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Nutritional screening in hospitalized pediatric patients: a systematic review Please cite this article as: Teixeira AF, Viana KD. Nutritional screening in hospitalized pediatric patients: a systematic review. J Pediatr (Rio J). 2016;92:343–52. ,☆☆ ☆☆ Study associated with the Multidisciplinary Residency Program in Health, Hospital Universitário, Universidade Federal do Maranhão (UFMA), São Luís, MA, Brazil.

Abstract

Objective:

This systematic review aimed to verify the available scientific evidence on the clinical performance and diagnostic accuracy of nutritional screening tools in hospitalized pediatric patients.

Data source:

A search was performed in the Medline (National Library of Medicine United States), LILACS (Latin American and Caribbean Health Sciences), PubMed (US National Library of Medicine National Institutes of Health), in the SCIELO (Scientific Electronic Library Online), through CAPES portal (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), bases Scopus e Web of Science. The descriptors used in accordance with the Descriptors in Health Sciences (DeCS)/Medical Subject Headings (MeSH) list were “malnutrition”, “screening”, and “pediatrics”, as well as the equivalent words in Portuguese.

Summary of the findings:

The authors identified 270 articles published between 2004 and 2014. After applying the selection criteria, 35 were analyzed in full and eight articles were included in the systematic review. We evaluated the methodological quality of the studies using the Quality Assessment of Diagnostic Accuracy Studies (QUADAS). Five nutritional screening tools in pediatrics were identified. Among these, the Screening Tool for the Assessment of Malnutrition in Pediatrics (STAMP) showed high sensitivity, almost perfect inter-rater agreement and between the screening and the reference standard; the Screening Tool Risk on Nutritional Status and Growth (STRONGkids) showed high sensitivity, lower percentage of specificity, substantial intra-rater agreement, and ease of use in clinical practice.

Conclusions:

The studies included in this systematic review showed good performance of the nutritional screening tools in pediatrics, especially STRONGkids and STAMP. The authors emphasize the need to perform for more studies in this area. Only one tool was translated and adapted to the Brazilian pediatric population, and it is essential to carry out studies of tool adaptation and validation for this population.

Keywords
Screening; Malnutrition; Pediatrics; Systematic review

Resumo

Objetivo:

Esta revisão sistemática tem por objetivo verificar as evidências científicas disponíveis sobre o desempenho clínico e acurácia diagnóstica dos instrumentos de triagem nutricional em pacientes pediátricos hospitalizados.

Fonte de dados:

Realizou-se busca nas bases de dados Medline (National Library of Medicine United States), LILACS (Latin American and Caribbean Health Sciences), PubMed (US National Library of Medicine National Institutes of Health), na biblioteca eletrônica SCIELO (Scientific Electronic Library Online), através do portal de periódicos da CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), bases Scopus e Web of Science. Os descritores utilizados conforme lista do DeCS (Descritores em Ciências da Saúde)/MeSH (Medical Subject Headings) foram “desnutrição”, “triagem” e “pediatria”, bem como, “malnutrition”, “screening” e “pediatrics”, respectivamente.

Síntese dos dados:

Identificou-se 270 artigos, publicados entre 2004 e 2014. Após aplicação dos critérios de seleção, 35 foram analisados na íntegra, sendo incluídos 8 artigos na revisão sistemática. Avaliou-se a qualidade metodológica dos estudos utilizando-se o QUADAS (Quality Assessment of Diagnostic Accuracy Studies). Verificou-se 05 instrumentos de triagem nutricional em pediatria. Dentre estes, o STAMP (Screening Tool for the Assessment of Malnutrition in Pediatrics) apresentou sensibilidade elevada, concordância quase perfeita inter-avaliador e entre a triagem e padrão de referência; o STRONGkids (Screening Tool Risk on Nutritional Status and Growth) evidenciou sensibilidade elevada, menor percentual de especificidade, concordância intra-avaliador substancial e facilidade de uso na prática clínica.

Conclusões:

Os estudos incluídos nesta revisão sistemática demonstraram um bom desempenho dos instrumentos de triagem nutricional em pediatria, principalmente STRONGkids e STAMP. Evidencia-se a necessidade de mais pesquisas nessa área. Apenas um instrumento foi traduzido e adaptado para a população pediátrica brasileira, sendo imprescindível a realização de estudos de adaptação e validação de instrumentos para essa população.

Palavras-chave
Triagem; Desnutrição; Pediatria; Revisão sistemática

Introduction

It has been widely described in the literature that inadequate nutritional status has negative implications for the child, resulting in important consequences for the child's health and development.11 Hulst JM, Zwart H, Hop WC, Joosten KF. Dutch national survey to test the STRONGkids nutritional risk screening tool in hospitalized children. Am J Clin Nutr. 2010;29:106-11.33 Mehta NM, Corkins MR, Lyman B, Malone A, Goday PS, Carney LN, et al. Defining pediatric malnutrition: a paradigm shift toward etiology-related definitions. J Parenter Enteral Nutr. 2013;37:460-81.

Malnutrition in pediatric patients is a severe pathological condition and a risk factor for unfavorable outcome. It is associated with immune system vulnerability, increased risk of infections, postoperative complications, impaired wound healing, and development of pressure ulcers, as well as increased morbidity and mortality of the affected individuals.44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9.88 Costa MV, Pastore CA. Herramienta de cribado nutricional versus valoración nutricional antropométrica de niños hospitalizados: cuál método se asocia mejor con la evolución clínica? Arch Latinoam Nutr. 2015;65:12-20.

