Clinical Nutrition ESPEN xxx (2017) e1ee5
Contents lists available at ScienceDirect
Clinical Nutrition ESPEN journal homepage: http://www.clinicalnutritionespen.com
Original article
A prospective study of energy and protein intakes in critically ill patients M.A. Valizade Hasanloei a, D. Vahabzadeh b, *, A. Shargh c, A. Atmani d, R. Alizadeh Osalou a a
Emam Khomeini University Hospital, GICU Unite, Urmia University of Medical Sciences, Iran Maternal and Childhood Obesity Research Center, Urmia University of Medical Sciences, Iran Evaluation and Accreditation Office, Vice-chancellor of Clinical Affairs, Urmia University of Medical Sciences, Iran d Seyyed al shohada University Hospital, Urmia University of Medical Sciences, Iran b c
a r t i c l e i n f o
s u m m a r y
Article history: Received 2 December 2015 Accepted 17 October 2017
Background & aims: Providing adequate and appropriate food and nutrients satisfying the patients' safe nutritional need is one of the most important care practices for critically ill patients (CIPs) in ICU settings, and is strongly related to the patients' safety. Methods: In this prospective cross-sectional study data were collected from a 52-bed medical intensive care unit on 777 consecutive patients in six different ICUs. The patients' weights and heights were measured based on ulna length, knee height, MAC, Calf C, and Wrist C. Also, patient weight change history was asked for. All currently in-use dietary supplements and formulas in the ICU settings were checked for their ingredients. The patients' nutritional need was calculated individually for the disease state based on dietary ESPEN guidelines. Results: Mean ICU and hospital stay duration was 14.45 ± 11.81 and 15.38 ± 11.88 days respectively. Mean energy and protein requirements in the target population were 1804.61 ± 201.76 Kcal/day and 77.94 ± 12.72 gr/day, respectively. Mean actual energy and protein intakes were 1052.75 ± 561.25 Kcal/ day and 35.38 ± 23.19 gr/day, respectively. Satisfaction percents for mean energy and protein requirement in the total population were 58.34% (1052.75/1804.4) and 45.41% (35.38/77.9), respectively. In 21.4% and 4.4% of the studied group, energy and protein intakes were about 75e100% of the patients' actual need, respectively. Another data analysis for patients with over 10 days of inpatient time showed that only 14.2% of patients had energy intakes, and only 3.2% of them had protein intakes in the range of 75 e100% of their requirements. Conclusion: Results showed that energy and protein intakes in CIPs are low, disproportionate to their requirements. Therefore, actual dietary intake records, individual dietary requirement calculation, and individual dietary planning in relation with the patients' disease and stress should be considered. Such an accurate nutritional care process can promote patient safety. © 2017 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
Keywords: Energy intake Protein intake Intensive care unit Critically ill patients
1. Introduction ICU patients are often hypermetabolic, which can cause malnutrition [1e3]. Malnutrition is associated with mortality in these patients. One important unanswered question that has recently become more prevalent in the critical care literature is
* Corresponding author. Mother and Child Obesity Research Center, Research and Technology Institute, Kashani Street, PO Box: 5713613331, Urmia, Iran. Fax: þ98 4432253307(12). E-mail address:
[email protected] (D. Vahabzadeh).
regarding the dosage or amount of nutrition. There is a general consensus that excessive hypocaloric or hypercaloric feeding should be avoided, yet there is controversy about what the feeding target should be [3e5] (see Tables 1and 2). Delivering food and nutrients for an optimal nutrition according to the patients' needs through one of the possible routes such as enteral (EN) or parenteral (PN) in critically ill patients (CIPs) is a cornerstone for intensive care practice. CIPs that do not receive enough nutrients through oral feeding should be prepared for EN or PN nutritional support [6e8].
https://doi.org/10.1016/j.clnesp.2017.10.007 2405-4577/© 2017 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Valizade Hasanloei MA, et al., A prospective study of energy and protein intakes in critically ill patients, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.007
e2
M.A. Valizade Hasanloei et al. / Clinical Nutrition ESPEN xxx (2017) e1ee5 Table 2 Mean actual energy and protein intakes and requirements.
