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Revista Brasileira de Terapia Intensiva

AMIB - Associação de Medicina Intensiva Brasileira


ISSN: 0103-507X
Online ISSN: 1982-4335

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Cartolano FC, Caruso L, Soriano FG. Terapia nutricional enteral: aplicação de indicadores de qualidade. Rev Bras Ter Intensiva. 2009;21(4):376-383



Original Article

Enteral nutritional therapy: application of quality indicators

Terapia nutricional enteral: aplicação de indicadores de qualidade

Flávia De Conti CartolanoI, Lúcia CarusoII, Francisco Garcia SorianoIII

INutritionist, Trainee at Hospital Universitário da Universidade de São Paulo's Nutrition and Dietetics Service - USP - São Paulo (SP), Brazil
IINutritionist, Hospital Universitário da Universidade de São Paulo's Nutrition and Dietetics Service - USP - São Paulo (SP), Brazil
IIIPhysician for the Adult Intensive Care Unit - Hospital Universitário da Universidade de São Paulo - USP - São Paulo (SP), Brazil

Submitted on June 30, 2009
Accepted on October 20, 2009

Corresponding author:

Flávia De Conti Cartolano
Av. Professor Lineu Prestes, 2565 - Cidade Universitária - 1º A
ZIP: 05508-900 - São Paulo (SP), Brasil
Phone/Fax: (11) 3039-9357



OBJECTIVE: Monitor the adequacy of enteral nutritional therapy at the intensive care unit aiming to improve the quality of nutritional assistance.
METHODS: Prospective and observational study developed at the adult intensive care unit from 2005 to 2008. Patients over 18 years of age with exclusive enteral nutritional therapy for over 72h participated in the sample. The average values and the percentile adequacy of energy and proteins calculated, prescribed and administered in each year were analyzed. The factors responsible for the non-conformity of the administration planned were classified into intensive care unit extrinsic or intrinsic causes. The quality indicators proposed by the ILSI Brazil were applied, and expressed into percentile goals. In the statistic analyses, confidence interval and the t Student e Mann-Whitney (p<0.05) tests were used, according to the Epi Info program.
RESULTS: One hundred and sixteen patients were followed up. There were statically difference in values of energy and protein administered in 2005 and in 2006, when compared to those in 2008. The adequacy calculated/prescribed remained close to 100% in all the surveys and the adequacy administered/prescribed increased from 74% in 2005, to 89% in 2008. An increase in interruptions of enteral nutritional therapy for external factors and the decrease in interruptions for intensive care unit internal factors were verified. The quality indicators equally reflect the evolution of the patient care.
CONCLUSION: In the four yearly surveys, a progressive enhancement of nutritional support was verified. Quality indicators allow nutritional care evolution monitoring, the comparison to other services data, and are a new perspective for enteral nutritional therapy assessment.

Keywords: Nutritional therapy; Enteral nutrition; Nutritional assessment




The intensive care quality assurance concept has been increasingly discussed.(1) The nutritional support is currently seen as an additional therapeutic tool for this kind of care, and is fundamental for the patient's management when oral ingestion is not feasible.(2)

Severely ill patients, with a prolonged and complicated course, have intensive metabolic response, generally featuring hypermetabolism, with increased protein catabolism.(3) Thus, these patients have increased nutritional status depletion risk, which can additionally harm their clinical picture.

Currently available literature data suggest that early and appropriate enteral nutritional therapy (ENT) introduction may considerably decrease infections incidence and the hospital stay length.(1,4) However, intensive care patients frequently have nutritional support inadequacies, both for daily energy needs overestimation,(5) and late ENT introduction, and interruption for procedures.(6)

Thus, in the last years several studies were conducted aiming to evaluate non-conformity of the forecasted and administered calories and proteins. Another investigational issue regards the most contributing factors for ENT interruption. These trials showed a low adequacy rate for the administered versus the patients' needs, with the values ranging between 50 and 90%.(1,7,8)

In this context, this study aimed to evaluate the enteral nutritional therapy adequacy among adult patients in an intensive care unit (ICU).

