Development of the Brazilian Portuguese version of the “Grading scale for idiopathic normal pressure hydrocephalus”: cross-cultural adaptation, reliability and validity

Validação da escala de hidrocefalia de pressão normal idiopática para o português brasileiro: aplicação, confiabilidade e validade

ABSTRACT

Objective:

The current study translated to Portuguese and validated the normal pressure hydrocephalus (NPH) scale originally developed in English as the Grading Scale for Idiopathic Normal Pressure Hydrocephalus.

Methods:

Following Guillemin's validation protocol, the last version of the Portuguese NPH scale was applied to 121 consecutive patients with a diagnosis of normal pressure hydrocephalus (73 men and 48 women) from the Group of Cerebral Hydrodynamics from July 2010 to March 2012.

Results:

The mean age was 71.09 years old, ranging from 35 to 92 years. The rate of agreement and reproducibility was high, as confirmed by Cohen's Kappa coefficient, with excellent intraobserver correlation for the NPH scale items individually evaluated: gait (0.80), dementia (0.90) and incontinence (0.87).

Conclusions:

The Portuguese version of the Grading Scale for Idiopathic Normal Pressure Hydrocephalus was successfully translated and validated for use in Brazilian patients.

Keywords:
Hydrocephalus, normal pressure; translations; validation studies; surveys and questionnaires

RESUMO

Objetivos:

o presente estudo valida para a língua portuguesa a escala de hidrocefalia de pressão normal (HPN) desenvolvida em língua inglesa como “Escala de classificação para hidrocefalia de pressão normal idiopática”.

Métodos:

Usando o método de Guillemin, uma versão traduzida da escala foi aplicada em 121 pacientes consecutivos com diagnóstico de hidrocefalia de pressão normal (73 homens e 48 mulheres) no Grupo de Hidrodinâmica Cerebral do Hospital das Clínicas da FMUSP de julho de 2010 a março de 2012.

Resultados:

a média de idade foi de 71,09 anos, variando de 35 a 92 anos. A taxa de concordância e reprodutibilidade foi alta, conforme confirmado pelo coeficiente Kappa, com excelente correlação intraobservador para itens de escala HPN que avaliou a marcha (0,80), demência (0,90) e incontinência (0,87).

Conclusões:

a versão em português da escala de graduação para pacientes com HPN foi traduzida e validada com sucesso para uso em pacientes brasileiros de ambos os sexos.

Palavras-chave:
hidrocefalia de pressão normal; traduções; estudos de validação; inquéritos e questionários

Normal pressure hydrocephalus (NPH) is a neurological disease characterized predominantly by progressive development of gait apraxia, cognitive disturbances and urinary incontinence. Other neuropsychiatric symptoms may also occur^{1,2,3,4,5,6,7}. It promotes the patient's functional dependence and is responsible for family and social burden^{8,9,10,11,12,13,14,15}. However, in many cases, symptoms may be mitigated with appropriate surgical treatment and multidisciplinary neurocognitive rehabilitation⁹.

Many scales are widely applied to evaluate NPH; however, most of them are not specific, having been adapted from the evaluation of cognitive deficits (Mini Mental State Examination, Cambridge Cognitive Assessment and Montreal Cognitive Assessment) and from motor evaluations (Timed Up and Go, Dynamic Gait Index, Berg Balance Scale, and others)^{1,2,3,4,5,6,7,8,9,10,11,12,13,14,15}.

However, a specific scale has been developed to address all three components of the triad. The Grading Scale for Idiopathic Normal Pressure Hydrocephalus was originally developed in Japan in the English language, based on a cooperative study, between 1996 and 1999, to determine the most predictive diagnostic criteria for NPH patients¹³. It comprises three domains (gait, dementia and urinary incontinence) with scores ranging from 0 to 12 (the higher the score, the worse the symptoms). It is easily and rapidly applied and may be used as a follow-up evaluation tool, correlating with post treatment symptoms and results¹.

The objective of the present study was to validate the Grading Scale for Idiopathic Normal Pressure Hydrocephalus developed in English that was translated into Portuguese as the Normal Pressure Hydrocephalus Patient Graduation Scale (NPHPGS).

