil. Tel.: +55 11 2661-3373; fax: +55 11 2661-7969. E-mail address: [email protected] (R. P. Rodrigues Pereira)

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Summary Introduction: Integration of the neuromuscular system is required for maintaining

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balance and adequate voiding function. Children with enuresis have delayed maturation of the motor cortex, with changes in the sensory and motor systems. Along with various alterations, including the genetic, hormonal, behavioral, and sleep disturbances, and

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neuromotor and sensory deficits associated with nocturnal enuresis (NE) in children and adults, a consistent alteration in the posture of children with NE has been observed in

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the current practice. Because posture and the balance control system are strongly connected, this study aimed to investigate posture and balance in children and teenagers

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with NE.

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Material and methods: A total of 111 children with enuresis were recruited to the enuretic group (EG) and 60 asymptomatic children made up the control group (CG). The participants were divided into two age subgroups: (A) 7-11 years old, N=77 for EG/A, N=38 for CG/A; and (B) 12-16 years old, N=34 for EG/B, N=22 for CG/B. Balance was assessed using an electronic force plate (100 Hz) to calculate the area of the center of pressure (COP) displacement. The COP is the point that results from the action of vertical forces projected onto the force plate. Sensory integration was analyzed using a 60-second trial with the subject standing under four conditions: (1) eyes open,

ACCEPTED MANUSCRIPT stable surface; (2) eyes closed, stable surface; (3) eyes open, unstable surface; (4) eyes closed, unstable surface. Posture was assessed by placing reflective anatomical landmarks on the anterior

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superior iliac spine, the posterior superior iliac spine, the greater trochanter, and lateral malleolus. A photograph was taken while the subject stood quietly. The angles were obtained from landmark connections using software to assess the following posture

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variables: pelvic ante/retroversion and pelvic ante/retropulsion.

Results: The EG showed a greater area of COP displacement compared with the CG

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under all four sensory conditions and both subgroups, except for EG/B in condition 3. Regarding posture, EG showed higher pelvic anteversion angles than CG. Conclusions: Enuretic children showed forward inclination of the pelvis and had worse

Nocturnal

enuresis;

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Keywords:

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balance compared with control children.

Posture;

Postural

balance;

Physiotherapy

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Introduction Nocturnal enuresis (NE), also called bedwetting, is defined as involuntary voiding while sleeping in people aged >5 years. It is related to developmental disturbances and

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frequently causes psychological and social suffering for the affected children and their families. Monosymptomatic nocturnal enuresis can be defined as the presence of urine incontinence during sleep, and non-monosymptomatic when associated with other

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symptoms of the lower urinary tract, including: nocturnal and diurnal losses, bladder changes, post residual urine, UTI, constipation and/or encopresis. This set of associated

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symptoms can cause deterioration of bladder function, upper urinary tract and, in extreme cases, even kidney failure [1].

The two subtypes of enuresis are important for understanding the pathophysiology of the current study. At present, NE does not seem to be an isolated

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phenomenon because various alterations, including genetic [2], hormonal [3], behavioral disturbances [4,5], sleep disturbances [6,7], and neuromotor and sensory deficits [8,9,10,11,12] have been reported in children and adolescents with NE.

childhood.

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Therefore, NE may be a manifestation of multifactorial disorders of development during

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Recent publications have indicated that the picture of NE and its associated

alterations remains unclear. Are these alterations causes or consequences of NE? Do they occur independently or along with NE? Are there any other manifestations of the development delay related to NE? In the current clinical practice, consistent alterations of posture and balance have been noticed in children and adolescents with NE during their physiotherapy evaluations. These alterations may be an important part of the developmental

ACCEPTED MANUSCRIPT disturbances in children with NE. Therefore, it was hypothesized that children and adolescents with NE could present with postural and balance alterations. This study

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aimed to investigate posture and balance in children and adolescents with NE.

Methods

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The current study had an observational cross-sectional design. It comprised two groups: the enuretic group (EG), with a total of 111 children diagnosed with NE aged

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10.27±2.61 years), and the control group (CG), with 60 healthy children (aged 10.88±2.40 years). The EG children were initially screened, categorized into monosymtomatic or non-monosymptomatic NE, and referred to the study by two physicians from the Pediatric Nephrology Unit, Instituto da Criança do Hospital das

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Clínicas, University of Sao Paulo - Medical School (HC-FMUSP). The CG children were recruited from relatives of students and workers at the hospital. For both groups, their legal guardians signed a consent form approved by the Ethics Committee of this

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hospital (CAPpesq No 0609/11).