This clinical condition slows down the recovery process, demanding prolonged hospital stay and increasing costs related to medication and health care.44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9.,55 Spagnuolo MI, Liguoro I, Chiatto F, Mambretti D, Guarino A. Application of a score system to evaluate the risk of malnutrition in a multiple hospital setting. Ital J Pediatr. 2013;39:1-7.,88 Costa MV, Pastore CA. Herramienta de cribado nutricional versus valoración nutricional antropométrica de niños hospitalizados: cuál método se asocia mejor con la evolución clínica? Arch Latinoam Nutr. 2015;65:12-20.,99 Gholampour Z, Hosseininasab M, Khademi G, Sezavar M, Abdollahpour N, Imani B. Assessment of nutritional status based on STRONGkids tool in Iranian hospitalized children. Int J Child Health Nutr. 2015;4:61-6. Even with the frequent association between hospital malnutrition and risk of adverse clinical events, this is a problem that remains largely underestimated and that sometimes goes unnoticed.33 Mehta NM, Corkins MR, Lyman B, Malone A, Goday PS, Carney LN, et al. Defining pediatric malnutrition: a paradigm shift toward etiology-related definitions. J Parenter Enteral Nutr. 2013;37:460-81.,1010 Sikorová L, Zavřelová B. Evaluation of malnutrition of hospitalized children using the Screening Tool for the Assessment of Malnutrition in Paediatrics. Čas Lék Čes. 2012;151:397-400.1212 Baxter JB, Al-Madhaki FI, Zlotkin SH. Prevalence of malnutrition at the time of admission among patients admitted to a Canadian tertiary-care paediatric hospital. Paediatr Child Health. 2014;19:413-7.

In recent decades, within the scenario of the epidemiological and nutritional transition, Brazilian studies have evidenced a significant decrease in the prevalence of child malnutrition in the country.1313 Batista Filho M, Rissin A. A transição nutricional no Brasil: tendências regionais e temporais. Cad Saude Publica. 2003;19:181-91.,1414 Monteiro CA, Benício MH, Konno SC, Silva AC, Lima AL, Conde WL. Causas do declínio da desnutrição infantil no Brasil, 1996–2007. Rev Saude Publica. 2009;43:35-43. However, in opposition to a downward trend in malnutrition in the general population, the situation is getting worse in hospitals, as demonstrated by the increase in its incidence1515 Araújo MA, Lima LS, Ornelas GC, Logrado MH. Análise comparativa de diferentes métodos de triagem nutricional do paciente internado. Com Ciencias Saude. 2010;21:331-42.,1616 Waitzberg DL, Caiffa WT, Correia MI. Hospital malnutrition: the Brazilian national survey (IBRANUTRI): a study of 40,000 patients. Nutrition. 2001;17:573-80. and prevalence.1717 Leite HP. Como identificar o risco nutricional em crianças hospitalizadas?. Rev Bras Terap Intens. 2003;15:132.

Although it is difficult to quantify the actual prevalence of malnutrition in hospitalized children, scientific evidence emphasizes their frequency in this group. International studies show malnutrition rates between 19% and 45.6% in hospitalized children.11 Hulst JM, Zwart H, Hop WC, Joosten KF. Dutch national survey to test the STRONGkids nutritional risk screening tool in hospitalized children. Am J Clin Nutr. 2010;29:106-11.,1818 Dogan Y, Erkan T, Yalvac S, Altay S, Çullu Çokugras F, Aydin A, et al. Nutritional status of patients hospitalized in pediatric clinic. Turk J Gastroenterol. 2005;16:212-6.2020 Rodriguez YH, Guerra ML, Cabrera YJ, Fonte LM, Montequín ZC. Estado nutricional de los niños ingresados en el Hospital Pediátrico de Pinar del Río. Rev Ciencias Medicas. 2012;16:84-97. In Brazil, surveys indicate rates of 18% to 58%.2121 Péret Filho LA, Penna FG, Rodrigues FG, Santana DP, Hanan B, Oliveira GN, et al. Avaliação nutricional de crianças internadas em enfermaria geral de um hospital público. Pediatria (São Paulo). 2005;27:12-8.2424 Magalhães EA, Martins MA, Rodrigues CC, Moreira AS. Associação entre tempo de internação e evolução do estado nutricional de crianças internadas em um hospital universitário. Demetra. 2013;8:103-14.

During hospitalization, children can be malnourished or aggravate a pre-existing malnutrition situation. Therefore, it is essential to achieve the early detection of nutritional depletion during hospital stay.11 Hulst JM, Zwart H, Hop WC, Joosten KF. Dutch national survey to test the STRONGkids nutritional risk screening tool in hospitalized children. Am J Clin Nutr. 2010;29:106-11.,2525 Prado RC, Santos PF, Assis EM, Zaban AL. Desnutrição e avaliação nutricional subjetiva em pediatria. Com Ciencias Saude. 2010;21:61-70.