METHODS

A cross-sectional, observational study was performed on 121 patients of both genders, aged over eighteen years of age, with a medical diagnosis of NPH. Patients were recruited by means of a consecutive sample, according to the following criteria.

Inclusion criteria

Patients with an idiopathic or secondary NPH diagnosis, older than eighteen years of age, of both genders, who agreed to participate. The NPH diagnosis was considered in patients with at least one of the constituent symptoms of the classic triad (urinary incontinence, memory impairment, or gait apraxia), and evidence of hydrocephalus on neuroimaging (CT or MRI).

Exclusion criteria

Patients with an altered level of consciousness, patients with clinically decompensated systemic diseases or malignancies.

The present study was approved by the Ethics Committee for Analysis of Research Projects of the Hospital das Clínicas of the Faculty of Medicine of the University of São Paulo.

Translation

The Grading Scale for Idiopathic Normal Pressure Hydrocephalus was translated into Portuguese in a standardized way to guarantee the quality and reliability of the original version, according to the method by Guillemin et al.¹⁶.

Translation was carried out by two bilingual Brazilian neurologists, experienced in the validation of instruments, and the two final translations were compared by the translators, correcting the inconsistencies, and developing a consensual translation. Afterwards, the back-translation to English was performed by two other bilingual neurologists, who were different from the previous ones and did not know the original scale.

Additionally, a comparison of the versions was made by a multidisciplinary committee, comprising physicians and physiotherapists who were not involved in the translation process, defining the Portuguese version of the scale as “Escala de Graduação do Paciente com Hidrocefalia de Pressão Normal” (the above-mentioned NPHPGS). This Portuguese version of the scale is shown in Figure 1.

Figure 1
Portuguese version of the Grading Scale for Idiopathic Normal Pressure Hydrocephalus¹³ – the Normal Pressure Hydrocephalus Patient Graduation Scale.

Validation

Patients were individually evaluated at two different times, with a one-week interval. Data were collected by physiotherapist A and, subsequently, by physiotherapist B, sequentially evaluating the same patient. In this way, it was possible to compare the results and avoid errors between observers. On the first day, the initial protocol was determined, so that these results could be compared to test the reliability of the new instrument containing personal data by application of the Functional Independence Measure (FIM), Berg Balance Scale (BBS), Dynamic Gait Index (DGI), Timed Up and Go (TUG) and the NPHPGS by physiotherapist A. On the same day, the second physiotherapist B applied the NPHPGS to verify reproducibility between observers.

The TUG test evaluates the time taken to walk a short distance and has been proven to be a good option for diagnosis, outcome prediction, and postoperative follow-up, although there have been no studies of isolated TUG performance in the setting of NPH^{1,17,18,19,20,21,22}.

The FIM is a scale that evaluates disability in neurological patients according to their ability to perform routine daily personal activities, such as self-care, sphincter control, mobility and locomotion, communication and social cognition^{17,18,19,20,21,22}.

The DGI assesses an individual's ability to modify balance while walking, in the presence of external demands. The test is performed with a marked distance of 20 feet and can be performed with or without an assistive device. Eight tasks are graded on a score from 0 to 3 (0, severe impairment; 1, moderate impairment; 2, minimal impairment; 3, no gait dysfunction), for a maximum score of 24. The eight tasks include 1) level surface gait, 2) change in gait speed, 3) gait with horizontal head turns, 4) gait with vertical head turns, 5) gait with pivot turn, 6) stepping over obstacles, 7) stepping around obstacles, and 8) stair climbing^{17,18,19,20,21,22}.

The BBS is one of the most widely-used and recognized balance measures. It has been validated in several populations, including stroke, and cut-off scores have been determined to identify those at risk of falls and those who need a gait aid for ambulation. It is commonly applied during inpatient rehabilitation, and has been shown to predict length of stay and discharge destination^17–22.

After one week, the patients underwent a new evaluation of the NPHPGS by the initial physiotherapist A, to verify the intraobserver (test/retest) reproducibility.