List of abbreviations BMI LOS GRV CVA GICU NICU SICU MICU ICU MAC Calf C GCS EN PN ESPEN CIPs
Body Mass Index Length of Stay Gastric Residual Volume CerebroVascular Accident General Intensive Care Unit Neurological Intensive Care Unit Surgical Intensive Care Unit Medical Intensive Care Unit Intensive Care Unit Mid Arm Circumference Calf Circumference Glasgow Coma Score Enteral Nutrition Parenteral Nutrition European Society for Enteral and Parenteral Nutrition Critically Ill Patients
Variable (measure)
Mean ± SD
P value
Actual energy intake (Kcal/day) Energy requirement (Kcal/day) Actual protein intake (Kcal/day) Protein requirement (Kcal/day)
1052.75 ± 561.25 1804.61 ± 201.76 35.38 ± 23.19 77.9 ± 12.72
P < 0.001 P < 0.001
Recently, guidelines have suggested that starting EN within 24 h of ICU admission is important for patients with hemodynamically stable conditions [15e17]. Most methods used for the calculation of energy requirement in ICU patients include Harris Benedict formula, indirect calorimetry, and guidelines based on established recommendations [16e19]. Different observational studies have revealed that although there are different cut-offs in rules for defining nutritional intakes as sufficient or insufficient, most intakes are much lower than the patients' requirements [11,14]. 2. Material and methods 2.1. Study design
There is a general agreement that EN is preferable to PN for nutritional support [7]. EN is associated with fewer side effects and discomforts, such as a lower infection incidence rate and lower length of hospital stay and costs [8,9]. The problem is the impossibility of satisfying all patients' needs with EN most of the times [10,11]. Patients with long ventilator dependence are frequently susceptible to over- and under-feeding because there are frequent impeding factors such as GI intolerance, frequent tube feeding interruptions, and the need for diagnostic tests or procedures. A high gastric residue volume (GRV), vomiting, nausea, ileus, bloating and diarrhea are the most common GI discomforts [12,13]. Different studies have revealed that low calorie and protein intakes, mostly less that 70% of the patients' requirements, can be related to unfavorable clinical outcomes. Unfortunately in most cases the delivered amount of nutrition is not sufficient [12e14]. Table 1 Demographic and baseline characteristics of patients. Variable (measure)
Value
Age (mean ± SD) Sex (n, percent)
61.32 ± 18.85 Female: 46.66% Male: 53.33% 62.66 ± 12.20 167.59 ± 11.80 24.75 ± 5.22 29.87 ± 5.94
Weight (means ± SD) Height (means ± SD) Mid Arm Circumference (mean ± SD) Calf Circumference (mean ± SD) BMI Category (n, percent) 18.49 18.5e24.9 25e29.9 30e34.9 35e39.9 40 Type of feeding rout (n, percent) Oral EN PN Mixed Types of EN route (n, percent) NG PEG PEJ Ventilator Dependence Yes No Length ICU stay (mean ± SD)
20.1% 53.1% 20.2% 5.7% 0.6% 0.1% 14/4% 68.2% 7.5% 9.9% 94.2% 4.3% 1.5% 62.9% 37.1% 14.45 ± 11.81
This study conducted as a prospective observational study from February 2012 to October 2014. Patients were recruited from 6 different ICUs including GICU, NICU, SICU, MICU, and stroke and post-surgery ICU from Imam Khomeini educational hospital, Urmia, Iran. Study performed after inspection by Medical Ethics Committee of the Urmia University of Medical Sciences about any possible ethical issues. 2.2. Participants 1183 adult CIPs, 18 years or older, who had been admitted to the 6 different ICUs were screened for eligibility. Inclusion criteria were being over eighteen years old, over a 4-day stay in ICU, receiving at least one type of feeding (Oral, EN, and PN) or their combination. Participants were consecutive patients who had entered ICU and stayed for more than 96 h with feeding having been started in the first 72 h of admission, from February 2012 to October 2014. From the target population, 20.03% (237) died, 6.08% (72) with a GCS equal or less than 3, 3.88% (46) had less than 4 days of LOS, and 4.31% (51) had a delayed feeding initiation (feeding starting after the 4th day), and thus were excluded from study. Therefore, finally 777 participants were included. 2.3. Data collection and measurements Data about familial, medical and drug history, and laboratory test results were extracted from the patients' medical records. Anthropometric and delivery data were collected by direct measuring or were extracted from medical records which had been recorded by nurses or registered dietitians. The patients' heights were measured by ulna length measurement, and then their ideal body weights were computed. Body sizes were determined after wrist circumference measurement. For predicting their current body weight, the most recent body weight history was asked from the patients' surrogates, and also estimation was performed by Krandal and Lorenzo weight prediction formulas for CIPs. Mid arm muscle circumference (MAC) and calf circumference (CC) for each patient was measured and recorded in an specifically provided nutritional form. Evaluation of the patients' malnutrition status was conducted based on their body mass index (BMI). After height and weight prediction, patients'
