- Email: [email protected]
Randomized clinical trial of nutritional counseling for malnourished hospital patients
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Revista Clínica Española www.elsevier.es/rce
ORIGINAL ARTICLE
Randomized clinical trial of nutritional counseling for malnourished hospital patients夽 C. Casalsa,∗ , N. García-Agua-Solerb , M.Á. Vázquez-Sánchezc , M.V. Requena-Torod , L. Padilla-Romerod , J.L. Casals-Sáncheze a
Departamento de Fisiología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigaciones Biomédicas, Facultad de Ciencias del Deporte, Universidad de Granada, Granada, Spain b Departamento de Farmacología y Pediatría, Cátedra de Economía de la Salud y Uso Racional del Medicamento, Facultad de Medicina, Universidad de Málaga, Málaga, Spain c Centro de Salud San Andrés Torcal, Distrito Sanitario Málaga-Guadalhorce, Málaga, Spain d Hospital Clínico Universitario Virgen de la Victoria, Málaga, Spain e Sección de Reumatología, Hospital Clínico Universitario Virgen de la Victoria, Málaga, Spain Received 7 December 2014; accepted 11 February 2015
KEYWORDS Malnutrition; Targeted counseling; Public health nursing; Quality of life; Mortality; Body weight; Daily activities; Long-term care; Patient readmission; Diet
Abstract Introduction: Malnutrition is associated with an increased risk of mortality and morbidity, longer hospital stays and general loss of quality of life. The aim of this study is to assess the impact of dietary counseling for malnourished hospital patients. Patients and methods: Prospective, randomized, open-label study of 106 hospital patients with malnutrition (54 in the control group and 52 in the intervention group). The intervention group received dietary counseling, and the control group underwent standard treatment. We determined the patients’ nutritional state (body mass index, laboratory parameters, malnutrition universal screening tool), degree of dependence (Barthel index), quality of life (SF-12), degree of satisfaction (CSQ-8), the number and length of readmissions and mortality. Results: The patients who underwent the ‘‘intervention’’ increased their weight at 6 months, while the controls lost weight (difference in body mass index, 2.14 kg/m2 ; p < .001). The intervention group had better results when compared with the control group in the Malnutrition Universal Screening Tool scores (difference, −1.29; p < .001), Barthel index (difference, 7.49; p = .025), SF-12 (difference, 13.72; p < .001) and CSQ-8 (difference, 4.34, p < .001) and required fewer readmissions (difference, −0.37; p = .04) and shorter stays for readmissions (difference, −6.75; p = .035). Mortality and laboratory parameters were similar for the 2 groups.
夽 Please cite this article as: Casals C, García-Agua-Soler N, Vázquez-Sánchez MÁ, Requena-Toro MV, Padilla-Romero L, CasalsSánchez JL. Ensayo clínico aleatorizado del asesoramiento nutricional en pacientes desnutridos hospitalizados. Rev Clin Esp. 2015. http://dx.doi.org/10.1016/j.rce.2015.02.012 ∗ Corresponding author. E-mail address: [email protected] (C. Casals).
2254-8874/© 2015 Published by Elsevier España, S.L.U.
RCENG-1129; No. of Pages 7
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C. Casals et al. Conclusions: Nutritional counseling improved the patients’ nutritional state, quality of life and degree of dependence and decreased the number of hospital readmissions. © 2015 Published by Elsevier España, S.L.U.
PALABRAS CLAVE Desnutrición; Consejo dirigido; Enfermería en salud comunitaria; Calidad de vida; Mortalidad; Peso corporal; Actividades cotidianas; Cuidado a largo plazo; Readmisión del paciente; Dieta
Ensayo clínico aleatorizado del asesoramiento nutricional en pacientes desnutridos hospitalizados Resumen Introducción: La desnutrición se asocia a un mayor riesgo de mortalidad y morbilidad, a estancias hospitalarias más largas y a un deterioro general de la calidad de vida. Este estudio se propone evaluar en pacientes desnutridos hospitalizados el impacto del asesoramiento dietético. Pacientes y métodos: Estudio prospectivo, aleatorizado, abierto, en 106 pacientes hospitalizados con desnutrición (54 grupo control, 52 en el de «intervención»). El grupo «intervención» recibió asesoramiento dietético y el grupo control el tratamiento habitual. Se determinó el estado nutricional (índice de masa corporal, parámetros analíticos, Malnutrition Universal Screening Tool), el grado de dependencia (índice de Barthel), la calidad de vida (SF-12), el grado de satisfacción de los pacientes (CSQ-8), el número y días de reingresos hospitalarios y la mortalidad. Resultados: Los pacientes sometidos a «intervención» aumentaron de peso a los 6 meses, mientras que los controles perdieron peso (diferencia en el IMC de 2,14 kg/m2 [p < 0,001]). El grupo «intervención» mostró mejores resultados respecto al grupo control en las puntuaciones obtenidas en el Malnutrition Universal Screening Tool (diferencia −1,29; p < 0,001), Barthel (diferencia 7,49; p = 0,025), SF-12 (diferencia 13,72; p < 0,001), y CSQ-8 (diferencia 4,34, p < 0,001), y precisaron de un menor número de reingresos (diferencia −0,37; p = 0,04) y de días de rehospitalización (diferencia −6,75; p = 0,035). La mortalidad y los parámetros analíticos fueron similares en grupos. Conclusiones: El asesoramiento nutricional mejoró el estado nutricional, la calidad de vida y el grado de dependencia de los pacientes, además disminuyó el número de reingresos hospitalarios. © 2015 Publicado por Elsevier España, S.L.U.
Background In developed countries, malnutrition especially affects hospitalized individuals, with a prevalence that varies (according to the definition of malnutrition employed and the characteristics of each study’s patients1,2 ) between 20% and 50%.3---6 Malnutrition in hospital patients is associated with longer hospital stays, an increased risk of readmission and higher mortality rates.1,7 It is estimated that hospital costs can be up to 75% higher for malnourished patients.8 Oral nutritional supplements have demonstrated their usefulness in improving the nutritional state in various clinical conditions.9,10 Malnutrition can also be treated using nutritional counseling.11 However, the efficacy of counseling is still a matter of debate, even though a number of studies have indicated that it improves the nutritional state of patients with various chronic diseases.12---15 Systematic reviews have highlighted the considerable heterogeneity in the results of the nutritional counseling employed.16,17 Although the efficacy of counseling in increasing patients’ dietary intake and weight appears to have been proven, there is no conclusive evidence regarding other
circumstances such as mortality, hospital readmissions, length of hospital stay and functional capacity.11,16,17 The method for implementing the intervention and the coordination and continuity of nursing care after hospital discharge appears to improve the results of counseling.11,18 The aim of this study was to assess the effects of a 6month intervention program on dietary counseling compared with standard treatment on the nutritional state of hospitalized patients with malnutrition secondary to a disease after hospital discharge.