In this sense, the patient nutritional status assessment identifies only those who are already malnourished, and not those at risk of malnutrition.55 Spagnuolo MI, Liguoro I, Chiatto F, Mambretti D, Guarino A. Application of a score system to evaluate the risk of malnutrition in a multiple hospital setting. Ital J Pediatr. 2013;39:1-7.,2626 Sermet-Gaudelus I, Poisson-Salomon A-S, Colomb V, Brusset M-C, Mosser F, Berrier F, et al. Simple pediatric nutritional risk score to identify children at risk of malnutrition. Am J Clin Nutr. 2000;72:64-70. To prevent hospital malnutrition, studies show that the early detection of nutritional risk is essential, as it allows appropriate nutritional interventions to prevent malnutrition and its consequences.22 Jonkers C, Klos M, Kouwenoord K, Kruizenga H, Remijnse W. Guideline screening and treatment of malnutrition. Translation of the Dutch guideline screening and treatment of malnutrition; 2011, version June 2011. Available from: http://www.fightmalnutrition.eu [cited 20 Jan 2015].
http://www.fightmalnutrition.eu...
,44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9.,55 Spagnuolo MI, Liguoro I, Chiatto F, Mambretti D, Guarino A. Application of a score system to evaluate the risk of malnutrition in a multiple hospital setting. Ital J Pediatr. 2013;39:1-7.,88 Costa MV, Pastore CA. Herramienta de cribado nutricional versus valoración nutricional antropométrica de niños hospitalizados: cuál método se asocia mejor con la evolución clínica? Arch Latinoam Nutr. 2015;65:12-20.,1212 Baxter JB, Al-Madhaki FI, Zlotkin SH. Prevalence of malnutrition at the time of admission among patients admitted to a Canadian tertiary-care paediatric hospital. Paediatr Child Health. 2014;19:413-7.,2727 Eufrásio RE. Avaliação nutricional subjetiva global em pediatria: Adaptação e análise de um questionário [Monografia]. Natal (RN): Universidade Federal do Rio Grande do Norte; 2014.

For adult patients, several screening tools have been validated in a variety of clinical scenarios and with different groups of patients.44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9. However, appropriate tools for pediatric use are scarce,2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6.,2929 White M, Lawson K, Ramsey R, Dennis N, Hutchinson Z, Soh XY, et al. A simple nutrition screening tool for pediatric inpatients. J Parenter Enteral Nutr. 2014;20:1-7. and there is no consensus about the best method to assess risk of malnutrition in these patients.11 Hulst JM, Zwart H, Hop WC, Joosten KF. Dutch national survey to test the STRONGkids nutritional risk screening tool in hospitalized children. Am J Clin Nutr. 2010;29:106-11.,88 Costa MV, Pastore CA. Herramienta de cribado nutricional versus valoración nutricional antropométrica de niños hospitalizados: cuál método se asocia mejor con la evolución clínica? Arch Latinoam Nutr. 2015;65:12-20.,3030 Carvalho FC, Lopes CR, Vilela LC, Vieira MA, Rinaldi AE, Crispim CA. Tradução e adaptação cultural da ferramenta STRONGkids para triagem do risco de desnutrição em crianças hospitalizadas. Rev Paul Pediatr. 2013;31:159-65.

Although there are recommendations of several societies to perform nutritional risk identification in pediatric patients,33 Mehta NM, Corkins MR, Lyman B, Malone A, Goday PS, Carney LN, et al. Defining pediatric malnutrition: a paradigm shift toward etiology-related definitions. J Parenter Enteral Nutr. 2013;37:460-81.,3131 Kondrup J, Allison SP, Elia M, Vellas B, Plauth M. ESPEN guidelines for nutrition screening 2002. Clin Nutr. 2003;22:415-21. in practice, due to the lack of a simple and validated method, nutritional screening is not yet widely performed.44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9.,9 Gholampour Z, Hosseininasab M, Khademi G, Sezavar M, Abdollahpour N, Imani B. Assessment of nutritional status based on STRONGkids tool in Iranian hospitalized children. Int J Child Health Nutr. 2015;4:61-6. Any tool designed for nutritional screening in pediatrics should be simple, fast, reproducible,77 Villares JM, Calderón VV, García CB, Lama More R, Ferreiro SR, Quintana LP. Evaluación del estado nutricional de niños ingresados en el hospital en España; estudio DHOSPE (Desnutrición Hospitalaria en el Paciente Pediátrico en España). Nutr Hosp. 2013;28:709-18. and have good sensitivity and specificity.44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9.,2929 White M, Lawson K, Ramsey R, Dennis N, Hutchinson Z, Soh XY, et al. A simple nutrition screening tool for pediatric inpatients. J Parenter Enteral Nutr. 2014;20:1-7.,3232 Erkan T. Methods to evaluate the nutrition risk in hospitalized patients. Türk Ped Arş. 2014;49:276-81.

Therefore, this systematic review aimed to verify the available scientific evidence on the clinical performance and diagnostic accuracy of the tools used for screening malnutrition risk in pediatric patients.

Methods

This was a systematic review of the literature on the available scientific evidence on the clinical performance and diagnostic accuracy of the tools used for malnutrition risk screening in pediatric patients, published between 2004 and 2014.

The search strategy used included searches in the MEDLINE, LILACS, PubMed, the SciELO electronic library databases; the CAPES Portal was used to access the Scopus and Web of Science databases. The descriptors were chosen according to the Descriptors in Health Sciences (DeCS) and Medical Subject Headings (MeSH) list. In accordance with the DeCS list, the used terms were “desnutrição,” “triagem,” and “pediatria” in Portuguese; the MeSH descriptors were “malnutrition,” “screening,” and “pediatrics”, in English. In addition to descriptors, the Boolean operator “AND” was applied for the combination of terms in the databases.

Searches using the references of selected articles were also performed, aiming to identify publications not previously found that were relevant to the review topic. The searches were performed from November 2014 to April 2015.

The following inclusion criteria were defined for adequate article selection: studies on hospitalized pediatric patients, which assessed the use of some nutritional risk screening tool; and articles published in the last decade (2004–2014) in Portuguese, English, and/or Spanish. The exclusion criteria were: qualitative studies, review articles, editorials, letters to the editor, book chapters, articles not available to be accessed in full, and also articles that did not have data on the sensitivity and specificity of the screening tools.