Considering that this trial was conducted yearly since 2005, the 2008 data were compared versus the previous ones,(9-11) with a new analysis perspective, using the International Life Sciences Institute's Nutrition Committee Clinical Nutrition Taskforce nutritional therapy quality indicators.(12)



This was prospective observational trial. The project was cleared by the Institution's Ethics Committee (CEP 603/05) and all patients signed an Informed Consent Form.

The data survey was conducted for periods between 53 and 120 days per analyzed year. Only patients receiving at least 72 hours EN (enteral nutrition) were included. Exclusion criteria: concomitant oral and/or parenteral nutrition, non-adherence to the informed consent, and palliative care. The nutritional needs calculations were based on the usual body weight, either adjusted or estimated (ideal age weight, according to standard reference tables).(13-15) The energy-protein recommendations for each clinical status were made according to the unit pre-established protocol.(9) As those were all bed restricted patients in heart or respiratory disease situations, the total energy expenditure was estimated using the Harris-Benedict formula, adding an activity factor of 1.2. For surgical patients, in addition to this factor, an injury factor was also added, ranging according the surgery. In renal or liver insufficiency cases, or sepsis, the calculation was based on the calories per bodyweight (kilograms) recommendation.

All enteral nutrition lines were installed in the post-pyloric region, being the positioning confirmed by X-ray examination. The diets were given using a closed system, with continued infusion during an average 22 hours/day, with the remainder 2 hours reserved for procedures and drugs administration. As per the unit protocol,(16) all patients started ENT with an infusion rate of 25 mL/hour, increasing 10 mL/hour every four hours until reaching 55 mL/hour. After this, each patient progressed to the specific individual target. The available enteral formulas were normocaloric normoproteic, normocaloric hyperproteic or hypercaloric and hyperproteic.

The data collection was started on the first enteral nutrition day, and lasted until the nutritional therapy was discontinued, patient's death or discharge from the unit. The daily collected data included: 24 hours infused volume, number of intestinal movements and, in case of interruption, the event related factors. These causes were differentiated as intrinsic and extrinsic to the unit.

The caloric-protein adequacy by comparison of the calculated and the prescribed, and by the prescribed and the given was estimated as a percent ratio, considering as the standard reference value a figure above 90%.(17,18) For these calculations, data before the patient reached the proposed nutritional target infusion speed were not considered.

The 2008 results were compared to those from 2005, 2006 and 2007.(9-11) For this the Student t test was used for analyzing parametrical variables, the Mann-Whitney U test was used for non-parametric variables, both with p< 0.05 significance level and the confidence interval for the proportions. These tests were conducted using the Epi Info version 3.5.1 statistical software.

The quality indicators used are agreed with the issued by ILSI Brazil.(12) The parameters evaluated are shown in table 1.



A total of 116 patients were evaluated, being 33 in 2005, 30 in 2006, 20 in 2007 and 33 in 2008. The Table 2 shows the population and the enteral nutrition therapy characterization, according to the year.

It can be seen that no statistically significant differences were found for 2008 regarding mean age, gender distribution, ENT aspects and ICU stay length, allowing the ENT-related criteria comparison, as shown in tables 3 and 4.

Since the first survey, an increase in the mean time needed to start the ENT was seen, from 25.3 hours in 2005 to 28.6 hours in 2008. A slight drop was seen only when the 2008 data were compared to the 2007 ones, however the differences were not significant.

Regarding the nutritional target, the mean time to reach it has been dropping, as well as the number of patients reaching the target came to its maximal value. It should be stressed that in 2005, 97% of the patients reached the proposed target speed.(10) In the consecutive years, 100% of the patients reached this target. Regarding the persistence with enteral nutrition, the values ranged with the surveys.

The calculated energetic nutritional targets were, in all surveys, about 25 kcal/kg/day, and regarding proteins, the calculations were also very similar with the years. It was also observed that the prescribed target neared the initially calculated in all analyzed periods, except for proteins prescription in 2005, as hyperproteic formulas were only introduced in this unit in 2006.

During the surveys there was a positive approximation between the prescribed nutritional target and the actually administered energy and protein values, with statistical differences between the 2005 and 2006 results, and the 2008 results. This becomes more evident when analyzed under the adequacy rate perspective (Table 4) as, while in the first follow-up year the adequacy rate versus prescribed was 74% both for calories and proteins, in 2008 this was around 89%.