RESULTS

A total of 121 patients were studied, with a higher percentage of male patients (60.33%). The overall age range was between 35 and 92 years, with a higher concentration of patients between 71 and 80 years. The mean age was 71.09 years with standard deviation = 2.8 years. Primary NPH was present in 50 patients, while secondary NPH was present in 71 patients (usually following meningitis, trauma or subarachnoid hemorrhage). As for the domains, there was a higher frequency of gait impairment (96.69%), followed by dementia (85.95%) and urinary incontinence (79.33%). The summary of results are presented in the Table.

Table
Summary of results, with evaluation of correlation and observer agreement.

Variable			Statistical analysis
			Cohen's Kappa coefficient for measuring agreement
Patients
Female (n)	38		Intraobserver	Interobserver
Male (n)	73	Gait	0.80	0.91
Mean age (years)	71	Dementia	0.90	0.86
		Urinary incontinence	0.87	0.87
Symptoms (%)			Pearson's Correlation
Gait apraxia	96		NPHPGS and FIM	0.842
Dementia	85		NPHPGS and BBS	0.803
Urinary incontinence	79		NPHPGS and DGI	0.694
			NPHPGS and TUG	0.557

• FIM: Functional independence measure; BBS: Berg balance scale; DGI: Dynamic gait index; TUG: Timed up and go; NPHPGS: Normal pressure hydrocephalus patient graduation scale.

To evaluate the reliability and reproducibility, the scale was applied by the same evaluator with a one-week interval (intraobserver analysis) and different raters on the same day (interobserver analysis). The results were analyzed by Cohen's Kappa coefficient for measuring agreement. For intraobserver agreement, a general Kappa value was obtained, with an excellent concordance for the gait items (0.80), dementia (0.90) and incontinence (0.87).

Subsequently, an analysis of the validation of the method was carried out through the interobserver agreement, with excellent agreement for the gait items (0.91), dementia (0.86) and incontinence (0.87).

The comparison of the NPHPGS with the other scales was performed using Pearson's correlation coefficient, followed by the hierarchy shown in the graphs obtained from the ANOVA test values and multiple comparisons of the Tukey Test.

A satisfactory correlation was found in the NPHPGS and FIM scales, using Pearson's correlation (0.842). The hierarchy was obtained according to NPH values: below 40, between 40 and 79 and above 80 (Figure 2).

Figure 2
Correlation of data of the Portuguese NPHPGS and the FIM. Confidence interval = mean ± 1.96 * standard deviation / √ (n-1).

NPHPGS: Normal pressure hydrocephalus patient graduation scale; FIM: Functional independence measure;

A satisfactory correlation was found between the NPHPGS and BBS scores using Pearson's correlation (0.803). The hierarchy was obtained according to the NPH values: below 36, between 36 and 45, and above 46 (Figure 3).

Figure 3
Correlation of data of the Portuguese NPHPGS and the BBS. Confidence interval = mean ± 1.96 * standard deviation / √ (n-1).

NPHPGS: Normal pressure hydrocephalus patient graduation scale; BBS: Berg balance scale.

A moderate correlation was found between the NPHPGS and DGI, using Pearson's correlation (0.694). The hierarchy was obtained according to the NPH values: below 19, equal to, or above 19 (Figure 4).

Figure 4
Correlation of data of the Portuguese NPHPGS and the DGI. Confidence interval = mean ± 1.96 * standard deviation / √ (n-1).

NPHPGS: Normal pressure hydrocephalus patient graduation scale; DGI: Dynamic gait index.

A moderate correlation was found between the NPHPGS and TUG, using Pearson's correlation (0.557). The hierarchy was obtained according to NPH values: below 12, between 13 and 19, between 20 and 29, and above 30 (Figure 5).

Figure 5
Correlation of data of the Portuguese version of the NPHPGS Scale and the TUG. Confidence interval = mean ± 1.96 * standard deviation / √ (n-1).

NPHPGS: Normal pressure hydrocephalus patient graduation scale; TUG: Timed up and go.