The article selection process was carried out in four stages, according to the model recommended by the Cochrane Collaboration:3333 De Vet HC, Eisinga A, Riphagen II, Aertgeerts B, Pewsner D,Mitchell R. Chapter 7: searching for studies. In: Deeks JJ,Bossuyt PM, Gatsonis C, editors. Cochrane handbook for systematic reviews of diagnostic test accuracy version 1.0.0. TheCochrane Collaboration; 2008. Available from: http://www.srdta.cochrane.org [cited 18 Jan 2014].
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1 – identification of the articles by searching the databases and articles retrieved through the references of selected articles; 2 – selection, at this stage, the duplicate articles were excluded, and by screening the titles and abstracts of the remaining articles, the authors excluded those that had no association with the keywords defined for the search; 3 – the eligibility was assessed by reading the articles in full (excluding those that did not meet the pre-established eligibility criteria) and; 4 – inclusion of eligible articles in the systematic review.

To evaluate the clinical performance and diagnostic accuracy of the tools, the following criteria were considered: sensitivity – screening capacity to detect individuals who were actually at nutritional risk; specificity – the capacity to diagnose individuals with no nutritional risk; positive predictive value – the patient's probability to be at risk among those who tested positive; and negative predictive value – the patient's probability to be healthy among those who tested negative.3434 Menezes AM, Santos IS. Curso de epidemiologia básica para pneumologistas: 4ª parte–Epidemiologia clínica. J Pneumol. 1999;25:321-6.

The authors also verified whether the studies analyzed the reproducibility and reliability of the screening tools, using data from the agreement analysis between the assessed nutritional risk screening and the used reference standard, as well as the intra- and inter-bserver agreement shown in the studies. To interpret the Kappa statistical value, the classification of Landis and Koch was considered:3535 Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159-75. no agreement (<0); poor agreement (0–0.19); mild agreement (0.20–0.39); moderate agreement (0.40–0.59); substantial agreement (0.60–0.79); and almost perfect agreement (0.80–1.00).

To assess the methodological quality of the studies, a modified version of Quality Assessment of Diagnostic Accuracy Studies (QUADAS) was used.3636 Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;3:1-13. Recommended by the Cochrane Handbook,3737 Reitsma JB, Rutjes AW, Whiting P, Vlassov VV, Leeflang MMG,Deeks JJ. Chapter 9: assessing methodological quality. In: DeeksJJ, Bossuyt PM, Gatsonis C, editors. Cochrane handbook for systematic reviews of diagnostic test accuracy version 1.0.0. TheCochrane Collaboration; 2009. Available from: http://srdta.cochrane.org [cited 24 Jan 2014].
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this tool is designed to measure the sources of bias, variability, and quality of information in the studies.3636 Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;3:1-13. This version evaluates 11 of the 14 items of the original version, considering that the remaining items (2, 8, and 9) refer to problems related to how to report data, and not exactly to the methodological quality of the study.3838 Ministério da Saúde, Brasil, Secretaria de Ciência, Tecnologia e Insumos Estratégicos, Departamento de Ciência e Tecnologia. Diretrizes metodológicas: elaboração de revisão sistemática e metanálise de estudos de acurácia diagnóstica. Brasília: Ministério da Saúde, Secretaria de Ciência, Tecnologia e Insumos Estratégicos, Departamento de Ciência e Tecnologia, Ministérioda Saúde; 2014, v. 1. A good study performance is verified when it has a positive evaluation in at least eight of the 11 items of QUADAS.3939 Simões PW. Prevalência de papilomavírus humano no câncer de mama e apoio ao diagnóstico de câncer de mama pelas redes bayesianas: revisão sistemática e metanálise [Thesis]. Criciúma (SC): Universidade do Extremo Sul Catarinense; 2012.

Results

Initially, 270 articles were identified, and at the end of the selection process, according to the model recommended by the Cochrane Collaboration, eight articles were quantified, which met all the pre-established eligibility criteria and, therefore, were included in this systematic review (Fig. 1).

Figure 1
Flowchart of article selection for the systematic review, according to the Cochrane Collaboration model.

Of the eight selected studies, three (37.5%) were published in 2012. The age of the individuals who participated in the studies ranged from 1 month to 18 years. A complete description of the articles is shown in Table 1.

Table 1
Characterization of the articles included in the systematic review.

The assessment of the methodological quality of the articles showed that most (62.5%, n = 5) had “good methodological performance”. In three of the articles (37.5%), the sample was not representative of the population. The authors observed heterogeneity in the choice of the reference standard. In this respect, two studies (25%) did not have an adequate reference standard (anthropometry), and furthermore, the information of four studies (50%) did not allow to verify whether the interpretation of results of the reference test and the index test was independently performed in the included studies, or if there was review bias. The result of the methodological quality assessment, according to the modified version of QUADAS,3636 Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;3:1-13. is shown in Fig. 2.

Figure 2
Results of the methodological quality evaluation of each study included in the systematic review, according to QUADAS. , Yes; ×, No; ?, Unclear.