In the figure 1 the percent distribution of causes leading to EN discontinuation is shown. It is noticeable that, concomitant to an increase in the discontinuations for extrinsic issues, there was a decrease in EN discontinuation for intrinsic unit issues.

From all causes (Figures 2 and 3), tracheostomy was the 2008's most contributing external cause for percent inadequacy in EN administration. It can also be seen an increase with the years in the proportion of EN pauses for procedures. Regarding intrinsic causes, it can be said that these are trending to a balanced distribution, however with an increased participation of interruptions for gastrointestinal complications (18.3%). On the other hand, it has been possible to reduce, since 2006, the fasting time needed for extubation, as well as naso-enteral tube (NET)-related issues.

Regarding the quality indicators used (Table 5), the results show that 100% of the ENT patients had their energy and protein estimated needs attended. The frequency of patients with inappropriate fasting time before ENT ranged with the years from 10 to 20%, the results being within the proposed target. The frequency of inadvertent displacement of enteral tubes was low as well.

Initially almost 40% of the total EN days had administered calories inadequacy. For proteins, this percent was lower, about 30%. However, in 2008 these values were approximately 19% and 15%, respectively.

Regarding the indicator quantifying the diarrhea frequency, it was not possible to calculate for all years. It was seen that in 2008 this frequency was 6.76%, i.e., within the proposed target (<10%).



Early EN introduction has been associated with lower infection complication rates and reduced ICU stay lengths.(19-21) Although the time to ENT start increased in the studied population, these time averages (from the patient admission until EN start) remained below 48 hours in all years, i.e., within the guidelines' proposed times, which are between 24 and 48 hours.(19-20) In a study by O'Meara et al.,(22) the average time to EN start in critical mechanic ventilation patients was 39.7 hours (±36.3h).

Regarding the nutritional target, the patients have been increasingly reaching it within a shorter average time. This suggests that the unit-adopted protocol favors an appropriate progression of the enteral formula, reducing risks, complications and promoting a rapid and effective course, contributing to minimize the nutritional wastage in this period.(10)

The energetic nutritional targets, calculated based in an average 25 kcal/kg/day agrees with the Intensive Care Nutritional Therapy Guide, which recommends during the acute phase to provide 20 to 25 kcal/kg/day and during the recovery and stabilization phase 25 to 30 kcal/kg/day.(20) Considering the average of what was actually given during the enteral nutrition (Table 3), it can be seen a significant difference for the 2008 results versus those for 2005 and 2006. It becomes then clear that the patients, in average, have being receiving values closer to the recommended.

Considering as conformity percent values above 90%, an improvement could be seen in the nutritional assistance with the years. Looking at the values found regarding ENT administration adequacy in the four surveys, it is clear that the adult ICU practices are increasingly effective, also additionally emphasizing the importance of the previously established enteral nutrition infusion protocol.(16) What can have contributed for the observed quality results, in addition to the protocol, is the work of a continuously educated Multidisciplinary Nutritional Therapy Team.

Different studies have found given/prescribed adequacy rates below the found for 2008. Van den Broek et al.,(8) analyzing just energy adequacy in exclusive EN patients, found an 87% average adequacy. O'Meara et al.,(22) found values close to 50%, ranging according to the hospitalization day. Reid et al.,(5) studying the energy-protein administration adequacy for above 72 hours mechanic ventilation patients observed in average 81% for energy and 76% for protein adequacy. Previous studies found even lower rates. (7,17,23,24)

This picture implies a considerable nutritional deficit, evidencing the difficulty to provide an actual ENT infusion closer to the calculated values. At the same time, it stresses the importance of identifying the causes of the ENT administration interruptions, allowing strategies implementation which can minimize their effects.(10)

EN administration is rendered difficult by directly intensive care-related issues, as hemodynamic instability, fasting for tests and nursing procedures, NET mechanic problems, among others.(9,25) In the literature, the most mentioned causes for EN interruptions involve nursing procedures, gastrointestinal intolerances (vomiting, high gastric residues volume), tube repositioning, tests and surgical interventions.(5,17,18,22) In this trial, the main cause extrinsic to the ICU for EN infusion interruption was the tracheostomy procedure, while, regarding the intrinsic causes, the main reason for ENT pause was gastrointestinal complications. A trial by Rice et al.(7) found that only 9% of the pauses were due to gastrointestinal issues, while O'Leary-Kelley et al.,(18) found it in 36.7%.