Please cite this article in press as: Valizade Hasanloei MA, et al., A prospective study of energy and protein intakes in critically ill patients, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.007
M.A. Valizade Hasanloei et al. / Clinical Nutrition ESPEN xxx (2017) e1ee5
calorie and protein requirements were calculated based on ESPEN (European Society for Parenteral and Enteral Nutrition) guideline recommendations. 2.4. Estimated intakes and requirements Based on ESPEN guidelines, during the first 24 h of patient admission, feeding should be initiated using a standard highprotein formula [17]. Within the acute and initial phases of critical illness, an exogenous energy supply in excess of 20e25 kcal/kg/ day based on the ideal body weight (IBW) should be avoided, whereas during recovery, the aim should be providing values as much as 25e30 kcal/kg/day. Protein requirements have been adjusted at 1.2e1.5 gr/kg/day for most CIPs based on their condition and underlying disease [17]. Therefore, based on the abovementioned recommendations, we calculated energy and protein requirements. Calculation was performed for each participant in different values according to the date of assessment. Fluid requirement was estimated based on 1 cc/kcal for each patient. For the assessment of hand-made hospital formulas, samples were taken from hospital hand-made formulas (gavages) and analyzed for their composition, mainly based on energy, carbohydrate, protein and fat content. All currently in-use dietary supplements and formulas in ICU settings were checked for their ingredients. Intakes through all feeding routes were calculated. In this study, intake levels equal to or greater than 75% of the patients' requirements were considered adequate. 2.5. Data analysis Data analysis was performed by SPSS 21 for Windows. P values equal to or less than 0.05 were considered as the level of significance. Descriptive statistics were used to examine the characteristics of patients. Paired sample t-tests and independent samples ttests were used to determine the difference between patients' intake and requirements in each evaluation session. 3. Results There were 777 eligible patients included in the study during the two-year study interval. Mean age in the target population was 61.32 ± 18.85 years; 53.33% were men and 46.66% were women. Among these participants, 26.38% (205) were traumatic, 20.84% (162) had respiratory dysfunctions, 20.07% (156) had different types of cancer, 19.30% (150) had CVA, and 13.38% (104) suffered from other disorders. Among the patients studied, 68.2% received EN, 7.5% received PN, 9.9% received feeding via mixed routes, and 14.4% via oral feeding. Mean length of ICU and hospital stay was 14.45 ± 11.81days (range: 1e180 days) and 15.38 ± 11.88 days (range: 3e116 days), mean mechanical ventilation was 11.24 ± 3.18 days. Mortality rate was 25.2% (196 from 777 subjects) for the entire period of the study. In the time of nutritional assessment, 62% of eligible patients were in the 10th day of their admission, 10% were in the 7e10th day, and 21% were in the 4e7th day. Mean actual energy intake for the study population was 1052.75 ± 561.25 Kcal/day, while the mean energy requirement was 1804.61 ± 201.76 Kcal/day, based on patients' stress and bedridden time period. Comparison of the means showed a significant difference between actual energy intakes and requirements (P < 0.001). Mean actual protein intake and requirement were 35.38 ± 23.19 gr/day and 77.9 ± 12.72 gr/day respectively, and the analysis for comparing these means for protein showed a significant difference (P < 0.001).
e3
Table 3 Percent of energy satisfaction in categories based on different length of ICU staying. Energy satisfaction category
Time (days)
1e3 3.1e7 7.1e10 >10
Total
Total
0-50%
50.01e75%
75.01e100%
>100%
5.6% 7.9% 4% 20.5% 38%
0.9% 5.2% 3.4% 22.9% 32.3%
0% 5.9% 1.3% 14.2% 21.4%
0% 1.9% 1.3% 5% 8.3%
6.5% 20.9% 9.9% 62.7% 100%
Table 4 Percent of protein satisfaction in categories based on different length of ICU staying. Protein satisfaction category
Time (days)
1e3 3.1e7 7.1e10 >10
Total
Total
0-50%
50.01e75%
75.01e100%
>100%
4.7% 12.8% 6.2% 35.9% 59.6%
0.9% 6.3% 2.8% 19.3% 29.8%
0% 0.9% 0% 3.2% 4.4%
0% 0.9% 1% 4.3% 6.2%
6.5% 20.9% 10% 62.7% 100%
Data showed that satisfaction percents for mean energy and protein requirement in the total population were 58.34% (1052.75/ 1804.4) and 45.41% (35.38/77.9), respectively. Subgroup analysis showed that in 21.4% and 4.4% of the studied group, energy and protein intakes were about %75e100 of the patients' actual need, respectively. Finally, another data analysis was conducted for patients with over 10 days of inpatient time. Data from this analysis showed that only 14.2% of patients had energy intakes, and 3.2% had protein intakes in the range of 75e100% of their requirements (Tables 3 and 4).