DISCUSSION

The lack of evaluation instruments aimed at NPH patients that have been translated and validated for Portuguese may restrict the research in this field. We translated and validated the Grading Scale for Idiopathic Normal Pressure Hydrocephalus. This instrument was designed to quantify the degree of deficit in patients with NPH¹³.

In the intraobserver evaluation, the agreement was 0.80 for gait, 0.90 for dementia and 0.87 for urinary incontinence, all classified as excellent concordance. The same classification was found for the interobserver evaluation, with 0.91 for gait, 0.86 for dementia and 0.87 for urinary incontinence. These results favor the use of the evaluated instrument.

Although there is no gold standard for NPH evaluation, many scales have already been developed and used in the literature to assess the severity of the NPH triad. However, the main problem faced is the similarity between items in these domains, which often hinders the interviewer's scoring.

Kubo²³ developed the grading scale for the evolution of NPH symptoms. However there has been criticism regarding items in the cognitive domain that tended to dubiously score amnesia, inattention and disorientation. In the gait domain, there was also an inconsistency of classification, as the scale had a different classification for the imbalance item, but without distinction of an objective gait disorder. Cordero Tous et al.²⁴ carried out a prospective study using clinical scales and radiological findings to evaluate 40 patients with NPH. The items of the NPH scale in the cognitive domain were confusing, including the vegetative state, severe dementia and personality changes, which were difficult to stage and describe.

Owler et al.²⁵ described a modified scale for NPH for the clinical classification of patients. However, this scale subjectively evaluated daily life activities, and sphincter domain symptoms were only described as present or absent, which was also subjective and not elucidating. Thus, the NPH evaluated in the study by Mori¹³ seemed to be more objectively applied and complete.

Regarding the evaluation of the scores of the new NPHPGS, the scores compared with other widely-used and validated scales. In the comparison with the FIM total score, there was a high concordance of the findings, as the patients who presented with the greatest impairment on the NPHPGS were concomitantly classified with greater impairments in the FIM scale. Correlation was statistically satisfactory (-0.842). The same response was observed for the BBS (-0.803), DGI (-0.694) and TUG (-0.557). The above results confirm that the Grading Scale for Idiopathic Normal Pressure Hydrocephalus¹³ and its Portuguese-validated version correlates with NPH symptoms and should be applied to evaluate these patients.

In conclusion, the present study showed a statistically significant correlation between the NPHPGS and the TUG, FIM, DGI and BBS. Additionally, the NPHPGS scale had also satisfactory interobserver and intraobserver agreement in the analysis of scores in the translated version. Thus, the Portuguese version is validated and may be used in assessing NPH.

• Support: The present study was approved by the Ethics Committee for Analysis of Research Projects (CAPpesq) of the Hospital das Clínicas of the Faculty of Medicine of the University of São Paulo (HCFMUSP).