The results found with the quality indicators also mirrored improved nutritional assistance. Since the continued system was introduced as the local ICU ENT infusion method, when also the evaluations were started, 100% of the EN patients had their caloric and protein needs calculated.

It can be noticed that the frequency of inadvertent displacement of enteral tube was low. A possible explanation for the low inadvertent NET displacement frequency is that only displacements where the NET had to be replaced, letting out, e.g., tube migrations from post-pyloric to gastric position, as it was not possible collecting these data.

Regarding inappropriate caloric-protein offer days rate, the results observed are consistent in terms of calories (<20%), however a little above for the proteins established target (<10%). Nevertheless, although the insufficient protein days rate didn't reach the aimed value, the yearly percent decline shows that we are moving towards our target. Taking the 2008 results, a significant difference (p<0.05) versus previous years (2005, 2006 and 2007) was seen, evidencing a favorable progression towards reaching this quality indicator target.

According to the literature-adopted diarrhea definition, its incidence may range from 16 to 63%.(26) In the paper by Elpern et al.,(25) where the same methodology for diarrhea characterization as this trial was used, diarrhea frequency was of 38% total EN days, while our result for 2008 it was only 6.76%.

Thus, it can be seen that ENT nutritional assistance has shown values compliant to the quality indicators-applied proposed targets. Application of these indicators in ENT is a new evaluation perspective, and allow monitoring the assistance quality and long term data comparisons with other services. However, as this analysis was based on a recent publication, no other results were found that allowed a comparison with other units, what likely will be very soon possible.



In the four consecutive yearly surveys performed, we observed an evolution, also with statistically significant differences for the results observed, and this was continuous and reached the scientific literature-recommended values. Thus, patients under nutritional therapy should be routinely monitored. This proposal is of paramount importance, taking into consideration the difficulties involving nutritional evaluation in critically ill patients.



1. Santana-Cabrera L, O'Shanahan-Navarro G, García-Martul M, Ramírez Rodríguez A, Sánches-Palacios M, Hernández-Medina E. Calidad del soporte nutricional artificial en una unidad de cuidados intensivos. Nutr Hosp. 2006;21(6):661-6.

2. Petros S, Engelmann L. Enteral nutrition delivery and energy expenditure in medical intensive care patients. Clin Nutr. 2006;25(1):51-9.

3. Villet S, Chiolero RL, Bollman MD, Revelly JP, Cayeux R N MC, Delarue J, Berger MM. Negative impact of hypocaloric feeding and energy balance on clinical outcome in ICU patients. Clin Nutr. 2005;24(4):502-9.

4. Marik PE, Zaloga GP. Early enteral nutrition in acutely ill patients: a systematic review. Crit Care Med. 2001;29(12):2264-70. Erratum in: Crit Care Med. 2002;30(3):725.

5. Reid C. Frequency of under- and overfeeding in mechanically ventilated ICU patients: causes and possible consequences. J Hum Nutr Diet. 2006;19(1):13-22.

6. Heyland DK, Schroter-Noppe D, Drover JW, Jain M, Keefe L, Dhaliwal R, Day A. Nutrition support in the critical care setting: current practice in canadian ICUs - opportunities for improvement? JPEN J Parenter Enteral Nutr.2003;27(1):74-83.

7. Rice TW, Swope T, Bozeman S, Wheeler AP. Variation in enteral nutrition delivery in mechanically ventilated patients. Nutrition. 2005;21(7-8):786-92.

8. van den Broek PW, Rasmussen-Conrad EL, Naber AH, Wanten GJ. What you think is not what they get: significant discrepancies between prescribed and administered doses of tube feeding. Br J Nutr. 2009;101(1):68-71.

9. Teixeira ACC, Caruso L, Soriano FG. Terapia nutricional enteral em unidade de terapia intensiva: infusão versus necessidades. Rev Bras Ter Intensiva. 2006;18(4):331-7.

10. Aranjues AL, Teixeira ACC, Caruso L, Soriano FG. Monitoração da terapia nutricional enteral em UTI: indicador de qualidade? Mundo Saúde (1995). 2008;32(1):16-23.