4. Discussion Although nutritional assessment in critically ill patients is difficult and time-consuming, it is necessary for providing a safe and appropriate medical nutrition therapy in conjunction with pharmaceutical treatment [6,12]. To achieve this goal, intermittent and continuous nutrition monitoring during ICU stay has been recommended [12,15]. Most feeding protocols recommend gradually increasing the nutrition over the first several days of ICU stay, specifically starting enteral feeding in the first 24 h of ICU admission, or ideally 72e96 h after admission for an effective intensive care [15e17]. The latter has been highly recommended by the more recent published studies and evidence-based guidelines [19e21]. The present prospective and observational study was conducted in an educational hospital of Urmia University of Medical Sciences, Iran. 1183 critically ill patients in need of full or partial nutritional support were recruited from six different 52-bed ICUs. In this study, patients' calorie and protein requirements and actual intakes were recorded or calculated individually, and therefore comparisons were made for evaluating the level of insufficiency. After excluding a number of cases based on exclusion criteria, 777 eligible patients were entered into the two-year study interval (from February 2012 to October 2014). Patients' mean age was 61.32 ± 18.85 years, with 53.33% men and 46.66% women. There are different methods for energy need calculation or prediction, as indicated by different studies. Harris Benedict (HB) equation, indirect calorimeter, and evidence-based guideline recommendation are the most used methods in different studies [16e19,22]. In addition, for calculating the protein needs, there are recommendations based on the percent of total daily energy requirements or per kilograms of body weight [23e26]. We used
Please cite this article in press as: Valizade Hasanloei MA, et al., A prospective study of energy and protein intakes in critically ill patients, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.007
e4
M.A. Valizade Hasanloei et al. / Clinical Nutrition ESPEN xxx (2017) e1ee5
ESPEN guideline recommendations for energy and protein daily requirement calculations in this study [17], because these guidelines are in prior for use by our dietitians in ICU settings, because of easily and practically nutritional care providing by them. There was no access to indirect calorimeter in our hospital settings, and HB equation overestimates energy requirement in most cases. Because of this overestimation, physicians do not accept calorie prescriptions by this formula. They believe that the prescribed amounts are high and should be reduced. Similar results have been presented in previous studies [9,20]; thus, we used ESPEN guideline recommendations for our study population. Similar studies have conducted such requirement calculations according to evidencebased guidelines or protocols [19,25]. In this study, we made a comparison between average daily amount of energy and protein requirements and actual daily intakes. Similar studies had made such comparisons before [9,11]; however, in several studies, daily requirements, prescribed, and administrated amounts had been evaluated and compared [18,27]. A combination of these three comparisons has provided different study protocols, as seen in the literature. Different levels have been defined as cut-offs for determining sufficiency or insufficiency of intake. In a number of studies, intakes equal to or more than 90% of the patient's requirement have been considered as sufficient [2,9,27]. Other studies have considered 60% of the patient's requirement, and in others 75% or greater amounts of requirement have been determined as sufficient [3,5]. These levels have been either too strictly or loosely defined in many studies. For example, in studies by Isidro et al. and Binnekade et al., intakes equal to or more than 90% of the patient's requirement have been considered as sufficient; on the other hand, the least amount has been presented as a borderline for preventing clinical unfavorable outcomes such as infection [19]. In the present study, we considered intake levels equal to or greater than 75% of the patient's requirement as adequate. Another reason for our definition comes from previous studies. Several studies have indicated that a low-calorie intake in ICUs is associated with better clinical outcomes [1], whereas others have demonstrated that higher energy intakes can be related to more favorable results [14,27]. Hence, based on the data from the most recent studies, intakes equal to or more than 60% of the patient's daily requirement were defined as the cut-off for detecting the level of adequacy [5,28]. Unlike most other studies that have evaluated daily intakes in a short period of time or during a specific