The analysis of the studies showed the use of five nutritional risk screening tools in hospitalized pediatric patients: Screening Tool for the Assessment of Malnutrition in Pediatrics (STAMP)4040 McCarthy H, Dixon M, Crabtree I, Eaton-Evans MJ, McNulty H. The development and evaluation of the Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMPª) for use by healthcare staff. J Hum Nutr Diet. 2012;25:311-8.4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. in four (50%) of the studies, Screening Tool Risk on Nutritional Status and Growth (STRONGkids)55 Spagnuolo MI, Liguoro I, Chiatto F, Mambretti D, Guarino A. Application of a score system to evaluate the risk of malnutrition in a multiple hospital setting. Ital J Pediatr. 2013;39:1-7.,4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6.,4444 Huysentruyt K, Alliet P, Muyshont L, Rossignol R, Devreker T, Bontems P, et al. The STRONGkids nutritional screening tool in hospitalized children: a validation study. Nutrition. 2013;29:1356-61. in three (37.5%), Pediatric Yorkhill Malnutrition Score (PYMS)2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6.,4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. in two (25%), Pediatric Nutrition Screening Tool (PNST)2929 White M, Lawson K, Ramsey R, Dennis N, Hutchinson Z, Soh XY, et al. A simple nutrition screening tool for pediatric inpatients. J Parenter Enteral Nutr. 2014;20:1-7. in one (12.5%), and the Subjective Global Nutritional Assessment (SGNA)2929 White M, Lawson K, Ramsey R, Dennis N, Hutchinson Z, Soh XY, et al. A simple nutrition screening tool for pediatric inpatients. J Parenter Enteral Nutr. 2014;20:1-7. in one (12.5%).

The sensitivity of the screening tools ranged from 59%2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6. to 100%.4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. STAMP and STRONGkids showed the best results regarding sensitivity (100%).

Most tools had a specificity between 53%55 Spagnuolo MI, Liguoro I, Chiatto F, Mambretti D, Guarino A. Application of a score system to evaluate the risk of malnutrition in a multiple hospital setting. Ital J Pediatr. 2013;39:1-7. and 92%;2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6. for this parameter, STRONGkids and STAMP had the lowest percentages of specificity, 7.7%4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. and 11.54%,4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. respectively, whereas PYMS had high specificity (92%).2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6. It was also observed that all studies had high negative predictive value (between 73.6% and 100%).

The agreement between nutritional risk screening and the reference standard was verified in four of the studies (50%), with better performance of STAMP4040 McCarthy H, Dixon M, Crabtree I, Eaton-Evans MJ, McNulty H. The development and evaluation of the Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMPª) for use by healthcare staff. J Hum Nutr Diet. 2012;25:311-8. (k = 0.882, 95% CI: 0.646–1.000). Regarding the interobserver agreement, it varied from moderate (0.40–0.59)2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6. to almost perfect (0.80–1.00);4040 McCarthy H, Dixon M, Crabtree I, Eaton-Evans MJ, McNulty H. The development and evaluation of the Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMPª) for use by healthcare staff. J Hum Nutr Diet. 2012;25:311-8.,4141 Lama More RA, López AM, Álvarez MH, Chicano C, Martínez RG, Ruzafa EL. Validación de una herramienta de cribado nutricional para pacientes pediátricos hospitalizados. Nutr Hosp. 2012;27:1429-36. the STAMP tool showed the best interobserver agreement. For the intraobserver agreement, STRONGkids4444 Huysentruyt K, Alliet P, Muyshont L, Rossignol R, Devreker T, Bontems P, et al. The STRONGkids nutritional screening tool in hospitalized children: a validation study. Nutrition. 2013;29:1356-61. showed the best performance, with substantial agreement (k ≥ 0.60–.79; Table 2).

Table 2
Sensitivity, specificity, predictive values, and reproducibility of the studies included in the systematic review.

Discussion

A systematic review is a valuable tool, both in individual diagnostic test assessment and to compare different tests in a same target-condition. Its results may dispel clinical doubts or explore other questions, showing the way so that the answer can be found in the best way.4545 Iared W, Valente O. Revisões sistemáticas de estudos de acurácia. Diagn Tratamento. 2009;14:85-8.

This systematic review of diagnostic accuracy studies synthesized the results of several studies that evaluated nutritional risk screening tools to be used in hospitalized pediatric patients.

The methodological quality of most studies was considered high. The main methodological problems were related to lack of adequate information to determine whether the interpretation of the nutritional screening used was independent or whether there was influence of the knowledge of the reference standard results, or vice versa, characterizing a review bias of the results.

In this aspect, the review bias can lead to inflated measures of diagnostic accuracy, and also, depending on the degree of subjectivity associated to the index test (screening), its interpretation can be strongly influenced when the standard reference result is known.3636 Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J. The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol. 2003;3:1-13.

In 37.5% of the studies, the sample was not representative, contrary to what recommends the Cochrane Handbook for diagnostic accuracy studies,3737 Reitsma JB, Rutjes AW, Whiting P, Vlassov VV, Leeflang MMG,Deeks JJ. Chapter 9: assessing methodological quality. In: DeeksJJ, Bossuyt PM, Gatsonis C, editors. Cochrane handbook for systematic reviews of diagnostic test accuracy version 1.0.0. TheCochrane Collaboration; 2009. Available from: http://srdta.cochrane.org [cited 24 Jan 2014].
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which recommends that an appropriate sample should be defined, configuring one of the main factors that can affect the test accuracy.

Regarding the reference standard used, this is still a controversial point, given the lack of a universally accepted gold standard for the diagnosis of nutritional risk in children.4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6.

Among the studies, it was observed that some used the assessment performed by a nutritionist as a reference standard. This parameter is considered inappropriate by other authors, who point out that not all countries have nutrition professionals, and their role can vary depending on the country.3232 Erkan T. Methods to evaluate the nutrition risk in hospitalized patients. Türk Ped Arş. 2014;49:276-81.,4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6.,4646 Joosten KF, Huslt JM. Nutritional screening tools for hospitalized children: methodological considerations. Clin Nutr. 2014;33:1-5. In this matter, anthropometrics has been better assessed as a reference standard, since it uses universally accepted parameters4444 Huysentruyt K, Alliet P, Muyshont L, Rossignol R, Devreker T, Bontems P, et al. The STRONGkids nutritional screening tool in hospitalized children: a validation study. Nutrition. 2013;29:1356-61. and is recommended by an international reference organization.4747 Hecht C, Weber M, Grote V, Daskalou E, Dell’era L, Flynn D, et al. Disease associated malnutrition correlates with length of hospital stay in children. Clin Nutr. 2014;34:53-59.