The EG comprised 65 children with monosymptomatic nocturnal enuresis, and

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46 with non-monosymptomatic nocturnal enuresis, according to the ICCS criteria [1]. The EG and CG were subdivided into two age subgroups: (A) 7-11 years old, EG/A NMonosymptomatic=47, NNonMonosymptomatic=30; CG/A N=38; and (B) 12-16 years old, EG/B NMonosymptomatic=18, NNonMonosymptomatic=16; CG/B N=22. The age subgroups were adopted due to variability in the area of COP displacement throughout the age range [13,14,15,16]. Children with anatomical changes in the urinary tract, genetic

ACCEPTED MANUSCRIPT syndromes, neurological conditions or diseases that could affect balance, cognitive impairments, trauma or previous orthopedic surgeries were not included in the study.

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Posture assessment

Posture refers to body alignment to maintain the proper conditions to perform movements [13]. It was assessed using a photogrammetry technique, which is

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considered as a reliable alternative to the quantitative evaluation of posture with measurement of linear and angular variables [17]. Reflective anatomical landmarks

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were placed on the lateral malleolus (LM), greater trochanter (GT), anterior superior iliac spine (ASIS), and posterior superior iliac spine (PSIS). A photograph was taken from the child’s right side while the child stood quietly against a dark, matte back wall. The room was prepared to reduce noise as much as possible. Total abolishment of noise

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was not guaranteed, however, the main distractors that could interfere with balance were controlled. A photographic digital camera was used (SONY Cyber-shot, 16.1 mega pixels, 5 x optical zoom, DSC- W570, São Paulo, SP, Brazil) that was fixed on a tripod

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placed in a controlled position.

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The angles obtained from the landmark connections were analyzed using software of postural assessment (SAPO). The following angles were used: pelvic ante/retroversion (ASIS-PSIS-horizontal) and pelvic ante/retropulsion (GT-LM-vertical) (Fig. 1. A). The pelvic ante/retroversion position indicated, respectively, the forward/backward rotation around the transversal axis of the pelvis. The pelvic ante/retropulsion position indicated, respectively, the anterior/posterior position of the pelvis related to the ankle [18].

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Balance assessment Balance is the ability to maintain body stability [13]. Data were acquired using a system that was made up of a force plate (EMG System do Brasil Ltda®, São José dos Campos,

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SP, Brazil.) and an analogue digital convertor (OR6 12-bits) connected to a computer at a frequency of 100 Hz. A computerized program transformed the primary center of pressure (COP) signal into numeric data throughout the acquisition duration (Fig. 1. B). The COP is the point that results from the action of vertical forces projected onto the

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force plate. Center of pressure displacement reflects the body’s movements in the

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attempt to keep the center of mass within the boundaries of the weight-supporting base (both feet) and maintain balance [19].

The children were asked to stand barefoot, with their arms at their sides, on a force plate embedded in the laboratory floor, and to remain motionless. Because the integration of visual, somatosensory and vestibular information is essential for balance,

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data from 60-second trials were collected under four different sensory conditions: (1) eyes open, standing on a stable surface; (2) eyes closed, standing on a stable surface; (3)

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eyes open, standing on an unstable surface; and (4) eyes closed, standing on an unstable surface. For conditions 1 and 2, the subjects stood directly on the force plate, and for

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conditions 3 and 4, the subjects stood on a 6-cm-tall foam pad (Airex balance pad®, density: 57 g dm-3; Airex AG specialty foams, Sins, Switzerland) placed on the force plate. To prevent motor learning of the balance response, a preset evaluation sequence was adopted for the four sensory conditions. Therefore, a sequence of conditions 1 to 4 was used to assess all sensory conditions: in condition 1, all sensory information was available and accurate, and in condition 4, only the sensory information coming from the vestibular system was accurate, making this condition the most challenging for the

ACCEPTED MANUSCRIPT nervous system [20,21]. A 60-second rest interval was permitted between each sensory condition trial.

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Statistical analysis

The statistical analyses were performed using Minitab® Statistical Software version 15 (Minitab, Inc., State College, Pennsylvania, USA) and IBM SPSS® Statistics for

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Windows Version 20.0 (IBM Corp., released 2011, Armonk, NY). The angles of the pelvis were compared between subgroups using the paired t-test, as these measurements

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were normally distributed. The area of COP displacement was analyzed using the Mann-Whitney test because the data did not meet the assumptions of the parametric

Results

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test. A significance level of 0.05 was adopted for all of the analyses.

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Age and body mass index (BMI) did not present differences between the EG and CG.