time of ICU stay [8,9,11], we evaluated patients' daily intakes in different times and intervals, in accordance with ICU length of stay. As a result, we believe that the results of this study can provide a better estimation of CIPs' intakes and can be used with more confidence than those of other studies. This study was conducted with a relatively desirable power in comparison with others [11,20,27] because of its relatively larger sample size. Many studies have smaller sample sizes than ours, but there are also a few studies with larger sample sizes [7,14]. The present study, in line with others [11,14], revealed that in spite of increasing the intakes with increasing the length of ICU stay and the patients' stabilization, there are still inadequate intakes in energy and protein in most cases. In sum, based on the results of this and other studies, we can conclude that protein and energy intakes are lower than the requirement, and are low in the majority of cases, specifically for protein. This can counteract other therapeutic activities and confound the goal of ICU care promotion. Thus it is necessary to use evidence-based guidelines and specified protocols, and setting rules by governmental policy makers in the hospital settings. Moreover, there is still a need for designing good clinical trials for deciding on the suitable daily requirements of protein and energy
for obtaining better clinical outcomes with nutritional practice in intensive care units. Statement of authorship Valizade Hasanloei MA was instructor, program manager, study supervising physician, Vahabzadeh D participated in data collection, dietary assessment, patients individual requirement calculation, and drafting the manuscript. Shargh A participated in Staff and official coordination for their co-working. Atmani A took part in data extraction and collection, data entering and preparation for analysis. Alizadeh Osalou R collaborated in cooperating ICU staff and residents for their integrated tasks. All authors have been engaged in the final steps for manuscript submission. Funding sources This work has received no funding. Conflicts of interest Authors state that there are no conflicts of interest. Acknowledgments Researchers appreciate all the nurses, staff, and residents of Urmia Imam Khomeini Hospital in different ICU settings for their participation in this study. Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.clnesp.2017.10.007. References [1] Krishnan JA, Parce PB, Martinez A, Diette GB, Brower RG. Caloric intake in medical ICU patients: consistency of care with guidelines and relationship to clinical outcomes. Chest J 2003;124(1):297e305. [2] Binnekade J, Tepaske R, Bruynzeel P, Mathus-Vliegen E, De Hann R. Daily enteral feeding practice on the ICU: attainment of goals and interfering factors. Crit Care 2005;9(3):R218e25. [3] Peterson SJ, Tsai AA, Scala CM, Sowa DC, Sheean PM, Braunschweig CL. Adequacy of oral intake in critically ill patients 1 week after extubation. J Am Dietetic Assoc 2010;110(3):427e33. [4] Stapleton RD, Jones N, Heyland DK. Feeding critically ill patients: what is the optimal amount of energy? Crit Care Med 2007;35(9):S535e40. [5] Tsai J-R, Chang W-T, Sheu C-C, Wu Y-J, Sheu Y-H, Liu P-L, et al. Inadequate energy delivery during early critical illness correlates with increased risk of mortality in patients who survive at least seven days: a retrospective study. Clin Nutr 2011;30(2):209e14. [6] Griffiths R, Bongers T. Nutrition support for patients in the intensive care unit. Postgrad Med J 2005;81(960):629e36. [7] Heyland DK, Cahill NE, Dhaliwal R, Sun X, Day AG, McClave SA. Impact of enteral feeding protocols on enteral nutrition delivery results of a multicenter observational study. J Parenter Enter Nutr 2010;34(6):675e84. [8] Petros S, Engelmann L. Enteral nutrition delivery and energy expenditure in medical intensive care patients. Clin Nutr 2006;25(1):51e9. [9] O'Leary-Kelley CM, Puntillo 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):222e31. [10] Casaer MP, Mesotten D, Hermans G, Wouters PJ, Schetz M, Meyfroidt G, et al. Early versus late parenteral nutrition in critically ill adults. N Engl J Med 2011;365(6):506e17. [11] Kim H, Stotts NA, Froelicher ES, Engler MM, Porter C. Enteral nutritional intake in adult Korean intensive care patients. Am J Crit Care 2013;22(2):126e35. [12] McClave SA, Martindale RG, Vanek VW, McCarthy M, Roberts P, Taylor B, et al. Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill patient: society of critical care medicine (SCCM) and American society for parenteral and enteral nutrition (ASPEN). J Parenter Enter Nutr 2009;33(3):277e316. [13] Arabi Y, Haddad S, Sakkijha M, Al Shimemeri A. The impact of implementing an enteral tube feeding protocol on caloric and protein delivery in intensive care unit patients. Nutr Clin Pract 2004;19(5):523e30.