Patients and methods This was a randomized, open clinical trial with a 6-month follow-up, conducted by case manager nurses from hospital and community care, at Hospital Clinic Virgen de la Victoria of Malaga and from 9 primary care centers of the healthcare district of Malaga-Guadalhorce, between October 1, 2010 and April 30, 2013. The study was approved by the Research Ethics Committee of the Malaga Healthcare District and was conducted in accordance with the Declaration of Helsinki
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were not undergoing treatment with dietary supplements or enteral or parenteral nutrition. The patient was then informed of the study and asked for their informed consent. Once the patient had been included, they were randomized. The inclusion criteria were the following: (a) hospitalization, (b) medium---high risk of malnutrition on the MUST scale, (c) older than 18 years, (d) willingness to participate in the study and signing of the informed consent form (in the event of cognitive impairment, the consent form was signed by the patient’s caregiver) and (e) resident of the geographical area corresponding to the participating health center. The exclusion criteria consisted of having undergone any of the following during hospitalization: (a) treatment with oral food supplements, enteral or parenteral nutrition, (b) treatment with chemotherapy or radiation therapy and (c) malabsorption syndrome. The patients assigned to the control group (group C) underwent the standard healthcare procedures, which consisted of delivering a discharge report to the patient for continuity of nursing care and a telephone call by the family nurse to the patient within 72 h of the discharge. Control patients were also provided a medical report for the followup by their family doctor during the hospital discharge. The patients assigned to the intervention group (group I) underwent nutritional counseling by case manager nurses, which began during the hospital stay and lasted 6 months. At the patient’s discharge, the case manager nurses (hospital and community) contacted the caregivers by telephone to notify them of the discharge. A continuity of care report was then issued. Within 48 h of the hospital discharge, the case manager nurse from the primary care center contacted the patient and scheduled a home visit or an office consultation, depending on the patient’s condition. The visit was scheduled for the first week after hospital discharge and included a nutritional assessment. The subsequent followup and actions depended on the malnutrition risk measured
What we know? Malnutrition affects 20---50% of hospitalized patients. The condition is associated with longer hospital stays, higher readmission rates and increased mortality. There is insufficient evidence supporting the usefulness of nutritional counseling. In this study, we assess the efficacy of a dietary counseling program on nutritional status and its consequences.
What this article provides? The nutritional counseling program, conducted by case manager nurses (hospital and primary care) for 6 months, improved the nutritional state of numerous patients and decreased their morbidity, improved their quality of life and increased their satisfaction with the care received compared with standard clinical practice. The Editors
(2008 version), the current law on the protection of personal data (Law 14/1999) and the law on the protection of patient rights (Law 15/2002). Screening was conducted to determine patient eligibility during their hospitalization, using the computer program Nutritional Filter (Filtro Nutricional, FILNUT).19 The disease types that motivated these hospitalizations are listed in Table 1. If the presence of a significant risk was detected, we proceeded with the assessment of each patient using the Malnutrition Universal Screening Tool (MUST).20 If a medium---high risk of malnutrition was detected, the patient was offered the opportunity to join the study provided they
Table 1
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Diagnoses that motivated the hospitalization of patients in the study. Control group n = 54
Biliary-pancreatic disease Heart failure Pneumonia and pleural effusion Other heart diseases Inguinal hernia Femoral neck fracture Neoplastic disease Peripheral vascular disease Renal failure Upper gastrointestinal hemorrhage Iron-deficiency anemia Cerebrovascular disease Bowel obstruction Closed patella fracture Anal fistulas and fissures Extrapyramidal disease
Intervention group n = 52
Total hospitalizations
Surgical departments
Total hospitalizations
Surgical departments
15 6 9 5 5 4 2 3 1 2 1 1 0 0 0 0
12 0 1 5 5 4 1 1 0 0 0 0 0 0 0 0
9 9 5 7 4 4 3 1 3 1 1 1 1 1 1 1
6 3 2 7 4 4 3 1 1 1 0 0 0 1 1 0
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C. Casals et al. Assessed for selection 538 patients Excluded: 432 patients Did not meet the criteria: 428 patients Declined to participate: 4 patients 106 patients randomized to groups 52 patients in the intervention group
54 patients in the control group 6 deaths 1 loss during follow-up
6 deaths
47 patients included in the analysis
46 patients included in the analysis
Figure 1
Flow diagram of patients included in the study.
by the MUST scale, conforming to the protocol described by the Malnutrition Action Group of the British Association for Parenteral and Enteral Nutrition.20 (a) For medium risk, specific dietary counseling was provided, the first step of which was to conduct a dietary history aimed at assessing the potential difficulties with properly following the diet. These difficulties included beliefs, trouble chewing and swallowing and diseases. The patient’s nutritional needs were also calculated, and a personalized diet was developed based on the identified problems and underlying diseases. At 15 days, the total dietary intake of the 2 previous days was assessed. If the intake was appropriate or improved, the assessment and dietary counseling were repeated at 1 month and subsequently every 2 months until the final assessment at 6 months of hospital discharge was completed. If the intake was inadequate or worsened, the malnutrition was treated as high risk. (b) For high risk, treatment was starting with specific dietary counseling and strategies to enrich the diet with ordinary food. Patients at high risk were reassessed at 2 weeks, and if there was no improvement in intake and weight gain, they were referred to their family doctor to determine if they should be referred to the Clinical Nutrition and Dietetics Unit. If the intake had improved and weight had increased, the patient was assessed each month. If, according to MUST, the patient transitioned to medium risk during follow-up, the patient was assessed every 2 months until the final assessment was completed 6 months after the discharge. The main study endpoint for assessing the nutritional state was the body mass index (BMI). The secondary endpoints for assessing the nutritional state included the results of the MUST scale, the number of patients who were still at risk of medium---high malnutrition after completing the study and the following laboratory parameters: total protein, albumin and cholesterol levels and total lymphocyte count. Morbidity was assessed using the number of
unscheduled hospital readmissions and length of the hospital stays resulting from these readmissions. The patientperceived quality of life was assessed using the Short Form 12 Health Survey (SF-12).21 The degree of functional dependence was assessed using the Barthel index.22 Patient satisfaction with the intervention was measured using the Client Satisfaction Questionnaire (CSQ-8).23 The sample size was calculated by considering BMI the most relevant variable and that BMI presented a distribution with a standard deviation of 3.26 in the adult Spanish population. If we consider a difference of 2.0 points in the BMI as clinically relevant (with an alpha and beta error of 0.05 and 0.20, respectively), 2 samples of 51 participants would be required, if we chose a 1:1 ratio between the samples. A descriptive study of the collected variables was conducted using their mean and standard deviation for continuous variables and frequency and percentages for categorical, ordinal and nominal variables. The goodness of fit to normal was determined based on the Kolmogorov---Smirnov test, rejecting normality if p < .1. The analysis variables at 6 months of follow-up were the before and after differences in each group. The comparison of means between the groups was performed using Student’s t-test for normal continuous variables, indicating the 95% confidence interval (95% CI). For non-normal continuous variables, we used the Mann---Whitney U test. To compare categorical variables, we applied the chi-squared test. To analyze the difference in risk reduction on the MUST scale, we used the comparison of proportions test. The odds ratio (OR) was calculated, with its 95% CI calculated using logistic regression. The SPSS 20.0 and Epidat 3.1 statistical programs were employed, setting statistical significance to p < .05.