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For each comparison between EG and CG, a previous within-group analyses comparing age subgroups A and B of monosymptomatic and non-monosymptomatic EN were performed. In the within-group comparison of posture assessment, no differences were shown in pelvic anteversion (P=0.93 and P=0.84 for subgroup A and B, respectively) and for pelvic antepulsion (P=0.78 and P=0.74 for subgroup A and B, respectively). In the within-group comparison of balance (area of COP displacement), considering age subgroups in each of the four different sensory conditions, differences were found with

ACCEPTED MANUSCRIPT P-values varying from 0.10-0.55 in subgroup A, and from 0.32-0.99 in subgroup B. Therefore, analyses were proceeded as a single EG comparing with CG. The EG children presented a higher angle of pelvic anteversion for both age

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subgroups (P=0.01 for both age subgroups) compared with the CG children. No difference in the angle of pelvic antepulsion was found between the groups. Table 1 shows descriptive analysis of the angles of the pelvis for the subgroups of EG and CG,

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and P-values obtained with comparison using Student’s t-test.

The EG children presented with a larger area of COP displacement in both age

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subgroups compared with the CG children. The subgroup EG/A showed a significant difference among the four sensorial conditions, while the subgroup EG/B showed significant differences among conditions 1, 2, and 4. Table 2 shows descriptive analysis of the area (cm²) of COP displacement under all sensory conditions for EG and CG, and

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Discussion

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the respective P-values obtained with comparisons using Mann Whitney U-test.

To investigate posture and balance in children and teenagers with NE, a group of 111

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NE and 60 control participants with ages ranging from 7-16 years were compared. Alterations such as developmental delays in motor [11,12] and speech acquisition, learning [22], physical growth and skeletal maturity [9] have been associated with NE; however, it is believed that this study is the first to describe alterations in posture and balance in children and teenagers with NE. Because the motor cortex comprises areas of voluntary control of voiding and areas of motor planning, a maturation deficit of the motor cortex may directly impact

ACCEPTED MANUSCRIPT balance, as found in the current study. Body balance is compromised by an impaired ability to keep the center of the body mass within the boundaries of the polygon established by both feet [13]. This ability depends on the perfect interaction of the

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musculoskeletal, motor and sensory nervous systems [13,23]. Sensory integration tests with a force plate have been widely used to quantify changes in balance (e.g. in children with chronic low back pain [24], women with stress

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incontinence [25], children with attention deficit and hyperactivity disorders (ADHD) [26], and children with hemophilia [27,28]). Despite the variations among studies, the

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‘common pathway’ for assessing balance is either via the deprivation of visual information (i.e. the eyes-closed condition) or by making the information from the receptors in the feet inaccurate (i.e. by standing on a foam surface) or by combining these strategies, as was done in the current study.

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The results showed important balance alterations in the children with NE. These children presented with a larger area of COP displacement compared with the children in the CG. When all sensory information was available (condition 1), the area of COP

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displacement was larger in both subgroups of children with NE. Although accounting for total offer of sensorial information and with the redundancy of the information,

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children in the EG oscillated in a larger area than those in the CG. Balance and posture are strongly related because posture is the result of the effort required to sustain the body against the force of gravity, which is refined by fine motor adjustments to maintain balance [13]. Therefore, it is possible that the higher pelvic anteversion may compromise children with EG abilities to perform such adjustments. The conditions that involved sensory privation (conditions 2, 3, and 4) yielded similar findings; the exception was condition 3 (with inaccurate somatosensory information), for which no

ACCEPTED MANUSCRIPT difference in the area of COP displacement was observed between subgroups EG/B and CG/B. Verifying that the area of COP displacement was higher in EG/B than CG/B in conditions 2 and 4 (both missing the visual information), it is believed that EG/B were

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not able to re-weight the remaining sensorial information to keep their balance stable. A specifically designed study should be carried out to better understand why somatosensory and vestibular information are not reliable for overcoming the lack of

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visual information in the balance control in EG/B.

The age subgroups were based on the age range of the participants in the

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current study (7-16 years). Shumway-Cook and Woollacott [13], when studying the development of sensory adaptation in children, found a high variability in the area of COP displacement throughout the age range. Hayes and Riach [14], Taguchi et al. [15], and Kirshenbaum et al. [16] showed that in children aged 12-15 years, the velocity of

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COP displacement reached the adult level. These findings suggested that splitting the participants into age subgroups would avoid bias in the between-group comparison. The photogrammetry technique has commonly been used to quantify changes in

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posture [17]. In the current study, posture was assessed and it was found that both groups presented with pelvic anteversion and antepulsion; however, compared with the

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CG, the EG showed higher angles only for pelvic anteversion. Pelvic anteversion (i.e. the forward inclination of the pelvis) is associated with lumbar hyperlordosis, suggesting poor muscular synergy in the abdominal wall and pelvic floor, which compromises urinary continence and the respiratory pattern, as reported by Hodges et al. [29]. Although the participants in the current study did not present with attention deficit/hyperactivity disorder (ADHD), according to DMS-5 criteria [30], restlessness

ACCEPTED MANUSCRIPT and distractedness were noticed during evaluation of the EG children, including some difficulty completing the assessments that required 60 seconds of quietness. As with Von Gontard et al. [11], the ‘reckless’ and ‘inattentive’ behavior of the EG children was

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noticed and suggested that NE children present with, if not ADHD, a significant motor coordination development disorder that may significantly compromise academic performance or daily life activity [30].