11. Chaves CG. Monitorização da terapia nutricional enteral na unidade de terapia intensiva. [Monografia de conclusão do Programa de Aprimoramento em Nutrição Hospitalar]. São Paulo: Hospital Universitário da Universidade de São Paulo; 2007.

12. Waitzberg DL, coordenador. Indicadores de qualidade em terapia nutricional. São Paulo: ILSI Brasil; 2008.

13. Burr ML, Phillips KM. Anthropometric norms in the elderly. Br J Nutr. 1984;51(2):165-9.

14. Cutts ME, Dowdy RP, Ellersieck MR, Edes TE. Predicting energy needs in ventilator-dependent critically ill patients: effect of adjusting weight for edema or adiposity. Am J Clin Nutr. 1997;66(5):1250-6.

15. Mahan LK, Escott-Stump S, editores. Krause alimentos, nutrição e dietoterapia. 10a ed. São Paulo: Roca; 2002.

16. Maia FOM, Hoshino WI, Caruso L. Protocolo de nutrição enteral. In: Soriano FG, Nogueira AC. Manual de terapia intensiva do hospital universitário da USP. São Paulo: Savier; No prelo 2009.

17. Binnekade JM, Tepaske R, Bruynzeel P, Mathus-Vliegen EM, de Hann RJ. Daily enteral feeding practice on the ICU: attainment of goals and interfering factors. Crit Care. 2005;9(3):R218-25.

18. O´Leary-Kelley CM, Puntilho KA, Barr J, Stotts N, Douglas MK. Nutritional adequacy in patients receiving mechanical ventilation who are fed enterally. Am J Crit Care. 2005;14(3):222-31.

19. Heyland DK, Dhaliwal R, Drover JW, Gramlich L, Dodek P; Canadian Critical Care Clinical Practice Guidelines Committee. Canadian clinical practice guidelines for nutrition support in mechanically ventilated, critically ill adult patientes. JPEN J Parenter Enteral Nutr. 2003;27(5):355-73.

20. Kreymann KG, Berger MM, Deutz NE, Hiesmayr M, Jolliet P, Kazandjiev G, Nitenberg G, van den Berghe G, Wernerman J; DGEM (German Society for Nutritional Medicine), Ebner C, Hartl W, Heymann C, Spies C; ESPEN (European Society for Parenteral and Enteral Nutrition). ESPEN Guidelines on Enteral Nutrition: Intensive care. Clin Nutr. 2006;25(2):210-23.

21. Kattelmann KK, Hise M, Russell M, Charney P, Stokes M, Compher C. Preliminary evidence for a medical nutrition therapy protocol: enteral feedings for critically ill patients. J Am Diet Assoc. 2006;106(8):1226-41. Review.

22. O'Meara D, Mireles-Cabodevila E, Frame F, Hummell AC, Hammel J, Dweik RA, Arroliga AC. Evaluation of delivery of enteral nutrition in critically ill patients receiving mechanical ventilation. Am J Crit Care. 2008;17(1):53-61.

23. Heyland DK, Dhaliwal R, Day A, Jain M, Drover J. Validation of the Canadian clinical pratice guidelines for nutrition support in mechanically ventilated, critically ill adult patients: results of a prospective observational study. Crit Care Med. 2004;32(11):2260-6.

24. Kyle UG, Genton L, Heidegger CP, Maisonneuve N, Karsegard VL, Huber O, et al. Hospitalized mechanically ventilated patients are at higher risk of enteral underfeeding than non-ventilated patients. Clin Nutr. 2006;25(5):727-35.

25. Elpern EH, Stutz L, Peterson S, Gurka DP, Skipper A. Outcomes associated with enteral tube feedings in a medical intensive care unit. Am J Crit Care. 2004;13(3):221-7.

26. Cremonini F, Caro SD, Nista EC, Bartolozzi F, Capelli G, Gasbarrini G, Gasbarrini A. Meta-analysis: the effect of probiotic administration on antibiotic-associated diarrhea. Aliment Pharmacol Ther. 2002;16(8):1461-7.



From the Nutrition and Dietetics Service - Hospital Universitário da Universidade de São Paulo - USP - São Paulo (SP), Brazil.



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