Results A total of 106 patients were randomized, 54 to group C and 52 to group I. Group C had 1 loss during follow-up due to a change of address. There were also 6 losses due to death in each of the groups. Therefore, the final analysis included a total of 93 patients, 47 in group C and 46 in
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Table 2 Characteristics of patients included in the study (data expressed as mean [standard deviation] or frequency [percentage]).
Age (years) Sex (female) Weight (kg) Body mass index (kg/m2 ) Need for surgery Hospital stay (days) Proteins (g/dL) Albumin (g/dL) Cholesterol (mg/dL) Lymphocyte (103/L) MUST Barthel index SF-12 Overall Physical component Mental component
Control group (n = 54)
Intervention group (n = 52)
p
73 26 63.4 24.2 29 14.6 5.8 2.5 147.3 1.67 2.4 62.5
73 27 62.5 24.3 37 21.0 5.6 2.4 143.5 1.36 2.6 58.6
(13) (52%) (13.17) (4.35) (71%) (17.08) (1.00) (0.44) (33.93) (0.57) (1.27) (28.84)
.640 .698 .529 .277 .123 .021* .316 .076 .456 .786 .354 .928
37.9 (13.66) 33.9 (12.35) 41.9 (15.65)
.890 .963 .616
(12) (48%) (11.55) (3.78) (55%) (8.24) (1.04) (0.76) (38.00) (1.49) (1.27) (28.54)
38.7 (13.56) 34.2 (11.98) 43.3 (15.67)
Abbreviations: MUST, malnutrition universal screening tool; SF-12, Short Form 12 Health Survey. * p < .05.
group I (Fig. 1). The initial general characteristics demonstrated by the study patients are shown in Table 2. The 2 groups were similar, with no significant differences between them, except for the hospital stay of the first hospitalization, which was longer for group I (6.4 ± 1.2 days). During the 6-month follow-up, food supplements were prescribed for 2 patients in group C and 1 patient in group I due to a worsening nutritional state (according to the MUST scale). The differences found at the end of the study in the variables measured at the start and end of follow-up (6 months later) are shown in Table 3. BMI was reduced in group C (mean change, −0.395 ± 2.43 kg/m2 ), while BMI increased in group I (mean change, 1.745 ± 2.06 kg/m2 ). The difference between the groups was 2.14 ± 0.47 kg/m2 . The MUST
score was 1.170 (1.67) points higher in group I than in the group C (p < .001). The MUST score showed a low risk at the end of the study for 19/47 patients in group C (40.4%; 95% CI 25.33---55.12%) compared with 39/46 patients in group I (84.8%; 95% CI 73.32---96.25%), for a difference of 44.4% (95% CI 24.8---64.0%; p < .001). The satisfaction with the intervention assessed using CSQ-8 was greater in group I than in group C (28.11 ± 3.57 vs. 23.77 ± 3.50; difference, 4.34 points; 95% CI 2.89---5.80; p < .01). Group C had 0.62 (1.11) readmissions/patient compared with 0.25 (0.40) in group I (difference, 0.37 readmissions/patient; p = .040). During follow-up, the patients in group C required 8.77 (24.77) days for readmissions, while those in group I required only 2.02 (4.53) days (difference,
Table 3 Changes in the nutritional parameters of the control and intervention groups after 6 months of follow-up. Data are expressed as mean (standard deviation). Control group (n = 54) Weight (kg) Body mass index (kg/m2 ) Proteins (g/dL) Albumin (g/dL) Cholesterol (mg/dL) Lymphocyte (103/L) MUST Barthel index SF-12 Overall Physical component Mental component
−0.903 −0.395 0.936 0.691 19.45 0.308 −1.170 9.362
(6.12) (2.43) (1.23) (0.74) (37.96) (1.40) (1.67) (19.07)
1.79 (12.86) 2.68 (11.86) 0.91 (14.23)
Intervention group (n = 52) 4.750 1.745 0.861 0.983 33.71 0.714 −2.457 16.848
(5.12) (2.06) (0.92) (0.66) (35.20) (0.66) (1.39) (19.29)
15.51 (15.07) 14.66 (15.19) 16.37 (15.71)
Abbreviations: MUST, malnutrition universal screening tool; SF-12, Short Form 12 Health Survey. a Mann---Whitney U. b Student t. * p < .05.
Difference
p
5.65 2.14 −0.23 0. 292 14.26 0.41 1.29 7.49
<.001*,a <.001*,a .749b .061b .070b .220a <.001*,a .025*,a
13.72 11.97 15.46
<.001*,b <.001*,b <.001*,b
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6.75 days; p = .035). There were no differences in mortality between the 2 groups, with 6/52 patients (11.54%) in group I versus 6/53 (11.32%) patients in group C (chi-squared, 0.001; p = .972).
Conflicts of interest
Discussion
Acknowledgements
The results of the study indicate that nutritional counseling is more effective than standard practice for improving the nutritional state of malnourished patients after hospitalization. The increase in BMI after nutritional counseling is consistent with the results of studies by other authors.24,25 However, the differences in the laboratory parameters did not achieve statistical significance, although the results suggest a more favorable outcome for the patients who underwent nutritional counseling. Moreover, the patients who were given nutritional counseling required fewer readmissions, suggesting that the intervention improved the overall health condition of the patients who followed the program. The patients who followed the nutritional counseling also had a better quality of life and a greater degree of independence. Improved quality of life after nutritional counseling has been previously reported12,26 but not the improvement in the functional independence index. An earlier study27 showed a tendency toward improved independence but did not achieve statistical significance. However, nutritional counseling had no effect on mortality. There could be numerous reasons for this result. On one hand, the advanced age and the underlying disease could have acted as unchangeable factors of mortality. On the other hand, the length of the intervention and followup might not have been sufficient. The majority of studies conducted to date have not reported any effect of nutritional counseling on mortality.13,16,17 However, the study by Ravasco et al.12 showed a reduction in mortality starting the fourth year of follow-up in patients with colorectal cancer who underwent dietary counseling when compared with control patients. Our study, with a 6-month follow-up and 106 patients, might not have sufficient power to detect differences in mortality due to the intervention. A significant limitation of our study is the lack of masking of the patients and health professionals, given that it was not possible to standardize a simulated educational intervention. To minimize potential biases, the final assessment and data analysis were performed by professionals other than those who conducted the intervention and follow-up. Despite the recommendations on this issue,1,3,5 many hospitals do not systematically conduct nutritional screening. The results of our study suggest that, for malnourished hospital patients, a 6-month interlevel nutritional counseling program (conducted by case manager nurses) is able to improve their nutritional state, quality of life, morbidity, functional independence and satisfaction to a greater degree than standard clinical practice.
The authors would like to thank the following nursing professionals for their collaboration in the study: María del Pilar Aguilar Trujillo, Yolanda Carrión Velasco, Pilar Castro López, José María Cruz Giráldez, Miguel García Jiménez, Remedios Madue˜ no Meléndez, Esperanza Martín Salvador, María de los Remedios Reina Campos, José Luis Sánchez del Campo, Carolina Sánchez Zayas, Rosalía Rioja Vázquez, Inmaculada Valero Cantero. We thank them for participating selflessly in the project and for employing their experience in patient health education.