The nutritional screening tool must be able to identify those patients that may benefit from the intervention, because they are either at risk of having or developing complications that are avoidable through adequate nutritional support.4141 Lama More RA, López AM, Álvarez MH, Chicano C, Martínez RG, Ruzafa EL. Validación de una herramienta de cribado nutricional para pacientes pediátricos hospitalizados. Nutr Hosp. 2012;27:1429-36.

Screening methods consist in the systematization of questions that investigate the existence of characteristics that may reflect or be related to nutritional deterioration.1515 Araújo MA, Lima LS, Ornelas GC, Logrado MH. Análise comparativa de diferentes métodos de triagem nutricional do paciente internado. Com Ciencias Saude. 2010;21:331-42. In th is regard, nutritional screening detects only the presence of malnutrition risk. Conversely, nutritional assessment, not only detects malnutrition, but also classifies its degree and allows for the collection of information to assist in its correction.4848 Raslan M, González MC, Dias MCG, Paes-Barbosa FC, Cecconello I, Waitzberg DL. Aplicabilidade dos métodos de triagem nutricional no paciente hospitalizado. Rev Nutr Campinas. 2008;21:553-61.

The STAMP tool was validated in a study performed in the United Kingdom.4949 McCarthy H, McNulty H, Dixon M, Eaton-Evans MJ. Screening for nutrition risk in children: the validation of a new tool. J Hum Nutr Diet. 2008;21:395-6. This nutritional screening tool considers three elements: the patient's clinical diagnosis and its nutritional implications (if any), the child's nutritional intake during hospitalization, and anthropometric measurements (where the measured value of the child's height and weight is recorded and compared to reference values by age and gender).1010 Sikorová L, Zavřelová B. Evaluation of malnutrition of hospitalized children using the Screening Tool for the Assessment of Malnutrition in Paediatrics. Čas Lék Čes. 2012;151:397-400.

The PYMS was developed and validated by Gerasimides et al.2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6. in the United Kingdom. It evaluates four predictors or recognized symptoms of malnutrition risk: body mass index (BMI), recent weight loss history, changes in food intake, and the expected effect of the current medical condition on the patient's nutritional status.2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6.

The STRONGkids, proposed by Hulst et al. in a multicenter study in the Netherlands,11 Hulst JM, Zwart H, Hop WC, Joosten KF. Dutch national survey to test the STRONGkids nutritional risk screening tool in hospitalized children. Am J Clin Nutr. 2010;29:106-11. is a questionnaire comprising four areas: global subjective assessment; nutritional risk of the patient's disease (presence of high-risk disease or predicted major surgery); nutritional intake and losses (decreased food intake, diarrhea and vomiting), and loss or absence of weight gain.11 Hulst JM, Zwart H, Hop WC, Joosten KF. Dutch national survey to test the STRONGkids nutritional risk screening tool in hospitalized children. Am J Clin Nutr. 2010;29:106-11.,3030 Carvalho FC, Lopes CR, Vilela LC, Vieira MA, Rinaldi AE, Crispim CA. Tradução e adaptação cultural da ferramenta STRONGkids para triagem do risco de desnutrição em crianças hospitalizadas. Rev Paul Pediatr. 2013;31:159-65.,5050 Ferreira AC. Caracterização Nutricional de Crianças e Adolescentes com diagnóstico de doença oncológica. Porto (PO): Universidade do Porto; 2012.,5151 Moeeni V, Walls T, Day AS. Assessment of nutritional status and nutritional risk in hospitalised Iranian children. Acta Paediatr. 2012;101:446-51. This is the only tool translated and culturally adapted into Portuguese.3030 Carvalho FC, Lopes CR, Vilela LC, Vieira MA, Rinaldi AE, Crispim CA. Tradução e adaptação cultural da ferramenta STRONGkids para triagem do risco de desnutrição em crianças hospitalizadas. Rev Paul Pediatr. 2013;31:159-65.

The PNST was designed by White et al.2929 White M, Lawson K, Ramsey R, Dennis N, Hutchinson Z, Soh XY, et al. A simple nutrition screening tool for pediatric inpatients. J Parenter Enteral Nutr. 2014;20:1-7. in Australia. It consists of four simple yes/no questions related to involuntary weight loss in recent days, poor weight gain in recent months, decrease in food intake in recent weeks and, also, if the child is thin or obese.3232 Erkan T. Methods to evaluate the nutrition risk in hospitalized patients. Türk Ped Arş. 2014;49:276-81. Nutritional risk is considered when there are two positive answers to the questions.2929 White M, Lawson K, Ramsey R, Dennis N, Hutchinson Z, Soh XY, et al. A simple nutrition screening tool for pediatric inpatients. J Parenter Enteral Nutr. 2014;20:1-7.,3232 Erkan T. Methods to evaluate the nutrition risk in hospitalized patients. Türk Ped Arş. 2014;49:276-81.

The SGNA is an adaptation of the Subjective Global Assessment, which has been validated for use in pediatric patients.5252 Secker DJ, Jeejeebhoy KN. Subjective global nutritional assessment for children. Am J Clin Nutr. 2007;85:1083-9. It consists of a questionnaire that collects and analyze several data: adequacy of the current height for age; adequacy of current weight for height; unintentional weight alterations; food intake; gastrointestinal symptoms; metabolic stress from the disease; and physical examination. Although mentioned as a screening tool, it is better characterized as a structured nutritional assessment.44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9.