Please cite this article in press as: Valizade Hasanloei MA, et al., A prospective study of energy and protein intakes in critically ill patients, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.007
M.A. Valizade Hasanloei et al. / Clinical Nutrition ESPEN xxx (2017) e1ee5 [14] Alberda C, Gramlich L, Jones N, Jeejeebhoy K, Day AG, Dhaliwal R, et al. The relationship between nutritional intake and clinical outcomes in critically ill patients: results of an international multicenter observational study. Intensive Care Med 2009;35(10):1728e37. [15] Singer P, Anbar R, Cohen J, Shapiro H, Shalita-Chesner M, Lev S, et al. The tight calorie control study (TICACOS): a prospective, randomized, controlled pilot study of nutritional support in critically ill patients. Intensive Care Med 2011;37(4):601e9. [16] Weijs PJ, Stapel SN, de Groot SD, Driessen RH, de Jong E, Girbes AR, et al. Optimal protein and energy nutrition decreases mortality in mechanically ventilated, critically ill patients a prospective observational cohort study. J Parenter Enter Nutr 2012;36(1):60e8. [17] Kreymann KG, Berger MM, Deutz NEP, et al. ESPEN Guidelines on Enteral Nutrition: Intensive care. Clin Nutri 2006;25:210e23. P, Mattens S, Rose T, Huyghens L. Bedside [18] De Waele E, Spapen H, Honore calculation of energy expenditure does not guarantee adequate caloric prescription in long-term mechanically ventilated critically ill patients: a quality control study. Sci World J 2012;2012. [19] Rubinson L, Diette GB, Song X, Brower RG, Krishnan JA. Low caloric intake is associated with nosocomial bloodstream infections in patients in the medical intensive care unit*. Crit Care Med 2004;32(2):350e7. [20] De Jonghe B, Appere-De-Vechi C, Fournier M, Tran B, Merrer J, Melchior J-C, et al. A prospective survey of nutritional support practices in intensive care unit patients: what is prescribed? What is delivered? Crit Care Med 2001;29(1):8e12. [21] Heyland DK, Murch L, Cahill N, McCall M, Muscedere J, Stelfox HT, et al. Enhanced protein-energy provision via the enteral route feeding protocol in
[22]
[23] [24]
[25]
[26] [27]
[28]
e5
critically ill patients: results of a cluster randomized trial*. Crit Care Med 2013;41(12):2743e53. Zusman O, Theilla M, Cohen J, Kagan I, Bendavid I, Singer P. Resting energy expenditure, calorie and protein consumption in critically ill patients: a retrospective cohort study. Crit Care 2016;20(1):367. Hoffer LJ, Bistrian BR. Appropriate protein provision in critical illness: a systematic and narrative review. Am J Clin Nutr 2012;96(3):591e600. van Schijndel RJS, Weijs PJ, Sauerwein HP, de Groot SD, Beishuizen A, Girbes AR. An algorithm for balanced protein/energy provision in critically ill mechanically ventilated patients. e-SPEN, Eur e-Journal Clin Nutr Metabolism 2007;2(4):69e74. Allingstrup MJ, Esmailzadeh N, Knudsen AW, Espersen K, Jensen TH, Wiis J, et al. Provision of protein and energy in relation to measured requirements in intensive care patients. Clin Nutr 2012;31(4):462e8. Weijs PJ, Wischmeyer PE. Optimizing energy and protein balance in the ICU. Curr Opin Clin Nutr Metabolic Care 2013;16(2):194e201. ~o calo rico-proteica da terapia nutricional Isidro MF, Lima DSCd. Adequaça dica Brasileira enteral em pacientes cirúrgicos. Revista da Associaç~ ao Me 2012;58:580e6. Martindale RG, McClave SA, Vanek VW, McCarthy M, Roberts P, Taylor B, et al. Guidelines for the provision and assessment of nutrition support therapy in the adult critically ill patient: society of critical care medicine and American society for parenteral and enteral nutrition: executive summary*. Crit Care Med 2009;37(5):1757e61.
Please cite this article in press as: Valizade Hasanloei MA, et al., A prospective study of energy and protein intakes in critically ill patients, Clinical Nutrition ESPEN (2017), https://doi.org/10.1016/j.clnesp.2017.10.007