Funding Project funded by a research grant from the Government of Andalusia (project PI-0489/2009).
The authors declare that they have no conflicts of interest.
References 1. Barker LA, Gout BS, Crowe TC. Hospital malnutrition: prevalence, identification and impact on patients and the healthcare system. Int J Environ Res Public Health. 2011;8:514---27. 2. Löser C. Malnutrition in hospital: the clinical and economic implications. Dtsch Arztebl Int. 2010;107:911---7. 3. Meijers JM, Halfens RJ, van Bokhorst-de vander Schueren MA, Dassen T, Schols JM. Malnutrition in Dutch health care: prevalence, prevention, treatment, and quality indicators. Nutrition. 2009;25:512---9. 4. Tsaousi G, Panidis S, Stavrou G, Tsouskas J, Panagiotou D, Kotzampassi K. Prognostic indices of poor nutritional status and their impact on prolonged hospital stay in a Greek university hospital. Biomed Res Int. 2014;2014:924270, http://dx.doi.org/10.1155/2014/924270. 5. Schindler K, Pernicka E, Laviano A, Howard P, Schütz T, Bauer P, et al. How nutritional risk is assessed and managed in European hospitals: a survey of 21,007 patients findings from the 2007---2008 cross-sectional nutrition Day survey. Clin Nutr. 2010;29:552---9. 6. Lobo Támer G, Ruiz López MD, Pérez de la Cruz AJ. Desnutrición hospitalaria: relación con la estancia media y la tasa de reingresos prematuros. Med Clin (Barc). 2009;132: 377---84. 7. Hiesmayr M, Schindler K, Pernicka E, Schuh C, SchoenigerHekele A, Bauer P, et al. Decreased food intake is a risk factor for mortality in hospitalized patients: the Nutrition Day survey 2006. Clin Nutr. 2009;28:484---91. 8. Pérez de la Cruz A, Lobo Támer G, Ordu˜ na Espinosa R, Mellado Pastor C, Aguayo de Hoyos E, Ruíz López MD. Desnutrición en pacientes hospitalizados: prevalencia e impacto económico. Med Clin (Barc). 2004;123:201---6. 9. Allen VJ, Methven L, Gosney MA. Use of nutritional complete supplements in older adults with dementia: systematic review and meta-analysis of clinical outcomes. Clin Nutr. 2013;32:950---7. 10. Ash S, Campbell KL, Bogard J, Millichamp A. Nutrition prescription to achieve positive outcomes in chronic kidney disease: a systematic review. Nutrients. 2014;6:416---51. 11. Baldwin C, Weekes CE. Dietary counselling with or without oral nutritional supplements in the management of malnourished patients. J Human Nutr Diet. 2012;25:411---26. 12. Ravasco P, Monteiro-Grillo I, Camilo M. Individualized nutrition intervention is a major benefit to colorectal cancer patients: long-term follow-up of a randomized controlled trial of nutritional therapy. Am J Clin Nutr. 2012;96:1346---53.
+Model
ARTICLE IN PRESS
Randomized clinical trial of nutritional counseling for malnourished hospital patients 13. Platek ME. The role of dietary counseling and nutrition support in head and neck cancer patients. Curr Opin Support Palliat Care. 2012;6:438---45. 14. Grobler L, Siegfried N, Visser ME, Mahlungulu SS, Volmink J. Nutritional interventions for reducing morbidity and mortality in people with HIV. Cochrane Database Syst Rev. 2013;2:CD004536, http://dx.doi.org/10.1002/14651858. 15. Sugawara K, Takahashi H, Kasai C, Kiyokawa N, Watanabe T, Fuiji S, et al. Effects of nutritional supplementation combined with low-intensity exercise in malnourished patients with COPD. Respir Med. 2010;104:1883---9. 16. Baldwin C, Weekes CE. Asesoramiento dietético para la desnutrición secundaria a una enfermedad en adultos (Revisión Cochrane traducida). La Biblioteca Cochrane Plus. Oxford: Update Software Ltd.; 2008. p. 4. Available from: http://www.update-software.com 17. Capra S, Lamb M, Vanderkrort D, Wai-chi Chan S. Efectividad de las intervenciones en ancianos desnutridos hospitalizados. Best Practice; 2007. p. 11. Available from: http:// www.evidenciaencuidados.es/evidenciaencuidados/evidencia/ bpis/pdf/jb/2007 11 2 AncianosDesnutridos.pdf [accessed 03.02.15]. 18. Courtney M, Edwards H, Chang A, Parker A, Finlayson K, Hamilton K. Fewer emergency readmissions and better quality of life for older adults at risk of hospital readmission: a randomized controlled trial to determine the effectiveness of a 24-week exercise and telephone follow-up program. J Am Soc Geriatr. 2009;57:395---402. 19. Villalobos Gámez JL, Guzmán de Damas JM, García Almeida JM, Galindo MM, Rioja Vázquez R, Enguix Armada, et al. Filnut-escala: justificación y utilidad en el cribaje de riesgo por desnutrición dentro del proceso infornut. Farm Hosp. 2010;34:231---6.
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20. Malnutrition Action Group. In: Todoric V, Russell C, Elia M, editors. The MUST explanatory booklet. A guide to the Malnutrition Universal Screening Tool (MUST) for adults. Redditch (Worcestershire). Reino Unido: BAPEN; 2011. Available from: http://www.bapen.org.uk/pdfs/must/must explan.pdf [accessed 03.02.15]. 21. Vilagut G, Valderas JM, Ferrer M, Garín O, López-García E, Alonso J. Interpretación de los cuestionarios de salud SF-36 y SF-12 en Espa˜ na: componentes físico y mental. Med Clin (Barc). 2008;130:726---35. 22. Cid-Ruzafa J, Damián-Moreno. Valoración de la discapacidad física: el índice de Barthel. Rev Esp Salud Publica. 1997;71:127---37. 23. Roberts RE, Attkisson CC. Assessing client satisfaction among Hispanics. Eval Program Plan. 1983;6:401---13. 24. Dobrila-Dintinjana R, Trivanovi´ c D, Zeli´ c M, Radi´ c M, Dintinjana M, Petranovi´ c D, et al. Nutritional support in patients with colorectal cancer during chemotherapy: does it work. Hepatogastroenterology. 2013;60:475---80. 25. Pereira de Silva R, Santos Burgos de Araujo IL, Coelho Cabral P, Pessoa de Araujo Burgos MG. Effects of oral nutritional support in hospitalized patients with AIDS. Nutr Hosp. 2013;28: 400---4. 26. Langius JA, Zandbergen MC, Eerenstein SE, van Tulder MW, Leemans CR, Kramer MH, et al. Effect of nutritional interventions on nutritional status, quality of life and mortality in patients with head and neck cancer receiving (chemo)radiotherapy: a systematic review. Clin Nutr. 2013;32: 671---8. 27. Rüfenacht U, Rühlin M, Wegmann M, Imoberdorf R, Ballmer PE. Nutritional counseling improves quality of life and nutrient intake in hospitalized undernourished patients. Nutrition. 2010;26:53---60.