Based on the components evaluated in the screening tools (STAMP, STRONGkids, and PYMS), a score was obtained that corresponds to the malnutrition risk level, described as low, moderate, or high, differently from the SGNA, which classifies patients as well nourished, moderately malnourished, and severely malnourished.

With the exception of SGNA, which was developed for use in adult patients and subsequently validated for use in pediatric patients,5252 Secker DJ, Jeejeebhoy KN. Subjective global nutritional assessment for children. Am J Clin Nutr. 2007;85:1083-9. all evaluated screening tools were developed for the pediatric population.

The evaluations of diagnostic accuracy in individual studies focus on the analysis of the index test performance compared to a reference test (sensitivity and specificity) or on the implications of positive and negative results of the index test.3838 Ministério da Saúde, Brasil, Secretaria de Ciência, Tecnologia e Insumos Estratégicos, Departamento de Ciência e Tecnologia. Diretrizes metodológicas: elaboração de revisão sistemática e metanálise de estudos de acurácia diagnóstica. Brasília: Ministério da Saúde, Secretaria de Ciência, Tecnologia e Insumos Estratégicos, Departamento de Ciência e Tecnologia, Ministérioda Saúde; 2014, v. 1. In this context, Hartman et al.44 Hartman C, Shamir R, Hecht C. Malnutrition screening tools for hospitalized children. Curr Opin Clin Nutr Metab Care. 2012;15:303-9. point out that the sensitivity, specificity, and reproducibility characteristics are essential for any tool aimed at nutritional assessment in pediatrics.

The STRONGkids and STAMP tools showed higher sensitivity and very low levels of specificity. Conversely, the PYMS showed better percentage of specificity. This finding may be related to the reference standard used in the studies, considering that, among the studies that had anthropometrics as the reference standard, no significant differences were found regarding these measurements, thus confirming the importance of an appropriate reference standard selection, since this choice can have important clinical implications.4747 Hecht C, Weber M, Grote V, Daskalou E, Dell’era L, Flynn D, et al. Disease associated malnutrition correlates with length of hospital stay in children. Clin Nutr. 2014;34:53-59.

In the case of nutritional risk assessment in children, higher sensitivity and positive predictive value reflect an increased likelihood that the child who was identified at nutritional risk by the tool is actually in this situation.4040 McCarthy H, Dixon M, Crabtree I, Eaton-Evans MJ, McNulty H. The development and evaluation of the Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMPª) for use by healthcare staff. J Hum Nutr Diet. 2012;25:311-8.

The tools that have low sensitivity are more susceptible to false-negative results; therefore, children who really are at nutritional risk are not diagnosed. As for those that have low specificity, they are more likely to provide false-positive results, implying in a diagnosis of risk in patients that do not have it.

The screenings should have high sensitivity in order to minimize the number of false negatives.3434 Menezes AM, Santos IS. Curso de epidemiologia básica para pneumologistas: 4ª parte–Epidemiologia clínica. J Pneumol. 1999;25:321-6. In this context, sensitivity is more important than specificity, because a false-positive result will only expose the patient to a detailed nutritional assessment, whereas a false negative can result in an undetected malnourishment condition.4444 Huysentruyt K, Alliet P, Muyshont L, Rossignol R, Devreker T, Bontems P, et al. The STRONGkids nutritional screening tool in hospitalized children: a validation study. Nutrition. 2013;29:1356-61.

The higher the degree of sensitivity of a test, the better its negative predictive value is, and thus, the greater the certainty that the individual with a negative result actually does not have the disease. And the more specific a test is, the better its positive predictive value (that is, the greater the confidence that a person with a positive result has the disease being assessed).3434 Menezes AM, Santos IS. Curso de epidemiologia básica para pneumologistas: 4ª parte–Epidemiologia clínica. J Pneumol. 1999;25:321-6.

Regarding the analysis of reproducibility and reliability, key measures to evaluate the accuracy of a nutritional screening tool, better performance of the STAMP and STRONGkids tools was observed (inter and intraobserver agreement, respectively). For the screening tool to have a reproducible measurement, it must have a good agreement, to reflect a high level of reliability.4242 Wong S, Graham A, Harini SP, Grimble G, Forbes A. Validation of the Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMP) in patients with spinal cord injuries (SCIs). Spinal Cord. 2012;51:424-9.

Regarding the applicability in pediatric practice, the ideal screening tool is the one that can quickly and reliably evaluate the patient's nutritional risk in order to indicate those who need a more detailed assessment and intervention.3232 Erkan T. Methods to evaluate the nutrition risk in hospitalized patients. Türk Ped Arş. 2014;49:276-81.,4646 Joosten KF, Huslt JM. Nutritional screening tools for hospitalized children: methodological considerations. Clin Nutr. 2014;33:1-5. If the screening tool is extensive, it is less likely to be used by health care providers.11 Hulst JM, Zwart H, Hop WC, Joosten KF. Dutch national survey to test the STRONGkids nutritional risk screening tool in hospitalized children. Am J Clin Nutr. 2010;29:106-11.

The studies by Spagnuolo et al.55 Spagnuolo MI, Liguoro I, Chiatto F, Mambretti D, Guarino A. Application of a score system to evaluate the risk of malnutrition in a multiple hospital setting. Ital J Pediatr. 2013;39:1-7. and Huysentruyt et al.4444 Huysentruyt K, Alliet P, Muyshont L, Rossignol R, Devreker T, Bontems P, et al. The STRONGkids nutritional screening tool in hospitalized children: a validation study. Nutrition. 2013;29:1356-61. presented the STRONGkids as a simple structure tool, of practical use in routine care (mean of three minutes) and easily applied in a hospital. A study that methodologically analyzed six pediatric nutritional screening tools also pointed out the STRONGkids as the easiest, most practical, and most reliable test.4646 Joosten KF, Huslt JM. Nutritional screening tools for hospitalized children: methodological considerations. Clin Nutr. 2014;33:1-5.