References

• ¹
  Mendes GA, de Oliveira MF, Pinto FC. The Timed Up and Go Test as a Diagnostic Criterion in Normal Pressure Hydrocephalus. World Neurosurg. 2017 Sep;105:456-61. https://doi.org/10.1016/j.wneu.2017.05.137
  » https://doi.org/10.1016/j.wneu.2017.05.137
• ²
  Hakim S, Adams RD. The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci. 1965 Jul-Aug;2(4):307-27. https://doi.org/10.1016/0022-510X(65)90016-X
  » https://doi.org/10.1016/0022-510X(65)90016-X
• ³
  Pereira RM, Suguimoto MT, Oliveira MF, Tornai JB, Amaral RA, Teixeira MJ, et al. Performance of the fixed pressure valve with antisiphon device SPHERA® in the treatment of normal pressure hydrocephalus and prevention of overdrainage. Arq Neuropsiquiatr. 2016 Jan;74(1):55-61. https://doi.org/10.1590/0004-282X20150190
  » https://doi.org/10.1590/0004-282X20150190
• ⁴
  Oliveira MF, Reis RC, Trindade EM, Pinto FC. Evidences in the treatment of idiopathic normal pressure hydrocephalus. Rev Assoc Med Bras (1992). 2015 May-Jun;61(3):258-62. https://doi.org/10.1590/1806-9282.61.03.258
  » https://doi.org/10.1590/1806-9282.61.03.258
• ⁵
  Oliveira MF, Oliveira JR, Rotta JM, Pinto FC. Psychiatric symptoms are present in most of the patients with idiopathic normal pressure hydrocephalus. Arq Neuropsiquiatr. 2014 Jun;72(6):435-8. https://doi.org/10.1590/0004-282X20140047
  » https://doi.org/10.1590/0004-282X20140047
• ⁶
  Oliveira MF, Saad F, Reis RC, Rotta JM, Pinto FC. Programmable valve represents an efficient and safe tool in the treatment of idiopathic normal-pressure hydrocephalus patients. Arq Neuropsiquiatr. 2013 Apr;71(4):229-36. https://doi.org/10.1590/0004-282X20130007
  » https://doi.org/10.1590/0004-282X20130007
• ⁷
  Kazui H, Mori E, Hashimoto M, Ishikawa M, Hirono N, Takeda M. Effect of shunt operation on idiopathic normal pressure hydrocephalus patients in reducing caregiver burden: evidence from SINPHONI. Dement Geriatr Cogn Disord. 2011;31(5):363-70. https://doi.org/10.1159/000328625
  » https://doi.org/10.1159/000328625
• ⁸
  Kameda M, Yamada S, Atsuchi M, Kimura T, Kazui H, Miyajima M, et al.; SINPHONI and SINPHONI-2 Investigators. Cost-effectiveness analysis of shunt surgery for idiopathic normal pressure hydrocephalus based on the SINPHONI and SINPHONI-2 trials. Acta Neurochir (Wien). 2017 Jun;159(6):995-1003. https://doi.org/10.1007/s00701-017-3115-2
  » https://doi.org/10.1007/s00701-017-3115-2
• ⁹
  Bateman GA, Loiselle AM. Can MR measurement of intracranial hydrodynamics and compliance differentiate which patient with idiopathic normal pressure hydrocephalus will improve following shunt insertion? Acta Neurochir (Wien). 2007;149(5):455-62. https://doi.org/10.1007/s00701-007-1142-0
  » https://doi.org/10.1007/s00701-007-1142-0
• ¹⁰
  Benejam B, Solana E, Poca MA, Junque C,, Sahuquillo J. Alteraciones cognitivas em pacientes com hidrocefalia crónica del adulto (“normotensiva”). Propuesta de um protocolo para su evaluación clínica. Neurocirurgía. 2008;19(4):309-21. https://doi.org/10.1016/S1130-1473(08)70217-3
  » https://doi.org/10.1016/S1130-1473(08)70217-3
• ¹¹
  Blomsterwall E, Svantesson U, Carlsson U, Tullberg M, Wikkelsö C. Postural disturbance in patients with normal pressure hydrocephalus. Acta Neurol Scand. 2000 Nov;102(5):284-91. https://doi.org/10.1034/j.1600-0404.2000.102005284.x
  » https://doi.org/10.1034/j.1600-0404.2000.102005284.x
• ¹²
  Feick D, Sickmond J, Liu L, Metellus P, Williams M, Rigamonti D, et al. Sensitivity and predictive value of occupational and physical therapy assessments in the functional evaluation of patients with suspected normal pressure hydrocephalus. J Rehabil Med. 2008 Oct;40(9):715-20. https://doi.org/10.2340/16501977-0241
  » https://doi.org/10.2340/16501977-0241