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Revista Clínica Española www.elsevier.es/rce
ORIGINAL ARTICLE
Randomized clinical trial of nutritional counseling for malnourished hospital patients夽 C. Casalsa,∗ , N. García-Agua-Solerb , M.Á. Vázquez-Sánchezc , M.V. Requena-Torod , L. Padilla-Romerod , J.L. Casals-Sáncheze a
Departamento de Fisiología, Instituto de Nutrición y Tecnología de los Alimentos, Centro de Investigaciones Biomédicas, Facultad de Ciencias del Deporte, Universidad de Granada, Granada, Spain b Departamento de Farmacología y Pediatría, Cátedra de Economía de la Salud y Uso Racional del Medicamento, Facultad de Medicina, Universidad de Málaga, Málaga, Spain c Centro de Salud San Andrés Torcal, Distrito Sanitario Málaga-Guadalhorce, Málaga, Spain d Hospital Clínico Universitario Virgen de la Victoria, Málaga, Spain e Sección de Reumatología, Hospital Clínico Universitario Virgen de la Victoria, Málaga, Spain Received 7 December 2014; accepted 11 February 2015
KEYWORDS Malnutrition; Targeted counseling; Public health nursing; Quality of life; Mortality; Body weight; Daily activities; Long-term care; Patient readmission; Diet
Abstract Introduction: Malnutrition is associated with an increased risk of mortality and morbidity, longer hospital stays and general loss of quality of life. The aim of this study is to assess the impact of dietary counseling for malnourished hospital patients. Patients and methods: Prospective, randomized, open-label study of 106 hospital patients with malnutrition (54 in the control group and 52 in the intervention group). The intervention group received dietary counseling, and the control group underwent standard treatment. We determined the patients’ nutritional state (body mass index, laboratory parameters, malnutrition universal screening tool), degree of dependence (Barthel index), quality of life (SF-12), degree of satisfaction (CSQ-8), the number and length of readmissions and mortality. Results: The patients who underwent the ‘‘intervention’’ increased their weight at 6 months, while the controls lost weight (difference in body mass index, 2.14 kg/m2 ; p < .001). The intervention group had better results when compared with the control group in the Malnutrition Universal Screening Tool scores (difference, −1.29; p < .001), Barthel index (difference, 7.49; p = .025), SF-12 (difference, 13.72; p < .001) and CSQ-8 (difference, 4.34, p < .001) and required fewer readmissions (difference, −0.37; p = .04) and shorter stays for readmissions (difference, −6.75; p = .035). Mortality and laboratory parameters were similar for the 2 groups.
夽 Please cite this article as: Casals C, García-Agua-Soler N, Vázquez-Sánchez MÁ, Requena-Toro MV, Padilla-Romero L, CasalsSánchez JL. Ensayo clínico aleatorizado del asesoramiento nutricional en pacientes desnutridos hospitalizados. Rev Clin Esp. 2015. http://dx.doi.org/10.1016/j.rce.2015.02.012 ∗ Corresponding author. E-mail address: [email protected] (C. Casals).
2254-8874/© 2015 Published by Elsevier España, S.L.U.
RCENG-1129; No. of Pages 7
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C. Casals et al. Conclusions: Nutritional counseling improved the patients’ nutritional state, quality of life and degree of dependence and decreased the number of hospital readmissions. © 2015 Published by Elsevier España, S.L.U.
PALABRAS CLAVE Desnutrición; Consejo dirigido; Enfermería en salud comunitaria; Calidad de vida; Mortalidad; Peso corporal; Actividades cotidianas; Cuidado a largo plazo; Readmisión del paciente; Dieta
Ensayo clínico aleatorizado del asesoramiento nutricional en pacientes desnutridos hospitalizados Resumen Introducción: La desnutrición se asocia a un mayor riesgo de mortalidad y morbilidad, a estancias hospitalarias más largas y a un deterioro general de la calidad de vida. Este estudio se propone evaluar en pacientes desnutridos hospitalizados el impacto del asesoramiento dietético. Pacientes y métodos: Estudio prospectivo, aleatorizado, abierto, en 106 pacientes hospitalizados con desnutrición (54 grupo control, 52 en el de «intervención»). El grupo «intervención» recibió asesoramiento dietético y el grupo control el tratamiento habitual. Se determinó el estado nutricional (índice de masa corporal, parámetros analíticos, Malnutrition Universal Screening Tool), el grado de dependencia (índice de Barthel), la calidad de vida (SF-12), el grado de satisfacción de los pacientes (CSQ-8), el número y días de reingresos hospitalarios y la mortalidad. Resultados: Los pacientes sometidos a «intervención» aumentaron de peso a los 6 meses, mientras que los controles perdieron peso (diferencia en el IMC de 2,14 kg/m2 [p < 0,001]). El grupo «intervención» mostró mejores resultados respecto al grupo control en las puntuaciones obtenidas en el Malnutrition Universal Screening Tool (diferencia −1,29; p < 0,001), Barthel (diferencia 7,49; p = 0,025), SF-12 (diferencia 13,72; p < 0,001), y CSQ-8 (diferencia 4,34, p < 0,001), y precisaron de un menor número de reingresos (diferencia −0,37; p = 0,04) y de días de rehospitalización (diferencia −6,75; p = 0,035). La mortalidad y los parámetros analíticos fueron similares en grupos. Conclusiones: El asesoramiento nutricional mejoró el estado nutricional, la calidad de vida y el grado de dependencia de los pacientes, además disminuyó el número de reingresos hospitalarios. © 2015 Publicado por Elsevier España, S.L.U.
Background In developed countries, malnutrition especially affects hospitalized individuals, with a prevalence that varies (according to the definition of malnutrition employed and the characteristics of each study’s patients1,2 ) between 20% and 50%.3---6 Malnutrition in hospital patients is associated with longer hospital stays, an increased risk of readmission and higher mortality rates.1,7 It is estimated that hospital costs can be up to 75% higher for malnourished patients.8 Oral nutritional supplements have demonstrated their usefulness in improving the nutritional state in various clinical conditions.9,10 Malnutrition can also be treated using nutritional counseling.11 However, the efficacy of counseling is still a matter of debate, even though a number of studies have indicated that it improves the nutritional state of patients with various chronic diseases.12---15 Systematic reviews have highlighted the considerable heterogeneity in the results of the nutritional counseling employed.16,17 Although the efficacy of counseling in increasing patients’ dietary intake and weight appears to have been proven, there is no conclusive evidence regarding other
circumstances such as mortality, hospital readmissions, length of hospital stay and functional capacity.11,16,17 The method for implementing the intervention and the coordination and continuity of nursing care after hospital discharge appears to improve the results of counseling.11,18 The aim of this study was to assess the effects of a 6month intervention program on dietary counseling compared with standard treatment on the nutritional state of hospitalized patients with malnutrition secondary to a disease after hospital discharge.