A study with pediatric patients from New Zealand, comparing the PYMS, the STAMP and the STRONGkids screening tests, showed that the all three are viable and able to identify nutritional risk, but the STRONGkids was the most reliable in that population.5353 Moeeni V, Walls T, Day AS. Nutritional status and nutrition risk screening in hospitalized children in New Zealand. Acta Paediatr. 2013;102:419-23. In contrast, when comparing these same tools applied to hospitalized children in Indonesia, Wonoputri et al.4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. recommend the PYMS as the most reliable in that setting.

The STAMP is described as a more detailed instrument, with longer application time (±10 min), possibly due to the interpretation of growth charts.1010 Sikorová L, Zavřelová B. Evaluation of malnutrition of hospitalized children using the Screening Tool for the Assessment of Malnutrition in Paediatrics. Čas Lék Čes. 2012;151:397-400. In this regard, the SGNA is reported as an extensive and time-consuming tool.4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. The STRONGkids has been considered faster to apply due to the exclusion of weight and height;1111 Durakbaşa ÇU, Fettahoğlu S, Bayar A, Mutus M, Okur H. The prevalence of malnutrition and effectiveness of STRONGkids tool in the identification of malnutrition risks among pediatric surgical patients. Balkan Med J. 2014;31:313-21. however, some authors55 Spagnuolo MI, Liguoro I, Chiatto F, Mambretti D, Guarino A. Application of a score system to evaluate the risk of malnutrition in a multiple hospital setting. Ital J Pediatr. 2013;39:1-7.,4343 Wonoputri N, Djais JT, Rosalina I. Validity of nutritional screening tools for hospitalized children. J Nutr Metab. 2014;2014:1-6. regards the exclusion of an objective evaluation as a disadvantage of this tool.

The studies included in this review showed that most nutritional screening tools in pediatric patients are viable for nutritional risk screening in pediatrics. However, all the tools presented advantages and limitations, which is in agreement with several studies that reinforce the need for more research in the area.2828 Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM. A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr. 2010;104:751-6.,4040 McCarthy H, Dixon M, Crabtree I, Eaton-Evans MJ, McNulty H. The development and evaluation of the Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMPª) for use by healthcare staff. J Hum Nutr Diet. 2012;25:311-8.,5454 Ling RE, Hedges V, Sullivan PB. Nutritional risk in hospitalised children: an assessment of two instruments. E Spen Eur E J Clin Nutr Metab. 2011;6:153-7.5656 Marginean O, Pitea AM, Voidazan S, Marginean C. Prevalence and assessment of malnutrition risk among hospitalized children in romania. J Health Popul Nutr. 2014;32:97-102. Moreover, only one of these tools has been translated and adapted into Portuguese language, which is a gap in the scientific production in this area.

Internationally, there are several recommendations regarding the performance of nutritional screening; however, they focus on adults and the elderly, due to the lack of an appropriate tool to identify nutritional risk in children on hospital admission.4040 McCarthy H, Dixon M, Crabtree I, Eaton-Evans MJ, McNulty H. The development and evaluation of the Screening Tool for the Assessment of Malnutrition in Paediatrics (STAMPª) for use by healthcare staff. J Hum Nutr Diet. 2012;25:311-8. In this sense, Sykorová and Zavřelová1010 Sikorová L, Zavřelová B. Evaluation of malnutrition of hospitalized children using the Screening Tool for the Assessment of Malnutrition in Paediatrics. Čas Lék Čes. 2012;151:397-400. emphasize the need for pediatric screening tools that are not only implemented, but truly functional, being targets of international accreditation standards and indicators of quality of care.

Furthermore, nutritional risk screening should be followed by regular assessments at the monitoring during hospitalization.4646 Joosten KF, Huslt JM. Nutritional screening tools for hospitalized children: methodological considerations. Clin Nutr. 2014;33:1-5. In this respect, STRONGkids, STAMP, and PYMS were originally designed for regular use in patients with prolonged hospital stay. However, their applicability for this objective requires further investigations.

Regarding the limitations of this systematic review, although the search process was extensive and detailed, there is a probability that important information has been lost due to articles published in other languages rather than English, Spanish, and Portuguese.

Conclusion

Nutritional risk screening is essential for the care of hospitalized pediatric patients. As for the choice of the screening tool to be used in hospital practice, it is imperative to know the aspects related to their clinical performance and diagnostic accuracy.

The studies included in this systematic review showed good clinical performance of the malnutrition risk screening tools in pediatric patients, mainly the STRONGkids and STAMP tools.

However, more research is necessary in order to explore the several aspects of the clinical application of these tools. Brazilian studies on this subject are incipient. Only the STRONGkids tool has been translated and adapted for the population of hospitalized Brazilian children, and therefore, it is critical for future studies to adapt and validate the other tools, considering their clinical performance and diagnostic accuracy for this population.

  • Please cite this article as: Teixeira AF, Viana KD. Nutritional screening in hospitalized pediatric patients: a systematic review. J Pediatr (Rio J). 2016;92:343–52.
  • ☆☆
    Study associated with the Multidisciplinary Residency Program in Health, Hospital Universitário, Universidade Federal do Maranhão (UFMA), São Luís, MA, Brazil.

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Publication Dates

  • Publication in this collection
    Jul-Aug 2016

History

  • Received
    17 July 2015
  • Accepted
    26 Aug 2015
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