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Considering the associations of ADHD with balance [25] and NE [5], in addition to the balance alterations in the NE children that were found in the current

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study, it is reasonable to suggest that ADHD, NE, and balance may be correlated. Moreover, ADHD, posture, and balance, as well as the behavioral [4,5] and sleep disturbances [6,7], and neuromotor and sensory deficits [8,9,10,11,12] are associated with NE, and may together be related to a failure of common areas of the nervous

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system that control motor, cognitive, and limbic functions. It is noteworthy that all of these disturbances are primarily functional deficits and that the encephalic function areas are not limited to the anatomical lobes of the brain.

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In this way, NE could be understood not as a single isolated phenomenon, but as part of a complex scenario of changes caused by the disturbance of nervous system

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maturation. A functional rehabilitation program may be indicated to improve balance and posture, stimulating the whole scenario of changes in the nervous system maturation, and perhaps with impact on urinary symptoms.

Limitations The lack of a comprehensive clinical evaluation of the nervous system, including other aspects of motor control, and cognitive and limbic functions, could be pointed out as a

ACCEPTED MANUSCRIPT limitation of the study; this could have elucidated the nervous system maturation

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disturbance lying behind NE.

Conclusion

Children and teenagers with NE present a higher forward inclination of the pelvis and a

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larger area of COP displacement, regardless of the accuracy of all sensory information.

Acknowledgements

We are very grateful to all the children and parents who participated in this study.

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Conflict of interest. Nil.

Funding. This paper was part of a major, multi-professional project, which received a

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research grand support from FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo). Although the support was not applied particularly to this part of the study,

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we believe that it was crucial in so many ways for the completion of the project. Therefore, the authors would like to address an acknowledgment for the financial support received from FAPESP (2011/17589-1).

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JE, Rowell L, et al. Handbook of physiology. Exercise: regulation and integration of multiples systems. New York: Oxford University; 1996. pp. 255-92. [24] Leitner C, Mair P, Paul B, Wick F, Mittermaier C, Sycha T, et al. Reliability of posturographic measurements in the assessment of impaired sensorimotor function in chronic low back pain. J Electromyogr Kinesiol 2009;19:380–90. [25] Smith MD, Coppieters MW, Hodges PW. Is balance different in women with and without stress urinary incontinence? Neurourol Urodyn 2008;27:71–8.

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mental disorders-fifth edition (DSM 5). Washington, DC: APA; 2013.

ACCEPTED MANUSCRIPT Table 1. Mean and standard deviation of the angles of the pelvis for the subgroups of EG and CG. Age

CG

P*

Pelvic anteversion

A

11.24±3.55

7.44±4.10

0.01

B

10.11±3.19

7.14±4.22

0.01

Pelvic antepulsion

A

3.39±1.70

3.57±1.72

0.93

B

4.29±1.99

4.43±1.98

0.75

*Comparison using Student’s t-test

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EG, enuretic group; CG, control group

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EG

subgroup

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Variables

ACCEPTED MANUSCRIPT Table 2. Median, Q1 and Q3 of the area (cm²) of center of pressure displacement under all sensory conditions for EG and CG. EG

CG

Median (Q1-Q3)

Median (Q1-Q3)

A

3.1 (1.68-4.49)

1.87 (1.11-2.85)

B

2.22 (1.44-3.49)

1.68 (1.31-2.25)

0.020

A

3.21 (2.04-6.36)

2.52 (1.65-3.76)

0.041

B

3.05 (1.54-4.0)

2.05 1.09-2.23)

0.043

A

4.95 (3.07-8.63)

2.82 (2.1-4.41)

0.002

B

3.64 (2.45-5.91)

A

4.95 (3.07-8.63)

B

3.64 (2.45-5.91)

2

3

4

P* 0.002

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1

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Age subgroup

2.65 (2.14-3.65)

0.314

3.55 (2.4-5.77)

0.001

3.04 (1.6-4.24)

0.047

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Conditions

*Comparisons using Mann Whitney U-test

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EG, enuretic group; CG, control group; Q1, first quartile; Q3, third quartile

Condition 1: eyes open, standing on a stable surface; Condition 2: eyes closed, standing on a stable surface; Condition 3: eyes open, standing on an unstable surface; and

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Condition 4: eyes closed, standing on an unstable surface

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Figures Fig. 1. A. Posture data collection diagram and a representation of the two evaluated

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angles.

ACCEPTED MANUSCRIPT Fig. 1. B. Balance data collection diagram for the four conditions of sensory

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information.