Patients and methods This was a randomized, open clinical trial with a 6-month follow-up, conducted by case manager nurses from hospital and community care, at Hospital Clinic Virgen de la Victoria of Malaga and from 9 primary care centers of the healthcare district of Malaga-Guadalhorce, between October 1, 2010 and April 30, 2013. The study was approved by the Research Ethics Committee of the Malaga Healthcare District and was conducted in accordance with the Declaration of Helsinki
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were not undergoing treatment with dietary supplements or enteral or parenteral nutrition. The patient was then informed of the study and asked for their informed consent. Once the patient had been included, they were randomized. The inclusion criteria were the following: (a) hospitalization, (b) medium---high risk of malnutrition on the MUST scale, (c) older than 18 years, (d) willingness to participate in the study and signing of the informed consent form (in the event of cognitive impairment, the consent form was signed by the patient’s caregiver) and (e) resident of the geographical area corresponding to the participating health center. The exclusion criteria consisted of having undergone any of the following during hospitalization: (a) treatment with oral food supplements, enteral or parenteral nutrition, (b) treatment with chemotherapy or radiation therapy and (c) malabsorption syndrome. The patients assigned to the control group (group C) underwent the standard healthcare procedures, which consisted of delivering a discharge report to the patient for continuity of nursing care and a telephone call by the family nurse to the patient within 72 h of the discharge. Control patients were also provided a medical report for the followup by their family doctor during the hospital discharge. The patients assigned to the intervention group (group I) underwent nutritional counseling by case manager nurses, which began during the hospital stay and lasted 6 months. At the patient’s discharge, the case manager nurses (hospital and community) contacted the caregivers by telephone to notify them of the discharge. A continuity of care report was then issued. Within 48 h of the hospital discharge, the case manager nurse from the primary care center contacted the patient and scheduled a home visit or an office consultation, depending on the patient’s condition. The visit was scheduled for the first week after hospital discharge and included a nutritional assessment. The subsequent followup and actions depended on the malnutrition risk measured
What we know? Malnutrition affects 20---50% of hospitalized patients. The condition is associated with longer hospital stays, higher readmission rates and increased mortality. There is insufficient evidence supporting the usefulness of nutritional counseling. In this study, we assess the efficacy of a dietary counseling program on nutritional status and its consequences.
What this article provides? The nutritional counseling program, conducted by case manager nurses (hospital and primary care) for 6 months, improved the nutritional state of numerous patients and decreased their morbidity, improved their quality of life and increased their satisfaction with the care received compared with standard clinical practice. The Editors
(2008 version), the current law on the protection of personal data (Law 14/1999) and the law on the protection of patient rights (Law 15/2002). Screening was conducted to determine patient eligibility during their hospitalization, using the computer program Nutritional Filter (Filtro Nutricional, FILNUT).19 The disease types that motivated these hospitalizations are listed in Table 1. If the presence of a significant risk was detected, we proceeded with the assessment of each patient using the Malnutrition Universal Screening Tool (MUST).20 If a medium---high risk of malnutrition was detected, the patient was offered the opportunity to join the study provided they
Table 1
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Diagnoses that motivated the hospitalization of patients in the study. Control group n = 54
Biliary-pancreatic disease Heart failure Pneumonia and pleural effusion Other heart diseases Inguinal hernia Femoral neck fracture Neoplastic disease Peripheral vascular disease Renal failure Upper gastrointestinal hemorrhage Iron-deficiency anemia Cerebrovascular disease Bowel obstruction Closed patella fracture Anal fistulas and fissures Extrapyramidal disease
Intervention group n = 52
Total hospitalizations
Surgical departments
Total hospitalizations
Surgical departments
15 6 9 5 5 4 2 3 1 2 1 1 0 0 0 0
12 0 1 5 5 4 1 1 0 0 0 0 0 0 0 0
9 9 5 7 4 4 3 1 3 1 1 1 1 1 1 1
6 3 2 7 4 4 3 1 1 1 0 0 0 1 1 0
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C. Casals et al. Assessed for selection 538 patients Excluded: 432 patients Did not meet the criteria: 428 patients Declined to participate: 4 patients 106 patients randomized to groups 52 patients in the intervention group
54 patients in the control group 6 deaths 1 loss during follow-up
6 deaths
47 patients included in the analysis
46 patients included in the analysis
Figure 1
Flow diagram of patients included in the study.
by the MUST scale, conforming to the protocol described by the Malnutrition Action Group of the British Association for Parenteral and Enteral Nutrition.20 (a) For medium risk, specific dietary counseling was provided, the first step of which was to conduct a dietary history aimed at assessing the potential difficulties with properly following the diet. These difficulties included beliefs, trouble chewing and swallowing and diseases. The patient’s nutritional needs were also calculated, and a personalized diet was developed based on the identified problems and underlying diseases. At 15 days, the total dietary intake of the 2 previous days was assessed. If the intake was appropriate or improved, the assessment and dietary counseling were repeated at 1 month and subsequently every 2 months until the final assessment at 6 months of hospital discharge was completed. If the intake was inadequate or worsened, the malnutrition was treated as high risk. (b) For high risk, treatment was starting with specific dietary counseling and strategies to enrich the diet with ordinary food. Patients at high risk were reassessed at 2 weeks, and if there was no improvement in intake and weight gain, they were referred to their family doctor to determine if they should be referred to the Clinical Nutrition and Dietetics Unit. If the intake had improved and weight had increased, the patient was assessed each month. If, according to MUST, the patient transitioned to medium risk during follow-up, the patient was assessed every 2 months until the final assessment was completed 6 months after the discharge. The main study endpoint for assessing the nutritional state was the body mass index (BMI). The secondary endpoints for assessing the nutritional state included the results of the MUST scale, the number of patients who were still at risk of medium---high malnutrition after completing the study and the following laboratory parameters: total protein, albumin and cholesterol levels and total lymphocyte count. Morbidity was assessed using the number of
unscheduled hospital readmissions and length of the hospital stays resulting from these readmissions. The patientperceived quality of life was assessed using the Short Form 12 Health Survey (SF-12).21 The degree of functional dependence was assessed using the Barthel index.22 Patient satisfaction with the intervention was measured using the Client Satisfaction Questionnaire (CSQ-8).23 The sample size was calculated by considering BMI the most relevant variable and that BMI presented a distribution with a standard deviation of 3.26 in the adult Spanish population. If we consider a difference of 2.0 points in the BMI as clinically relevant (with an alpha and beta error of 0.05 and 0.20, respectively), 2 samples of 51 participants would be required, if we chose a 1:1 ratio between the samples. A descriptive study of the collected variables was conducted using their mean and standard deviation for continuous variables and frequency and percentages for categorical, ordinal and nominal variables. The goodness of fit to normal was determined based on the Kolmogorov---Smirnov test, rejecting normality if p < .1. The analysis variables at 6 months of follow-up were the before and after differences in each group. The comparison of means between the groups was performed using Student’s t-test for normal continuous variables, indicating the 95% confidence interval (95% CI). For non-normal continuous variables, we used the Mann---Whitney U test. To compare categorical variables, we applied the chi-squared test. To analyze the difference in risk reduction on the MUST scale, we used the comparison of proportions test. The odds ratio (OR) was calculated, with its 95% CI calculated using logistic regression. The SPSS 20.0 and Epidat 3.1 statistical programs were employed, setting statistical significance to p < .05.