• ¹³
  Mori K. Management of idiopathic normal-pressure hydrocephalus: a multiinstitutional study conducted in Japan. J Neurosurg. 2001 Dec;95(6):970-3. https://doi.org/10.3171/jns.2001.95.6.0970
  » https://doi.org/10.3171/jns.2001.95.6.0970
• ¹⁴
  Pinto FC, Saad F, Oliveira MF, Pereira RM, Miranda FL, Tornai JB, et al. Role of endoscopic third ventriculostomy and ventriculoperitoneal shunt in idiopathic normal pressure hydrocephalus: preliminary results of a randomized clinical trial. Neurosurgery. 2013 May;72(5):845-53. https://doi.org/10.1227/NEU.0b013e318285b37c
  » https://doi.org/10.1227/NEU.0b013e318285b37c
• ¹⁵
  Toma AK, Tarnaris A, Kitchen ND, Watkins LD. Working towards patient oriented outcome assessment in normal pressure hydrocephalus, what is the most important? Acta Neurochir (Wien). 2011 Jan;153(1):177-80. https://doi.org/10.1007/s00701-010-0781-8
  » https://doi.org/10.1007/s00701-010-0781-8
• ¹⁶
  Guillemin F, Bombardier C, Beaton D. Cross-cultural adaptation of health-related quality of life measures: literature review and proposed guidelines. J Clin Epidemiol. 1993 Dec;46(12):1417-32. https://doi.org/10.1016/0895-4356(93)90142-N
  » https://doi.org/10.1016/0895-4356(93)90142-N
• ¹⁷
  Podsiadlo D, Richardson S. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc. 1991 Feb;39(2):142-8. https://doi.org/10.1111/j.1532-5415.1991.tb01616.x
  » https://doi.org/10.1111/j.1532-5415.1991.tb01616.x
• ¹⁸
  VanSwearingen JM, Brach JS. Making geriatric assessment work: selecting useful measures. Phys Ther. 2001 Jun;81(6):1233-52.
• ¹⁹
  Koh GC, Chen CH, Petrella R, Thind A. Rehabilitation impact indices and their independent predictors: a systematic review. BMJ Open. 2013 Sep;3(9):e003483. https://doi.org/10.1136/bmjopen-2013-003483
  » https://doi.org/10.1136/bmjopen-2013-003483
• ²⁰
  Chivukula S, Tempel ZJ, Zwagerman NT, Newman WC, Shin SS, Chen CJ, et al. The Dynamic Gait Index in Evaluating Patients with Normal Pressure Hydrocephalus for Cerebrospinal Fluid Diversion. World Neurosurg. 2015 Dec;84(6):1871-6. https://doi.org/10.1016/j.wneu.2015.08.021
  » https://doi.org/10.1016/j.wneu.2015.08.021
• ²¹
  Berg K, Wood-Dauphinee S, Gayton D. Measuring balance in the elderly: preliminary development of an instrument. Physiother Can. 1989;41(6):304-11. https://doi.org/10.3138/ptc.41.6.304
  » https://doi.org/10.3138/ptc.41.6.304
• ²²
  Blum L, Korner-Bitensky N. Usefulness of the Berg Balance Scale in stroke rehabilitation: a systematic review. Phys Ther. 2008 May;88(5):559-66. https://doi.org/10.2522/ptj.20070205
  » https://doi.org/10.2522/ptj.20070205
• ²³
  Kubo Y, Kazui H, Yoshida T, Kito Y, Kimura N, Tokunaga H, et al. Validation of grading scale for evaluating symptoms of idiopathic normal-pressure hydrocephalus. Dement Geriatr Cogn Disord. 2008;25(1):37-45. https://doi.org/10.1159/000111149
  » https://doi.org/10.1159/000111149
• ²⁴
  Cordero Tous N, Román Cutillas AM, Jorques Infante AM, Olivares Granados G, Saura Rojas JE, Iañez Velasco B, et al. Adult chronic idiopathic hydrocephalus-diagnosis, treatment and evolution: prospective study. Neurocirugia (Astur). 2013 May-Jun;24(3):93-101. Spanish. https://doi.org/10.1016/j.neucir.2011.12.007
  » https://doi.org/10.1016/j.neucir.2011.12.007
• ²⁵
  Owler BK, Momjian S, Czosnyka Z, Czosnyka M, Péna A, Harris NG, et al. Normal pressure hydrocephalus and cerebral blood flow: a PET study of baseline values. J Cereb Blood Flow Metab. 2004 Jan;24(1):17-23. https://doi.org/10.1097/01.WCB.0000093326.88757.49
  » https://doi.org/10.1097/01.WCB.0000093326.88757.49

Publication Dates

• Publication in this collection
  Oct 2018

History

• Received
  17 Mar 2018
• Reviewed
  24 May 2018
• Accepted
  03 July 2018