Results A total of 106 patients were randomized, 54 to group C and 52 to group I. Group C had 1 loss during follow-up due to a change of address. There were also 6 losses due to death in each of the groups. Therefore, the final analysis included a total of 93 patients, 47 in group C and 46 in
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Table 2 Characteristics of patients included in the study (data expressed as mean [standard deviation] or frequency [percentage]).
Age (years) Sex (female) Weight (kg) Body mass index (kg/m2 ) Need for surgery Hospital stay (days) Proteins (g/dL) Albumin (g/dL) Cholesterol (mg/dL) Lymphocyte (103/L) MUST Barthel index SF-12 Overall Physical component Mental component
Control group (n = 54)
Intervention group (n = 52)
p
73 26 63.4 24.2 29 14.6 5.8 2.5 147.3 1.67 2.4 62.5
73 27 62.5 24.3 37 21.0 5.6 2.4 143.5 1.36 2.6 58.6
(13) (52%) (13.17) (4.35) (71%) (17.08) (1.00) (0.44) (33.93) (0.57) (1.27) (28.84)
.640 .698 .529 .277 .123 .021* .316 .076 .456 .786 .354 .928
37.9 (13.66) 33.9 (12.35) 41.9 (15.65)
.890 .963 .616
(12) (48%) (11.55) (3.78) (55%) (8.24) (1.04) (0.76) (38.00) (1.49) (1.27) (28.54)
38.7 (13.56) 34.2 (11.98) 43.3 (15.67)
Abbreviations: MUST, malnutrition universal screening tool; SF-12, Short Form 12 Health Survey. * p < .05.
group I (Fig. 1). The initial general characteristics demonstrated by the study patients are shown in Table 2. The 2 groups were similar, with no significant differences between them, except for the hospital stay of the first hospitalization, which was longer for group I (6.4 ± 1.2 days). During the 6-month follow-up, food supplements were prescribed for 2 patients in group C and 1 patient in group I due to a worsening nutritional state (according to the MUST scale). The differences found at the end of the study in the variables measured at the start and end of follow-up (6 months later) are shown in Table 3. BMI was reduced in group C (mean change, −0.395 ± 2.43 kg/m2 ), while BMI increased in group I (mean change, 1.745 ± 2.06 kg/m2 ). The difference between the groups was 2.14 ± 0.47 kg/m2 . The MUST
score was 1.170 (1.67) points higher in group I than in the group C (p < .001). The MUST score showed a low risk at the end of the study for 19/47 patients in group C (40.4%; 95% CI 25.33---55.12%) compared with 39/46 patients in group I (84.8%; 95% CI 73.32---96.25%), for a difference of 44.4% (95% CI 24.8---64.0%; p < .001). The satisfaction with the intervention assessed using CSQ-8 was greater in group I than in group C (28.11 ± 3.57 vs. 23.77 ± 3.50; difference, 4.34 points; 95% CI 2.89---5.80; p < .01). Group C had 0.62 (1.11) readmissions/patient compared with 0.25 (0.40) in group I (difference, 0.37 readmissions/patient; p = .040). During follow-up, the patients in group C required 8.77 (24.77) days for readmissions, while those in group I required only 2.02 (4.53) days (difference,
Table 3 Changes in the nutritional parameters of the control and intervention groups after 6 months of follow-up. Data are expressed as mean (standard deviation). Control group (n = 54) Weight (kg) Body mass index (kg/m2 ) Proteins (g/dL) Albumin (g/dL) Cholesterol (mg/dL) Lymphocyte (103/L) MUST Barthel index SF-12 Overall Physical component Mental component
−0.903 −0.395 0.936 0.691 19.45 0.308 −1.170 9.362
(6.12) (2.43) (1.23) (0.74) (37.96) (1.40) (1.67) (19.07)
1.79 (12.86) 2.68 (11.86) 0.91 (14.23)
Intervention group (n = 52) 4.750 1.745 0.861 0.983 33.71 0.714 −2.457 16.848
(5.12) (2.06) (0.92) (0.66) (35.20) (0.66) (1.39) (19.29)
15.51 (15.07) 14.66 (15.19) 16.37 (15.71)
Abbreviations: MUST, malnutrition universal screening tool; SF-12, Short Form 12 Health Survey. a Mann---Whitney U. b Student t. * p < .05.
Difference
p
5.65 2.14 −0.23 0. 292 14.26 0.41 1.29 7.49
<.001*,a <.001*,a .749b .061b .070b .220a <.001*,a .025*,a
13.72 11.97 15.46
<.001*,b <.001*,b <.001*,b
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6.75 days; p = .035). There were no differences in mortality between the 2 groups, with 6/52 patients (11.54%) in group I versus 6/53 (11.32%) patients in group C (chi-squared, 0.001; p = .972).
Conflicts of interest
Discussion
Acknowledgements
The results of the study indicate that nutritional counseling is more effective than standard practice for improving the nutritional state of malnourished patients after hospitalization. The increase in BMI after nutritional counseling is consistent with the results of studies by other authors.24,25 However, the differences in the laboratory parameters did not achieve statistical significance, although the results suggest a more favorable outcome for the patients who underwent nutritional counseling. Moreover, the patients who were given nutritional counseling required fewer readmissions, suggesting that the intervention improved the overall health condition of the patients who followed the program. The patients who followed the nutritional counseling also had a better quality of life and a greater degree of independence. Improved quality of life after nutritional counseling has been previously reported12,26 but not the improvement in the functional independence index. An earlier study27 showed a tendency toward improved independence but did not achieve statistical significance. However, nutritional counseling had no effect on mortality. There could be numerous reasons for this result. On one hand, the advanced age and the underlying disease could have acted as unchangeable factors of mortality. On the other hand, the length of the intervention and followup might not have been sufficient. The majority of studies conducted to date have not reported any effect of nutritional counseling on mortality.13,16,17 However, the study by Ravasco et al.12 showed a reduction in mortality starting the fourth year of follow-up in patients with colorectal cancer who underwent dietary counseling when compared with control patients. Our study, with a 6-month follow-up and 106 patients, might not have sufficient power to detect differences in mortality due to the intervention. A significant limitation of our study is the lack of masking of the patients and health professionals, given that it was not possible to standardize a simulated educational intervention. To minimize potential biases, the final assessment and data analysis were performed by professionals other than those who conducted the intervention and follow-up. Despite the recommendations on this issue,1,3,5 many hospitals do not systematically conduct nutritional screening. The results of our study suggest that, for malnourished hospital patients, a 6-month interlevel nutritional counseling program (conducted by case manager nurses) is able to improve their nutritional state, quality of life, morbidity, functional independence and satisfaction to a greater degree than standard clinical practice.
The authors would like to thank the following nursing professionals for their collaboration in the study: María del Pilar Aguilar Trujillo, Yolanda Carrión Velasco, Pilar Castro López, José María Cruz Giráldez, Miguel García Jiménez, Remedios Madue˜ no Meléndez, Esperanza Martín Salvador, María de los Remedios Reina Campos, José Luis Sánchez del Campo, Carolina Sánchez Zayas, Rosalía Rioja Vázquez, Inmaculada Valero Cantero. We thank them for participating selflessly in the project and for employing their experience in patient health education.
Funding Project funded by a research grant from the Government of Andalusia (project PI-0489/2009).
The authors declare that they have no conflicts of interest.
References 1. Barker LA, Gout BS, Crowe TC. Hospital malnutrition: prevalence, identification and impact on patients and the healthcare system. Int J Environ Res Public Health. 2011;8:514---27. 2. Löser C. Malnutrition in hospital: the clinical and economic implications. Dtsch Arztebl Int. 2010;107:911---7. 3. Meijers JM, Halfens RJ, van Bokhorst-de vander Schueren MA, Dassen T, Schols JM. Malnutrition in Dutch health care: prevalence, prevention, treatment, and quality indicators. Nutrition. 2009;25:512---9. 4. Tsaousi G, Panidis S, Stavrou G, Tsouskas J, Panagiotou D, Kotzampassi K. Prognostic indices of poor nutritional status and their impact on prolonged hospital stay in a Greek university hospital. Biomed Res Int. 2014;2014:924270, http://dx.doi.org/10.1155/2014/924270. 5. Schindler K, Pernicka E, Laviano A, Howard P, Schütz T, Bauer P, et al. How nutritional risk is assessed and managed in European hospitals: a survey of 21,007 patients findings from the 2007---2008 cross-sectional nutrition Day survey. Clin Nutr. 2010;29:552---9. 6. Lobo Támer G, Ruiz López MD, Pérez de la Cruz AJ. Desnutrición hospitalaria: relación con la estancia media y la tasa de reingresos prematuros. Med Clin (Barc). 2009;132: 377---84. 7. Hiesmayr M, Schindler K, Pernicka E, Schuh C, SchoenigerHekele A, Bauer P, et al. Decreased food intake is a risk factor for mortality in hospitalized patients: the Nutrition Day survey 2006. Clin Nutr. 2009;28:484---91. 8. Pérez de la Cruz A, Lobo Támer G, Ordu˜ na Espinosa R, Mellado Pastor C, Aguayo de Hoyos E, Ruíz López MD. Desnutrición en pacientes hospitalizados: prevalencia e impacto económico. Med Clin (Barc). 2004;123:201---6. 9. Allen VJ, Methven L, Gosney MA. Use of nutritional complete supplements in older adults with dementia: systematic review and meta-analysis of clinical outcomes. Clin Nutr. 2013;32:950---7. 10. Ash S, Campbell KL, Bogard J, Millichamp A. Nutrition prescription to achieve positive outcomes in chronic kidney disease: a systematic review. Nutrients. 2014;6:416---51. 11. Baldwin C, Weekes CE. Dietary counselling with or without oral nutritional supplements in the management of malnourished patients. J Human Nutr Diet. 2012;25:411---26. 12. Ravasco P, Monteiro-Grillo I, Camilo M. Individualized nutrition intervention is a major benefit to colorectal cancer patients: long-term follow-up of a randomized controlled trial of nutritional therapy. Am J Clin Nutr. 2012;96:1346---53.
+Model
ARTICLE IN PRESS
Randomized clinical trial of nutritional counseling for malnourished hospital patients 13. Platek ME. The role of dietary counseling and nutrition support in head and neck cancer patients. Curr Opin Support Palliat Care. 2012;6:438---45. 14. Grobler L, Siegfried N, Visser ME, Mahlungulu SS, Volmink J. Nutritional interventions for reducing morbidity and mortality in people with HIV. Cochrane Database Syst Rev. 2013;2:CD004536, http://dx.doi.org/10.1002/14651858. 15. Sugawara K, Takahashi H, Kasai C, Kiyokawa N, Watanabe T, Fuiji S, et al. Effects of nutritional supplementation combined with low-intensity exercise in malnourished patients with COPD. Respir Med. 2010;104:1883---9. 16. Baldwin C, Weekes CE. Asesoramiento dietético para la desnutrición secundaria a una enfermedad en adultos (Revisión Cochrane traducida). La Biblioteca Cochrane Plus. Oxford: Update Software Ltd.; 2008. p. 4. Available from: http://www.update-software.com 17. Capra S, Lamb M, Vanderkrort D, Wai-chi Chan S. Efectividad de las intervenciones en ancianos desnutridos hospitalizados. Best Practice; 2007. p. 11. Available from: http:// www.evidenciaencuidados.es/evidenciaencuidados/evidencia/ bpis/pdf/jb/2007 11 2 AncianosDesnutridos.pdf [accessed 03.02.15]. 18. Courtney M, Edwards H, Chang A, Parker A, Finlayson K, Hamilton K. Fewer emergency readmissions and better quality of life for older adults at risk of hospital readmission: a randomized controlled trial to determine the effectiveness of a 24-week exercise and telephone follow-up program. J Am Soc Geriatr. 2009;57:395---402. 19. Villalobos Gámez JL, Guzmán de Damas JM, García Almeida JM, Galindo MM, Rioja Vázquez R, Enguix Armada, et al. Filnut-escala: justificación y utilidad en el cribaje de riesgo por desnutrición dentro del proceso infornut. Farm Hosp. 2010;34:231---6.
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20. Malnutrition Action Group. In: Todoric V, Russell C, Elia M, editors. The MUST explanatory booklet. A guide to the Malnutrition Universal Screening Tool (MUST) for adults. Redditch (Worcestershire). Reino Unido: BAPEN; 2011. Available from: http://www.bapen.org.uk/pdfs/must/must explan.pdf [accessed 03.02.15]. 21. Vilagut G, Valderas JM, Ferrer M, Garín O, López-García E, Alonso J. Interpretación de los cuestionarios de salud SF-36 y SF-12 en Espa˜ na: componentes físico y mental. Med Clin (Barc). 2008;130:726---35. 22. Cid-Ruzafa J, Damián-Moreno. Valoración de la discapacidad física: el índice de Barthel. Rev Esp Salud Publica. 1997;71:127---37. 23. Roberts RE, Attkisson CC. Assessing client satisfaction among Hispanics. Eval Program Plan. 1983;6:401---13. 24. Dobrila-Dintinjana R, Trivanovi´ c D, Zeli´ c M, Radi´ c M, Dintinjana M, Petranovi´ c D, et al. Nutritional support in patients with colorectal cancer during chemotherapy: does it work. Hepatogastroenterology. 2013;60:475---80. 25. Pereira de Silva R, Santos Burgos de Araujo IL, Coelho Cabral P, Pessoa de Araujo Burgos MG. Effects of oral nutritional support in hospitalized patients with AIDS. Nutr Hosp. 2013;28: 400---4. 26. Langius JA, Zandbergen MC, Eerenstein SE, van Tulder MW, Leemans CR, Kramer MH, et al. Effect of nutritional interventions on nutritional status, quality of life and mortality in patients with head and neck cancer receiving (chemo)radiotherapy: a systematic review. Clin Nutr. 2013;32: 671---8. 27. Rüfenacht U, Rühlin M, Wegmann M, Imoberdorf R, Ballmer PE. Nutritional counseling improves quality of life and nutrient intake in hospitalized undernourished patients. Nutrition. 2010;26:53---60.